Worm Control for Small Ruminants in Tropical Asia

113

Worm Control for Small Ruminants in Tropical Asia ACIAR

Worm Control for Small Ruminants in Tropical Asia
Editors: R.A. Sani, G.D. Gray and R.L. Baker

Australian Centre for International

Agricultural Research 2004
 The Australian Centre for International Agricultural Research © Australian Centre for International Agricultural Research
(ACIAR) was established in June 1982 by an Act of the GPO Box 1571, Canberra, Australia 2601.
Australian Parliament. Its primary mandate is to help identify www.aciar.gov.au
agricultural problems in developing countries and to email: [email protected]
commission collaborative research between Australian and
developing country researchers in fields where Australia has Sani R.A., Gray G.D., and Baker R.L. 2004
a special research competence. Worm Control for Small Ruminants in Tropical Asia
ACIAR Monograph 113
Where trade names are used this does not constitute
Worm control for small ruminants in tropical Asia

endorsement of nor discrimination against any product

ISBN 1 86320 471 7 (print)
by the Centre.
1 86320 472 5 (electronic)

Technical editing: Keith Binnington,

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This series contains the results of original research Design and layout: Design One Solutions
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ii
Foreword
Sustainable technologies for the control of worm The three objectives of the project were: to prevent the
parasites of goats and sheep in the tropics have been spread of resistance to anthelmintics (dewormers) used
developed through a series of international research for control of nematode parasites of sheep and goats in
projects, several of which have been supported Asia; to assess genetic variation in resistance to gastro-
by ACIAR. intestinal nematode parasites in different breeds of
sheep and goats; and to disseminate information
ACIAR funded a collaborative project between research
about control of internal parasites in the tropics.
organisations in Southeast Asia for ILRI and regional
partners to explore new ways to control helminth parasites This publication and the accompanying CD draw
in the tropics. The project aimed to increase small together information from a number of sources to
ruminant production in Southeast Asia by controlling describe the state of research and development
internal parasites, which are one of the major constraints on worm control in sheep and goats in Asia and
to sheep and goat production in the tropics. Control of the Pacific.
internal parasites also provides an avenue for general
This publication can also be downloaded from
improvement in husbandry methods.
the ACIAR website: www.aciar.gov.au.

Peter Core
Director
Australian Centre for International Agricultural Research

iii
iv
Worm control in small ruminants in tropical Asia
Contents

Preface and Acknowledgments 1 8. Worm control for small ruminants

in the Philippines G.D. Gray et al 121
1. Worm control for small ruminants in
9. Worm control for small ruminants
Southeast Asia R.A. Sani and G.D. Gray 3
in Indonesia Subandriyo, Tetty Sartika,
Suhardono and G.D. Gray 151
2. The economic impact of worm infections
in small ruminants in Southeast Asia,
10. Worm control for small ruminants
India and Australia R.S. McLeod 23
in Malaysia R.A. Sani, M. Adnan,
T.S. Cheah and P. Chandrawathani 189
3. Developing and testing integrated
approaches to sustainable parasite
11. Worm control for small ruminants in Thailand
control in small ruminants with farmers
S. Kochapakdee and S. Saithanoo 201
in the Philippines, Vietnam, and
Indonesia A.M.P. Alo 35
12. Goat production, parasites and testing
of control options in Lao, Cambodia
4. Anthelmintic resistance in small ruminant
and Vietnam R.A. Sani, Dinh Van Binh,
parasites: implications for smallholders
Nguyen Duy Ly, Sorn San and Viengsavanh
in Southeast Asia G.M. Hood 51
Phimphachanhvongsod. 211
5. Appropriate breeds and breeding
13. Worm control for small ruminants in Fiji
schemes for sheep and goats in the
P. Manueli 219
tropics R.L. Baker and G.D. Gray 63

14. Internal parasites of small ruminants

6. Options to overcome worm infection
in Papua New Guinea B.R. Joshi 241
for small ruminant producers in Nepal
R. K. Bain, B. R. Joshi, D. Gauchan
15. Internal parasites of small ruminants
and G. D. Gray 97
in Nepal B.R. Joshi 249
7. The impact of parasitism on the
development of small ruminant populations Appendix – list of authors 263
in Southeast Asia G.M. Hood 113

v
vi
Worm control for small ruminants in tropical Asia
Preface and Acknowledgments
The chapters in this volume were written originally that efforts to develop new approaches to worm
between 1999 and 2001 to support the efforts control, develop new technologies, and adapt existing
of projects being implemented by the International technologies, would be strengthened by making this
Livestock Research Institute with partners in Asia store of knowledge and experience available to the
and Australia. Now updated, and together with the project partners and their research teams. This has
accompanying CD, they describe information which, been done within the project by publishing the early
at the beginning of the projects, we believed was versions of these chapters and internal documents
lacking or incomplete because much of the research and circulating electronic versions on CD. As these
on parasite control in small ruminants in our partner initial projects drew to a close in 2003, it was timely
countries was not readily available. The difficulties to gather them in a single volume.
of publishing applied research of local importance
The chapters vary in style and content reflecting
in international media are widely acknowledged.
the different needs of the partner countries and the
If published, it is often in national journals and, quite
amount of information available. In a few cases,
appropriately, in the national language of the country
some original research is described briefly. Although
where the work has been carried out. However, local
being published formally here, the work is ongoing,
publication denies the authors the opportunity to have
and updates will be available electronically through
their work reviewed by peers in the international
the authors and the project website which can be
scientific and development community and denies
accessed via ILRI at www.ilri.org or directly at
regional and international readership access to the new
www.worminfo.org.
research. When an international journal editor returns
a well-written paper to its author commenting that The assessment of the the importance of small ruminants
‘the topic is not of sufficiently wide interest to our and the needs for parasite control in Nepal (Chapter 6)
readership’, that is often accurate and understandable was undertaken against a background of substantial
as most paying subscribers will be in Europe or North research of sheep and goats in Nepal, principally by
America, but little comfort to millions of farmers, scientists based at the Lumle and Pakhribas research
thousands of extension workers and hundreds of centres. That research is reviewed in Chapter 15.
scientists whose livelihoods in the tropics are either
The accompanying CD contains all these chapters and
constrained or occupied by the problems of worm
many other tools and resources to assist those with an
control.
interest in worm control. The immediate beneficiaries
Supporting information was therefore a priority for the will be researchers about to embark on a new research
projects which funded this collection of ‘grey’ literature project, extension or development workers trying to
that is ‘not cited internationally’. Our rationale has been solve immediate parasite problems or develop local

1
 control strategies, and teachers of animal, veterinary advocate of applied research to benefit poor farmers.
and extension science who will benefit from a more ACIAR contributed much to the earlier research being
complete approach to worm control than provided by summarised here, notably in Indonesia, Malaysia and
the lists of chemicals and parasites which dominate Fiji, and has contributed the funds to edit, publish and
the conventional literature. The final beneficiaries, of distribute this book and CD. Jenny Edwards provided
course, we expect to be the millions of poor livestock critical interpretation and skilful editing of many
keepers who depend on sheep and goats, those who chapters.
have no livestock but may use small ruminants as
a pathway to build some assets and income, and The names and institutions of those involved in these
subsistence farmers who may see the opportunity projects are reflected in the authorship and their
to expand their livestock farming to a more market- affiliations listed in the following pages. Missing,
oriented enterprise. however, are the hundreds of their collaborators and
the thousands of farmers across the region who have
The list of people and institutions to be acknowledged given up their time to answer questions, record data
is long and reflects the breadth of the partnerships that and travel hundreds of thousands of kilometres to create
have been developed and exploited to bring Better this information and knowledge. That they have done
Worm Control for Small Ruminants in Asia to the press. so reflects the importance they give to small ruminants
The logos of their institutions alone would occupy several as a source of livelihood in their communities and the
pages. Gathering and synthesising the information and degree to which helminth infections reduce the many
development of the decision support tool Goatflock is benefits that sheep and goats can provide. From this
a specific output of a project funded by the International publication, we hope that these constraints are better
Fund for Agricultural Development (TAG 443), where understood and that more people will find
Ahmed Sidahmed has provided critical support and
Worm control for small ruminants in tropical Asia

better ways of overcoming them.

insights into our efforts. That project has been
implemented in parallel with a project funded by the Rehana A. Sani
Australian Centre for International Agricultural Research G. Douglas Gray
(PN97133) where John Copland has been a staunch R. Leyden Baker

2
1. Worm control for small ruminants in Southeast Asia
R.A. Sani and G.D. Gray

Introduction
Two-thirds of the world’s poor live in Asia below in the context of rural poverty in Southeast Asia, to
nationally defined poverty lines and 479 million (65%) describe the vast majority of livestock keepers as being
of them are poor livestock keepers who derive a large engaged in the livestock sector, but rather that the
part of their household welfare from domesticated livestock sector is highly integrated into complex
animals (LID 1999, Thornton et al. 2003). In Southeast livelihoods based around multiple commodities and
Asia, the focus for this volume, the comparable figures sources of income. Livestock are an essential part of
are 161 m and 62 m (38%) with great variation existing systems and offer opportunities for high-value
between countries, between agroecological regions, production (IFAD 2002). This contrasts with temperate
and between communities with close or distant access to farming systems where farmers are often dedicated to
cities. Rural Southeast Asia is a group of countries with large-scale sheep or goat production. The parasites and
diverse cultures, economies and politics which is also hosts may be the same, but the nature of the problems
characterised by mixed farming systems. These systems caused by parasites and the options available for
are often described by their staple crop, eg rice, yam overcoming them are different and varied.
or maize, which is significant for the farming culture.
The rapidly changing patterns of demand for livestock
Nevertheless, with the possible exception of intensely and livestock products (dubbed the Livestock Revolution
irrigated farming systems, livestock are common to all by Delgado et al. 1999, and others) point to livestock
systems: poultry, small and large ruminants and pigs are production being an increasing component (at least in
ubiquitous and an essential part of the management value) of the agricultural economies of Southeast Asia.
of economic and natural resources. For example, at The extent to which the rural poor will benefit from these
the three project sites (described in Chapter 8) in the changes depends on how livestock can be integrated
Philippines, livestock are a major part of the village into developing markets, the potentially negative effects
economies, which are usually described as based of industrialised production in rural areas and whether
on rice, coconuts or fishing. Thus, it is not appropriate, cheaper livestock products benefit the rural poor as

3
 consumers as well as producers. There is scope for small This volume is arranged in two sections. The first section
ruminants to play an important role for smallholder describes some advances in techniques and in the
farmers in accessing these new markets. thinking behind worm control for smallholders in the
In Southeast Asia the dominant livestock species are humid tropics. Questions addressed include how to
large ruminants (cattle and buffalo), pigs and poultry. estimate the costs and benefits of control measures,
With the exception of Indonesia, goats and sheep are how to make best use of genetic variation in resistance,
relatively few. Their significance, however, which is now how to use computerised tools in assessing control
being exploited in several countries, is that they are small interventions, and how to use participatory approaches
livestock in high demand and can thrive on low inputs to help in devising sustainable control options.
and local resources. Their significance in South Asia is The second section includes separate chapters on
much greater and Chapters 6 and 15 on Nepal, with
published, ‘grey’ and some previously unpublished
reference to India in Chapter 6, are useful points of
information from Indonesia, Philippines, Nepal, Malaysia,
reference.
Thailand, Fiji and Papua New Guinea. Vietnam,
The focus of this volume is on small ruminant Lao and Cambodia are included in a single chapter
production, the effects that nematode parasites have as there has been little work on small ruminants in
on their productivity and ways of overcoming these these countries.
effects. In some chapters, ‘avoidance’ takes on more
The origins of this volume, and much of the work that
significance than ‘direct confrontation’. There are
is presented in it, lie in a workshop held in Bogor in
many technical ways to remove worms from goats and
sheep and make them grow better, the simplest being 1996, the proceedings of which were published by
drug treatment, and in conventional economic terms, ACIAR (Knox and LeJambre 1996). That workshop took
Worm control for small ruminants in Southeast Asia

these treatments are cost effective with a high return a very wide look at all the potential options available
on investment. Poor people, however, are not secure for worm control in the region and it is essential reading
enough (Wood 2003) to make this type of investment: for those who are interested in a more comprehensive
either they have higher priorities for cash-in-hand, they account of all possibilities. How much progress has been
are uncertain if their animals will survive, or they have made in the eight years since the Bogor workshop?
little confidence in when and how their animals will There certainly have been some technical advances,
be sold, and their price. Thus, any attempt to increase but as predicted at the workshop, no miracle drugs
goat and sheep production to benefit the poor must or vaccines have appeared on the world market.
address the wider reasons for the failure of the poor to A pessimistic view might be that the problems have
invest in technical solutions. This became increasingly worsened with increased resistance to anthelmintics.
obvious to the authors involved in the preparation of A more optimistic view is that there is wider
this volume and, as will be seen in several chapters, understanding of all the elements that contribute to
understanding and addressing social and market issues worm control: technical, social and economic, and
are highly significant.

4
that these need to work in harmony for the end point The breeds of sheep and goats available in the region
of worm control to be realised: improved livelihoods are described in each of the country chapters. There
for poor farmers from their sheep and goats. are many, and their origins are diverse, leading to
A key objective of this volume, and the accompanying a conclusion that there is sufficient diversity of genetic
CD, is to bring to a wider audience the treasure trove resources in the region to satisfy the genetic needs
of material in technical reports, in the so-called ‘grey’ of all possible small ruminant enterprises. The Indian
literature, and in journals which are not widely circulated subcontinent is the origin of most breeds but some,
and in languages not widely understood. The most such as the Barbados Blackbelly and Santa Ines sheep,
obvious example of this is in Indonesia where much and Boer goats, have been imported recently from
research on parasite control is published in Bahasa the Americas.
Indonesia. Subandriyo and colleagues have tried to both
summarise and translate many important publications
(Chapter 9).
This overview chapter will take the same path, by
singling out the control options and exploring their
potential contribution to worm control, examining
integrated approaches and finally considering the
potential for worm control as an entry point for
sustainable small ruminant production rather than an
isolated problem. This is preceded by a review and
discussion of the evidence for nematodes being an
important problem for sheep and goats and, very
briefly, a recap on the parasites and their hosts.

The parasites and their hosts

A wide range of parasites are found in sheep and goats
in Southeast Asia. They are mainly Haemonchus contortus
and Trichostrongylus spp., followed in prevalence by
Strongyloides papillosus, Oesophagostomum spp.,
Moniezia spp, Trichuris spp., Cooperia, the rumen and
Goats and sheep are often kept for food security and
pancreatic flukes, Bunostomum, Fasciola spp. and also
emergency sources of cash. (G.D. Gray)
Eimeria spp. The cooler climes of Nepal and North
Vietnam also host Teladorsagia and Nematodirus.

5
 The null hypothesis: controlling worms a starting point for the design of options for intervention.
The more critical cost and benefits, and those needed
is a waste of time and money by the agencies who will pay for them, are those of
the interventions themselves. The benefits of a single
Given the investments in parasite control in the last
intervention, for example improved grazing management
century, is it worth stepping back and reconsidering
to reduce mortality from nematodes, may have a much
the evidence for worms being a problem for sheep
wider benefit than simply ‘worm control’.
and goats in the tropics? Is it possible that investing
resources in the control of worms in sheep and goats
is not worth the effort, that these resources can be Effects of gastrointestinal nematodes
better invested elsewhere? Is it so obvious that parasites on production
constrain production and that public and private funds
Data from Southeast Asia is sparse. Comparison
should continue to be thrown at the problem? A premise
between parasitised and non-parasitised goats in two
of this entire volume and the basis of a significant section
villages in southern Luzon (Que et al. 1995) showed
of the pharmaceutical industry and the scientific that they differed in growth by several kilos over
community is that the benefits of removing gastrointestinal a period of six months, representing a good return
nematode worms from sheep and goats outweigh the on investment from a single dose of anthelmintic.
costs. In commercial large-scale production of small
ruminants with well-defined markets at least, the short-term Beriajaya and Copeman (1996) studied goats
costs and benefits are well understood. In smallholder and sheep on 50 farms in West Java, Indonesia to
production systems, this is far from the case. In part, investigate the seasonal effect of nematode parasitism
this is because the benefits of small ruminants are so on weight gain of recently weaned sheep and goats.
Worm control for small ruminants in Southeast Asia

many, for example, as assets, for weed control, and Weight gains of untreated animals were compared
as sources of fertiliser and security. These benefits are with those of an otherwise similar group treated
very difficult to quantify. But also there are very little data each two weeks with oxfendazole or albendazole to
on the effect on the more conventional parameters of suppress nematode parasitism. During the dry season,
value such as growth, mortality and offtake of meat, milk animals grew much faster than in the wet season and
and fibre, which themselves are often hard to value anthelmintic treatment had no effect on weight gains.
because of informal and non-metric markets, especially In the wet season, however, weight gains of both groups
in real farming systems outside the artificial confines of were lower and the effect of anthelmintic was to
research stations. These data are reviewed below, less increase growth rates in treated sheep by 25 per cent.
to provide an overall estimate of the effects of worms,
Pralomkarn et al. (1996) investigated the effects of
than to discuss the various ways of doing so. Having
internal parasites on growth rates of goats in village
reviewed this evidence, a case can be made for
environments in southern Thailand in a humid tropical
reducing the need for such estimates of loss, except as

6
climate and found the growth rates of goats drenched
every three weeks were significantly higher than for
those left undrenched and that drenching had most
effect on animals on a lower plane of nutrition.
The effects of parasitism are more obvious in losses
due to mortalities. In Malaysia, goat mortalities were
monitored closely in two studies. Among a flock of
grazing goats monitored from birth to 14 months of age
and not given dewormers, postmortem examination
showed deaths due to trichostrongyles were 32%
(Daud et al. 1991). Symoens et al. (1993) studied
13 goat smallholdings over 15 months and found
a mortality rate of 74% for animals up to one year
old and 34% adult mortality. Postmortem examination
confirmed the major causes of death as pneumonia
and haemonchosis.
Grazing sheep and goats are exposed to many threats
These first three studies illustrate several difficulties including dog attack. (D. Yulistiani)
in arriving at good and meaningful estimates of the
benefits of worm control. First, there is a need to The study by Que lasted six months and we do not
establish populations of animals which are free from know what happened to the animals after observation
worm infection. In each of the studies this was done ceased. Was there compensatory growth in the worm-
by anthelmintic treatment, which needs to be properly affected groups, as is often observed in on-station
applied using a fully effective chemical. In all cases the experiments? Third, criteria used for ‘effect’ in all the
chemical used was short-acting, lasting only a few days. experiments were growth rate and liveweight at the
The treated animals would therefore become infected end of the trial. The implication drawn from the trials
with larvae from the grazing they shared with non-treated was that this liveweight difference could be translated
animals within a week. In the case of the Indonesian into a financial loss by using a market price per kilo of
study, the chemical was given every fortnight which liveweight. No account is made of the timing of sale
would probably never allow adult worms to develop. (farmers often wait until an emergency or a particular
However, immature worms would certainly have season to sell animals) or the ability of the farmer to
been present. Thus, studies of this type will always get market price for the exact weight of the animal.
underestimate the worm effect when the control groups It is hard to know whether this over- or underestimates
are not free of infection. The second issue is timing. the effect of worms as the market value may be based

7
 on more qualitative traits such as ‘condition’ or ‘colour’. groups not treated with dewormer. As noted above, it
Certainly, no account is taken of the other attributes of is likely that these effects are underestimates because
the animals, such as manure production (likely to be of the short-term nature of the anthelmintic. Neither
depressed along with appetite in infected animals), or study recorded an effect of growth and only in goats
the costs of tending and young animals with diarrhoea. was there a reduction in liveweight gain. Was this
At face value it makes economic sense to spend money because of the different breeds used or the relatively
on a simple anthelmintic. Que estimated a benefit-cost low rainfall in the study areas? Of critical importance,
ratio of several hundred to one of doing so. But, by had offtake not been measured in these two studies,
and large, smallholder farmers do not treat their animals. it might have been concluded that worms had little or
There must be more to this than simple economics. no effect on production.
In this volume the economics of parasite control are In a similar type of long-term study, Thomson et al.
considered at the national (Chapter 2) and household (2000) measured offtake in Syrian sheep flocks and
(Chapter 4) levels. found such a small effect that it barely covered the
In south and central Asia and Africa more detailed cost of the dewormer. Presumably (but this is only
studies have been completed. In tropical Africa, two speculation) this is because of the dry environment and
comprehensive studies have been undertaken in Nigeria low worm challenge. Indeed, a scan of Table 1.1
(Osaer et al. 2000) and Senegal (Ankers 1998) might suggest that, as annual rainfall increases over
that also use anthelmintics to keep as many worms 10-fold from 300 mm in Syria to nearly 4 m in Java,
both the magnitude of loss increases and the nature of
as possible out of a control group of animals. These
loss changes: from offtake to reduced growth to high
studies were more comprehensive because they
Worm control for small ruminants in Southeast Asia

mortality. Had Pralomkarn, Que and Beriajaya and

measured many more animals (hundreds) over a longer
colleagues been able to measure offtake this hypothesis,
period (years) and many more traits. As the trials lasted
perhaps, could have been strengthened.
for more than one growing season, a key measurement
could be made — offtake. The engine-room of any Ghalsasi et al. (2002) addressed the difficulty of
livestock production system is the female of reproductive completely removing the worm population in a study
age and, if the main product is meat, the critical on the sheep flock in Maharashtra, India by using an
measures of engine efficiency are reproductive rate intraruminal capsule containing a macrocyclic lactone
and mortality rate. The more and heavier offspring which prevents incoming larvae form establishing. By
weaned and the sooner she becomes pregnant after comparing these animals with others treated every three
birth. the more efficient will be the herd or flock. Both months with ABZ and others untreated they were able
Osaer et al. and Ankers et al. measured very large to show that the infrequent treatment had no effect, but
reductions (26 and 46% respectively) in offtake in the by complete suppression of the worm population the

8
 Table 1.1 Summary of selected studies on the impact of gastrointestinal nematodes on production
of sheep and goats
Annual
Rainfall No. Effect on
Study Host (mm) N* Farms Dewormer Growth Mortality Offtake

Beriajaya and
Copeman 1996 Sheep 3,842 127 50 Monthly 25% None
Beriajaya and
Copeman 1996 Goat 3,842 96 50 Monthly 25% None
Que et al. 1995 Goat 2,100 39 2 4x 23% None
Pralomkarn et al. 1995 Goat 1337 24 1 4x 63% None
Ankers et al. 1998 Sheep 900 375 15 2x None None 26%
Osaer et al. 2000 Sheep 650 233 5 3x None None 24%
Osaer et al. 2000 Goat 650 385 5 3x None 6% 47%
Ghalsasi et al. 2002 Sheep 525 238 4 2x None None None
Ghalsasi et al. 2002 Sheep 525 238 4 Capsule None None 22%
Thomson et al. 2000 Sheep 300 432 10 2x None None 2%
*N: Number of adult sheep in stud

annual offtake per female in the flock increased by 22%. Sickness and death are what matter most
This raises a question for all the studies mentioned here; to smallholder farmers
had the worm population been completely suppressed,
would the effects have been even greater? In a series of, so far, unpublished studies in the
Philippines, Indonesia and Vietnam, smallholder goat
It is safe to conclude that worms do affect production and sheep farmers participated in discussion groups
in goats and sheep, that the effects are likely to vary which focused on the problems they faced. The leaders of
for many reasons, including those associated with the discussion groups were extensionists with backgrounds
geography, that most of the costs and benefits to in animal health and production and the discussions
smallholder farmers have not been included in estimates were organized in such a way that the starting points
and that the use of short-acting chemicals has led to were the most serious problems affecting the lives of the
underestimates of the true total impact of worm infections. farmers and their families. Not surprisingly these were

9
 often lack of income and lack of savings to deal with Reduce focus on absolute losses and
medical emergencies and education expenses. None of
increase focus on benefits from interventions
the farmers milk their goats or sheep and they described
the problems associated with them most often as ‘mortality The rationale of all these studies has been as a
of young’ and ‘sickness and diarrhoea’, especially during preliminary to designing effective options or control
the wet season. While it may be possible to interpret programs that minimise the impact of worms on
some of this sickness and death to parasitism, it is ‘production’ however narrowly or widely that is defined.
impossible to quantify how much without the long-term The options available to farmers now are: grazing
and detailed studies. For the smallholder farmers there management, improved nutrition, better housing and
are two important needs. The first is to address the water supply, better control of breeding and use of
problem in their terms — reducing mortality and signs chemical dewormers. With the exception of some
of sickness are obvious ways of doing this. Possibly dewormers, every one of these interventions has a much
more important, however, and hidden from the farmers, wider impact than just of worm infections. For example,
are the losses due to lost capacity to produce more using tree fodders to reduce intake of infective larvae
lambs and kids. Addressing the second problem requires also has an effect on the overall nutritional status of
a more prolonged effort by scientists and extensionists the animal, improving its resistance to infection and also
to provide information to increase awareness of the its growth and resistance to other diseases. Thus, the
potential gains. The initial outcomes of such an effort in overall benefits of any component of a control program
the Philippines are presented in Chapter 3 and a tool should consider the total range of benefits for production
for estimating the effects of reproduction using a computer and health. Likewise, removal of manure to prevent
model (Goatflock) is described in Chapter 7. re-infection around housing creates opportunities for
Worm control for small ruminants in Southeast Asia

Table 1.2 Control Options for Animal Diseases in Upland Villages of Lao PDR

Control Option and Likely Contribution to Successful Control

Improved Pens and Movement Chemical/Antibiotic

Disease Vaccination Clean Water Supply Control Treatment

Classical Swine Fever (CSF) ** * ** —

Fowl Cholera (FC) ** ** * —
Toxocariasis — — — ***
Haemorrhagic septicaemia (HS) * * * *
Source: ADB 2002; ***, complete control; —, no contribution to control.

10
applying the manure as fertiliser. Fodder trees can
improve rice yields through leaf fall into paddies.
Very quickly the estimate of benefits and attribution
of a particular intervention becomes complex and
beyond simple analysis of single factors and their
short-term effects.
An example of this approach is illustrated in Table 1.2
The most important diseases among pigs and large
ruminants in the uplands of Lao are classical swine fever
(CSF), fowl cholera (FC), toxocariasis and haemorrhagic
septicaemia (HS). While biologically these diseases are
quite distinct, the range of control options that might be
Counting worm eggs in faeces using flotation methods has
introduced for any one disease would have an effect
provided large amonts of clinical and epidemiological
on the others and lead to a decrease in the impact of
data. (G.D. Gray)
related groups of diseases, eg neonatal enteritis and
roundworms in pigs, roundworms of cattle and buffalo
(other than Toxocara) and coccidiosis in poultry. This is
quite apart from the increase in capacity required for the Control options
control of a single disease which would have flow-on Details of these options are contained in the country
effects across the extension service. chapters. This summary highlights the common practices
In summary, there remains the need for accurate and possibilities.
definition of the parasites that infect sheep and goats
and the direct impacts that they are having on easily Chemical control
measurable aspects of production. The more important
Most countries in Southeast Asia have all three of
effects, however, on reproduction rate, intermittent
the currently available broad-spectrum groups of
mortality and contribution to the farming systems and
anthelmintics, with benzimidazoles being the most
household economy are much more difficult to estimate.
widely used. Levamisole and macrocyclic lactones,
The most important question facing investors in livestock
in particular ivermectin, are used at levels directly related
health and production is how to allocate their resources
to the affluence of farmers, availability of government
and some of the interventions that can help control
subsidies and ease of availability. The narrow-spectrum
small ruminant parasites have wider benefits which
haemonchicide closantel is also available in a number
are not usually considered.
of forms, as a single chemical and in combination.
The extent of anthelmintic resistance has been estimated
in a number of ways.
11
 Use of chemical dewormers is an important option for
smallholders and other farmers. A study in East Africa
Nguti et al. (2002) – showed that under more extensive
grazing in a humid tropical system, 25% of the mortality
of young Red Maasai and Dorper sheep could be
attributed to parasites. Effective chemicals need not be
expensive and could be made widely available, but
their use is increasingly constrained by the emergence
of worms that are resistant to anthelmintic drugs, for
example in Malaysia (Dorny et al. 1993, 1994; Sivaraj
et al. 1994a, 1994b; Rahman 1993, 1994), Thailand
(Kochapakdee et al. 1995) and Indonesia (Dorny et al.
1995). In the Philippines, benzimidazole resistance
in a field population of Haemonchus contortus from
sheep has been confirmed in Mindanao (Van Aken et
al. 1994). Benzimidazoles have been in continuous
widespread use for up to 20 years in the Philippines
with little use of other chemical groups. Using an in Deworming chemicals can be highly effective if used
vitro larval development assay (LDA) in the Philippines correctly at the right time. (K.C. Patawaran)
the mean benzimidazole efficacy for goats was 82%
and for sheep was 62% (Ancheta et al. 2004). that anthelmintic resistance in parasites of small ruminants
Worm control for small ruminants in Southeast Asia

In Vietnam, deworming of goats is not a common in that country is rapidly increasing. It is perhaps fortunate
practice, with only 4–8% of farmers using chemical that most Asian countries with small ruminants have
dewormers because the cost is prohibitive. In that used mainly benzimidazoles. This has led to the fair
country an anthelmintic trial with goats on smallholder conservation of the broad-spectrum anthelmintics such
farms and on an institutional farm showed benzimidazole as levamisole and macrocyclic lactones, meaning they
efficacy of 70–80%, levamisole of 80–92% and can still be drawn upon if required. However, the cost
ivermectin of 75%. In south Thailand, benzimidazoles of such imported manufactured products can be the
failed to effectively reduce faecal egg counts while major limiting factor in their future usage. Chemical
levamisole was relatively effective and ivermectin dewormers are mainly manufactured for cattle and sheep
still effective. In Fiji, resistance to fenbendazole and the products or their dosages may not necessarily
and levamisole has been detected. Resistant worm be extrapolated for use in goats. Albendazole sustained
populations are emerging against the three main groups release capsules were not effective in goats but they
of anthelmintics in Malaysia, providing clear evidence are extremely effective in sheep in Fiji (Chapter 13).

12
Comparative pharmacokinetics of albendazole in sheep a system was proposed where farmers could form an
and goats revealed that the systemic availability of the association to make bulk purchases of anthelmintics,
drug was the same in both species but peak levels were which could be dispensed in smaller quantities
achieved earlier and fell off faster for goats, indicating according to flock size and also bought at discounted
a faster metabolic rate of albendazole in goats. prices (Misniwaty et al. 1996). The anthelmintic cost
Therefore, based on the disposition of ABZ metabolites as percentage of total revenue from selling fattened
in plasma, equivalent activity of ABZ in sheep and sheep is only about 3%. Hence, making anthelmintics
goats might be obtained by increasing the dose rate for available to farmers on a non subsidised free market
goats from 4.75 to 7.5 mg/kg, that is, 1.5 times the is viable (Scholz, 1992). Misniwaty et al. (1994) also
recommended dose for sheep (Hennessy et al. 1993). suggested that the most effective method of anthelmintic
In relation to this, Dorny et. al (1994) demonstrated distribution is an extension worker who is organized as
that closantel was active for a shorter time in Malaysian a supplier in a certain area. Apart from being a job
village goats than it is generally expected to be in sheep responsibilty, through this delivery network a certain
— at least 4 weeks at a dose of 7.5 mg/kg given income would be a motivating drive. The improvement of
orally. Thus, with a pre-patent period of 3 weeks for the delivery arm for anthelmintics would have an overall
H.contortus FECs in sheep would appear, at the earliest, general benefit in the distribution of other health tools
7 weeks after closantel administration. The period when such as antibiotics, vaccines and future approaches.
FECs reappeared after closantel administration (5 mg/kg
subcutaneously or 10mg/kg orally) in the village goats Given the pivotal role of anthelmintics in many worm
was 6 weeks. However, taking advantage of the control programs it is foreseen that their use will increase
sustained activity of closantel, which not only prevents in Asia. Therefore, it is imperative that animal health
reinfection but also resulted in a 72.5–86.8% lower workers be educated on the “do’s and don’ts” of
egg deposition on pasture during a 2-month period, anthelmintic use for the sustainable conservation
it is recommended that in Malaysia closantel be used of present-day drugs.
for strategic drenching alternately with broad-spectrum
anthelmintics. Improved nutrition
Given the opportunity, farmers would use anthelmintics Animals which are better nourished are better able to
as they perceive animals given these drugs to be fatter, withstand the effects of worm infection than those given
healthier and to have better appetites. So, for these a low plane of nutrition. Resistance of the animal to
reasons farmers are willing to invest in parasite control. larval establishment can be enhanced by improved
However, the reasons they don’t use anthelmintics are: protein nutrition (Sykes & Coop, 2001). In tropical
small flock sizes which makes purchasing large packets Asia, small ruminants rely mainly on grazing grass
of anthelmintics unviable; the cost of the drugs; and and forages which often have low nutritive value
their unavailability at the village level. In Indonesia and are given little or no protein supplementation.

13
 Increasing protein quantity and quality for animals from Beriajaya and Copeman (1996) suggest that as FEC
commercial sources may be a costly option. Therefore, were the same throughout the year it was the low levels
practices have focused on utilising locally available of nutrition during the wet season that affected the
feed resources such as tree leaves, farm by-products pathogenicity of gastrointestinal nematodes. Farmers
and cut forages. However, under grazing conditions, also realise the importance of supplementing their
there are no published studies which either directly animals’ diet. Dahlanuddin (2001) surveyed farmers in
or indirectly implicate nutritional status as having an Lombok, Indonesia and found that goats were offered a
impact on parasite levels in either sheep or goats. wide range of 30–40 different forages. Native grasses
and Sesbania grandiflora were mostly offered, as single
However, a report by Handayani and Gatenby
diets and, more often, as mixed diets. The latter, as well
(1988) investigated the interaction between system
as other tree leaves and agricultural byproducts, were
of management (grazing versus stall-feeding), nutrition
used even more during the dry season when native
(legume supplementation versus no legume) and
grasses were less available. The use of tree and
helminthiasis (with and without anthelmintic) in
shrub leaves reduces intake for ground-based and
sheep in North Sumatra. They concluded that legume
contaminated feeds. The highly nutritious Leucaena
supplementation reduced the egg count of grazing lambs
leucocephala was not used in some areas due to the
that were not given anthelmintic but the supplementation
temporary aversion by goats which farmers thought was
had no significant effect on mortality or growth rate.
permanent. Rice straw, although abundantly available,
The non-significant effect was probably due to the small
was not popular because goats rejected the straw.
sample size (four lambs per group). However, a closer
Preston’s work in Cambodia showed that diets for
look at the raw data revealed that there was a 50%
growing goats containing cassava foliage supported
reduction in mortality in the groups given the higher
Worm control for small ruminants in Southeast Asia

better growth and feed conversion, and exhibited

levels of legume supplementation compared to
protective mechanisms (presumably due to the content
unsupplemented lambs. Also, there was a trend
of condensed tannins in the cassava) against nematode
of 5–10 fold increase in growth rates among the
parasites than similar basal diets supplemented with
supplemented undrenched lambs. The existing worm
freshly cut grass. Dry matter digestibility was apparently
burden that was not removed at the start of the trial
depressed on the cassava, compared with the grass
had obliterated the benefits of legume supplementation
diets, but this negative nutritional effect appeared
in the untreated grazing group, which probably
to be more than compensated by the much higher
contributed to the high mortality rate of grazing lambs
protein intakes with cassava. Most goats in Vietnam
(38%). There was undisputably a very large effect of
grazed extensively on native grasses but only for about
anthelmintic treatment on survival and growth rate of
2 hours daily, which means that the animals do not eat
lambs that were given suppressive treatment.
sufficiently. Only 12–23% of farms there supplemented
with shrub and tree leaves such as Leucaena, jackfruit

14
and Flemingia. It is all very well to recommend
supplementing the animal diet with nutritious forages
but if these are not easily available, it is not an
option for the farmer. So, in these cases a simple
recommendation to allow the goats to graze for a
longer period may be more appropriate. Symoens
(pers. comm.) advised increasing the length of the
grazing period for goats in smallholder systems from
four to six hours, especially when the forage diet
is mainly grasses. This allowed an increase in the
quantity and quality of forages selected and ingested.

Ethnoveterinary therapy
Locally produced oral dewormers are used for worm
control by farmers and recommended by some animal
health workers. Plant remedies are often practised by
farmers not only as traditional panacea for good health
but also because modern anthelmintics may not be Spores from the free-living fungus Duddingtonia can
available or are too expensive. However, the use of prevent contamination of grass with worm larvae.
plant extracts as anthelmintics needs to be further (R.A. Sani)
investigated as there is a potential for their use in organic
particularly with less visible helminths. These refer to
and conventional production systems. Caution needs
the economically important helminths which are the
to be exercised when comparing results from different
trichostrongyles. In particular, papaya seed suspension
studies using plants, as the origin and preparation form
and papaya sap have been tried in several studies
of the plant may have differing efficacies against worms.
in vivo as well as in vitro with Haemonchus contortus
Most reports on apparent success of plants in eliminating infections and adult worms respectively and exhibited
visible endoparasites such as ascarids and tapeworms anthelmintic activity. However, two studies reported
need to be viewed with caution. They may well be on the toxicity of papaya sap causing some pathology
acting as laxatives and not strictly related to an of the gastrointestinal tract mucosa. Other plant extracts
anthelmintic effect. Few references exist to those were from nicotine, Areca catechu, Curcuma aeruginosa,
helminths which cannot be easily seen (Hammond et Zingiber purpureum, Monordica charantia and Morinda
al. 1997). In Indonesia there is a wealth of information citrifolia, all of which showed varying degrees of
on the use of medicinal plants in small ruminants, anthelmintic activity against H. contortus.

15
 Medicinal plants seem to be hugely popular with Biological control
ruminant farmers in the Philippines (Mateo, 1996).
Research on biological control using nematophagous
Several plants have been tested for their efficacy as
fungi as a new component for future integrated control
anthelmintics for goats in the Philippines. Crude extracts
of parasites of small ruminants has been ongoing for
of Mimosa pudica and Tinosphora rumphii were highly
about five years (Larsen 2002). In many areas of
effective against Haemonchus larvae in vitro and in
Southeast Asia this novel tool is particularly useful as
reducing worm egg counts and worm numbers (Faelnar
humidity and temperature are not limiting factors for
1997; Fernandez 1995). In Malaysia fresh leaves
the germination of fungal spores, which also applies
of neem (Azadirachta indica) are provided to animals.
to development of infective larvae. In India, Sri Lanka,
Current studies in Vietnam on effects of plants on
Malaysia, Indonesia and China, nematophagous fungi
Haemonchus larvae in vitro showed promising results
have been isolated and/or results in experimental
with extracts of some legumes, namely Leucaena
conditions have indicated the potential of using fungi
leucocephala, Acacia mangium and Calliandra sp.
in reducing nematode infections in ruminants (FAO
Farmers of small ruminants in rural Indonesia use 2002). Beriajaya and Ahmad (Indonesia, 1999)
traditional veterinary medicine extensively. Dano and used Arthrobotrys oligospora for biological control of
Bogh (1999) rightly stated that herbal remedies have nematode parasites of sheep. They infected 20 young
undergone many years of clinical trials and, as they sheep free of helminth infection with 5000 L3 of
prove reliable, are accepted by the users. It is only Haemonchus contortus, and six weeks later all sheep
when scientists attempt to extract the ‘active ingredient’ were divided into two groups of 10. One group
from various parts of these plants in various ways in received a number of A. oligospora four times at two-
their experiments (which sometimes yield negative results) weekly intervals, and the other group was a positive
Worm control for small ruminants in Southeast Asia

that the plants are deemed useless. However, scientific control. Examination was based on faecal worm egg
validation of such plants is crucial to be acceptable counts and recovery of larvae after culturing of faecal
to mainstream veterinary practices. It is therefore an samples. The results showed that the group receiving
exciting yet challenging area of research to embark fungi produced fewer larvae than the control.
upon. A rigorous evaluation of some African herbal
However, the two major obstacles that need to be
dewormers recently reached the same conclusion:
addressed if this form of biological control is to be
that evaluation of these traditional remedies needs
introduced in Asia, are the delivery system and the
to be made with traditional healers, using standard
affordable large-scale manufacture of fungal spores.
guidelines, as controlled trials often show no or small
effects on parasite burdens (Githiori 2003).

16
Genetics The immediate benefits of using worm measurements
to select breeding stock come from the monitoring of
Breeding approaches to decrease the impact disease levels and improved worm control. This usually
of nematode worms on goats and sheep are means less use of expensive and increasingly unreliable
increasingly important and many breeds of goats chemicals. Genetic gains depend on the intensity of
and sheep perform better in the presence of worm selection and the numbers of animals measured. Genetic
challenge than other breeds available to the farmer resistance can be used as part of an integrated health
(see Chapter 5). These include the Red Maasai, program, with adoption of rotational grazing systems,
Barbados Blackbelly, St Croix and Garole sheep and improved nutrition and management, confinement
East African goats. The simplest breeding approach is during risk periods and better use of chemicals.
to replace the currently used breed, which may have
been introduced quite recently, with an adapted breed Vaccines
of proven productivity and reduced need for other inputs
There are no commercially available vaccines for any
for worm treatment.
gut nematode parasite of any host, including man and
There is sufficient genetic variation in resistance to it is unlikely that a commercial vaccine will be produced
nematodes within breeds of sheep to allow selection for sheep or goats in the foreseeable future. Progress
for increased resistance but this would only be towards a vaccine against Haemonchus is most likely
applicable in production systems where breeding can to come from a recombinant version of the hidden gut
be controlled and there is systematic measurement of antigens which are known to be immunogenic and
production. This has happened in the field in Merino, effective in suppressing infections in a variety of field
Romney, and Blackface sheep, and Cashmere and conditions (Smith 2004XX). The research and
Guadeloupe goats. In Australia and New Zealand development tasks for producing such a recombinant
there are commercial breeding schemes which include antigen in commercial quantities, finding an appropriate
adjuvant and delivery systems and making the product
resistance to nematodes in their breeding objectives.
available for relatively poor farmers are considerable.
Measurement of resistance is by collection of faeces
from young sheep under challenge and counting Integrated control programs
the nematode eggs in the laboratory. This number,
combined with production measurements, is used The foundation for any program on parasite control
to select the next ram, buck or breeding female. is based on a sound knowledge of epidemiology of
parasite infection in a particular area. We now know
The greatest genetic change in modern time has been
that parasite control programs for smallholder farming
to decrease the resistance of indigenous breeds by the
systems in tropical Asia utilise strategic drenching,
introduction of exotic breeds with greater dependence
on chemicals for worm control. a combination of confined and grazing systems,
improved nutrition and controlled breeding. The countries

17
 which have epidemiological information on nematode
infections in sheep and goats include Indonesia, Fiji,
Philippines, Nepal, Malaysia and Thailand. These
countries are thus in a stronger position to plan and
implement parasite control programs.
The only practical option for reducing reliance on
anthelmintics depends on enhancing resistance of the
animal to larval establishment by improved protein
nutrition.and minimising exposure to parasites.
A substantial amount of information has been generated
from Fiji to utilise these two broad approaches, utilising
knowledge on epidemiology and integrating it with Increased income from meat, milk products and fibre is
rotational grazing and use of medicated urea-molasses one consequence of good management and worm control.
blocks (UMB). When medicated UMB was provided
to pregnant does grazing on permanent pastures, the
There is a vast amount of epidemiological information
number of animals showing clinical signs of parasitism
on helminth diseases from Indonesia. The effect of
was reduced three-fold. So, the use of UMB reduced the
season, time of grazing and host age on gastrointestinal
frequency of treatments and suppressed the periparturient
worm burden and carcass percentage of sheep in Java
rise in FEC in pregnant ewes. In a 10 paddock, 35-day provides useful discussion (Kusumamihardja, 1988).
rotation system medicated UMB reduced the number Sheep grazing in the dry season have significantly
Worm control for small ruminants in Southeast Asia

of salvage drenches four-fold, provided pregnant does lower worm burdens (average 1108 worms) than those
had access to the blocks for two cycles of the rotation grazing in the wet season (average 1928 worms).
in the six-cycle trial period. UMB provided to young and More interestingly, in the dry season sheep grazing in
maiden ewes not only improved their reproductive the mornings are at a higher risk of contracting heavier
performance at first lambing and reduced the number of worm burdens (1969 worms) than those grazing in
salvage drenches based on FEC but, more importantly, the afternoons (290 worms) whereas there was no
nearly halved lamb mortality rates. The increase in milk difference grazing at any time of the day in the wet
yield and quality afforded by the blocks enhanced season. These worms were identified to belong to the
the survival of lambs at weaning. These findings have strongyle group. These findings also corresponded with
important implications in reducing treatment costs and work by Sumartono (1985) who found a trend of
lamb mortalities, both of which are vital considerations highest egg production by Haemonchus contortus in
for the smallholder farmer. the morning, which declined in the afternoon and was
lowest in the early evening. These findings suggest that

18
during the wet season it is advisable to confine animals ■ Improved nutrition — including the use of tree and
and stallfeed them to reduce exposure to infective stages of shrub leaves to reduce intake for ground-based and
the parasite and to graze animals in the afternoons in contaminated feeds; plants with possible direct or
the dry season. These grazing tactics may be adopted indirect anthelmintic effect and cut-and-carry methods,
in areas which have distinct wet and dry seasons, such especially during times of heavy rain or heavy
as some areas in Indonesia, Philippines, Cambodia pasture contamination.
and Vietnam.
■ Grazing management and housing — improved
housing to reduce stress through better ventilation,
Participatory approaches
shelter, manure and feed management, rotational
The above integrated approaches are limited to the grazing and management of contaminated areas
technologies and are designed for application by a around housing.
farmer on the recommendation of an advisor or other
■ Controlled breeding — includes timing of breeding
extension agent. Inclusion of the farmer in development
to produce young susceptible kids and lambs when
of ideas and technical options and their evaluation,
worms can be best managed; considering possible
as well as the application of the technology, involves
a different approach to the research and development increase or decrease in genetic resistance when
process. The term ‘participatory’ is often applied to a deciding to use new genetics, especially ‘upgraded’
process that involves farmers and other important people or ‘improved’ bucks and rams.
who influence them and are affected by their successes A participatory process of testing and evaluating these
and failures. Their involvement is not just as recipients strategies alone and in combination has shown that
of technology but as active contributors to research controlled breeding has been the least successful. This
and development. One such approach is described outcome is location specific and other farmers working
in this volume by Alo (Chapter 3). It is worthwhile with other researchers in other farming systems may
commenting here on the technology options that were reach different conclusions.
agreed to be feasible, available and affordable by
some farmers in the Philippines. They were:
■ Use of effective chemicals — incorporating Forums for discussion
knowledge on anthelmintic resistance and use of There are a number of ways in which scientists and
alternative delivery methods such as feed blocks. others can informally discuss worm control and related
Quarantine drenching is an appropriate strategy for issues and interact with other communities working on
institutions and large commercial suppliers of stock. these problems. The following list will be useful as a
starting point to accessing this increasingly electronic
world of information sharing and debate.

19
 FAO networks and discussion groups The SParC newsletter and website
FAO has supported a Network for Helminthology in Originating from a project funded by ACIAR and
Africa which can be accessed at www.worms.org.za/. IFAD in the Philippines and Southeast Asia, the
This group recently conducted an electronic conference SparC newsletter has been produced in paper and
on “Managing Worms Sustainably — we need to electronic format since 1998. The newsletter and
reconsider present recommendations”. The unedited a wide collection of resource material are available
contributions can be obtained from through the website associated with these projects,
/econf/manworm.doc. www.worminfo.org and also included with this volume.

The ‘novel approaches’ series of meetings

Summary
Three meetings have been held — in Armidale,
Australia; Baton Rouge, USA; and Edinburgh, In livestock smallholdings in Asia there is a need to
Scotland. The fourth is in Merida, Mexico, with the change the emphasis from a disciplinary approach
theme: “Worm control or worm management: New where studies are focused on chemical control, genetics
paradigms in integrated control” indicating that some or grazing management to a multidisciplinary approach
changes in thinking about worms and parasites are where the integration of all disciplines is recognised
under way. The objectives of these meetings are to: as necessary. A further step, still being researched,
is recognising that the full participation of farmers and
1) update the scientific community on the current state other stakeholders is essential from the beginning of
of knowledge of novel approaches for the control a research or control program if the results are to be
of helminths in livestock,
Worm control for small ruminants in Southeast Asia

useful and sustainable in the long term. Additionally,

2) investigate the limitations affecting the application we speculate that gastrointestinal nematodes in small
of this knowledge and ruminants might be more usefully considered as
indicators of poor management than as a problem
3) investigate what strategies can be adopted to in their own right.
overcome the limitations.

20
References
Ankers, P., Itty, P., Zinsstag, J., Trawally, S. and Pfister, Knox, D.P. 2000. Development of vaccines against
K. 1998. Biannual anthelmintic treatments in village gastrointestinal nematodes. Parasitology 120,
Djallonke sheep in the Gambia: effects on productivity S43–S61.
and profitability. Preventive Veterinary Medicine 34,
Livestock in Development (LID) 1999. ‘Livestock in
215–225.
Poverty-Focused Development.’ LID: Crewkerne, UK.
Anon. 2002. Biological control of nematode parasites of
Mateo C.D. 1996. Herbal medicine in animal health care.
small ruminants in Asia. FAO Animal Production and
Animal Husbandry and Agricultural Journal 30(1), 52,
Health Paper, 104.
54–58, 60–61.
Baker, R.L. 2003. Exploring the genetic control of
Osaer, S., Goossens, B., Eysker, M. and Geerts, S. 2000.
resistance to gastrointestinal helminth infections in
The effects of prophylactic treatment on the productivity
sheep and mice. Animal Breeding and. Genetics
of traditionally managed Djallonke sheep and West
15, 183–190.
African Dwarf goats kept under high trypanosomiasis
Ghalsasi, P.M., Nimbkar, C., Kahn, L.P. and risk. Acta Tropica 74, 13–24.
Walkden-Brown, S.W. 2002. Effects of different
Thomson, E.F., Gruner, L., Bahhady, F., Orita, G.,
levels of worm control on meat production of deccani
Termanini, A., Ferdawai, A.K. and Hreitani, H. 2000.
sheep in shepherds’ flocks in Maharashtra India.
Effect of gastrointestinal and lungworm nematode
In ‘Proceedings of the 10th International Congress
infections on ewe productivity in farm flocks under
of the Asia–Australiasian Animal Production Societies
variable rainfall conditions in Syria. Livestock
(AAAP)’, New Delhi, September 23–29, pp. 152–156.
Production Science 63, 65–75.
Githiori, J.B., Höglund, J., Waller, P.J. and Baker,
Thornton, P.K., Kruska, R.L., Henninger, N., Kristjanosn,
R.L. 2003. The anthelmintic efficacy of the plant,
P.M., Reid, R.S. and Robinson, T.P. 2002. Locating
Albizia anthelmintica, against the nematode parasites
poor livestock keepers at the global level for research
Haemonchus contortus of sheep and Heligmosomoides
and development targeting. Land Use Policy 20,
polygyrus of mice. Veterinary Parasitology 116, 23–34.
311–322.
IFAD 2001. ‘Regional Assessment of Rural Poverty
Wood G. 2003. Staying Secure, Staying Poor: The
in Asia and the Pacific.’ IFAD: Rome.
Faustian Bargain. World Development 31, 455–471.

21
2. The economic impact of worm infections in small
ruminants in Southeast Asia, India and Australia
R.S. McLeod

Introduction
About 10% of the world’s sheep population and ■ calculate the annual economic impact of roundworm
29% of the goat population are reared in Southeast parasitism in each of the above countries
Asia, mostly by smallholders. Haemonchosis, a
■ quantify the economic benefits from sustainable
disease caused by the blood-sucking stomach worm
endoparasite control (SPC) adoption in the target
(Haemonchus contortus), has been identified as the
countries, which include Nepal, Indonesia, Vietnam
most serious endoparasite problem of small ruminants
and the Philippines.
in the region. Within sub-Saharan Africa, de Haan and
Bekure (1991) estimated that endoparasites cause The economic cost of roundworm parasitism alone
mortality and production losses in the order of $2 billion does not justify allocating funds toward parasitological
per year. However, valuation of the economic impacts research and extension (Perry and Randolph 1999).
of roundworms in Asia is confounded by a lack of The ability of research outcomes to reduce control and
accurate estimates of disease prevalence and the production-loss costs should guide funding decisions.
differing characteristics of small ruminant production Hence this attempt to quantify the potential economic
systems throughout the region. benefits of reducing roundworm impact in the target
countries. Decreasing the impact of roundworm
This chapter will:
parasitism is difficult, since conventional parasite
■ characterise small-ruminant production systems in control using anthelmintics has been adversely affected
selected Asian countries and Australia, using sets by increasing drug resistance in parasite populations. Gray
of tables that describe flock structure and size (1999) noted that greater attention to the development
of SPC strategies, which entail strategic anthelmintic
■ estimate roundworm prevalence and livestock
treatment, genetically resistant hosts, improved
mortality in India, Indonesia, Thailand, Vietnam,
management, vaccines, supplementary feeding
Australia, Nepal and the Philippines
and biological control, is needed.

23
 Small-ruminant production Indonesia has the largest small-ruminant flock in
Southeast Asia: about 15 million goats and eight million
Large flocks of small ruminants are found in Southeast
sheep. The national flock size has been increasing over
Asia and Australia. The numbers of goats in target
the past 20 years in response to the growing demand
Southeast and southern Asian countries are illustrated in
for meat.
Figure 2.1. Asia and Australia differ in their agro-climatic
conditions and livestock production practices and so The Philippines and Nepal have the next largest
the nature of small-ruminant production and the impacts flocks of small ruminants. Goats are widespread in the
of internal parasitism also vary. To systematically assess Philippines but sheep are uncommon, despite efforts to
the economic impact of roundworm parasitism, national integrate sheep production within tree cropping systems.
The economic impact of worm infections in small ruminants in Southeast Asia, India and Australia

flocks are characterised into village (small-scale Goat and sheep production is not widespread in
sedentary), commercial and transhumant systems. Malaysia, Thailand and Vietnam. National flock sizes
Parameters such as meat production and wool yield are small in these countries and large ruminant production
are detailed in Table 2.1 for each representative system. is of greater economic importance. In Thailand and
These parameters provide a baseline from which yield Malaysia small-ruminant production is becoming less
reductions, as a result of roundworm parasitism, important, perhaps because of increasing population
can be estimated. pressure and greater urbanisation.
The smallholder village, or sedentary, production system
is most commonly found in Thailand, Indonesia, Vietnam,
Figure 2.1 Small-ruminant flock sizes in
the Nepalese hills and the Philippines. Traditionally, milk
Southeast Asia (FAO 1999)
consumption has been low in Southeast Asia and small-
ruminants are reared for supplementary income from
meat production.
30

Sheep In India and Nepal, many sheep and goats are raised
Million head (1999)

Goats within transhumant systems. Madan (1996) indicated

20
that 30% of sheep in arid areas form part of permanent,
seasonal or temporary migratory flocks, with movement
10 dictated by the timing of monsoon rains. In mountainous
regions, sheep are also raised as part of migratory
0 systems. Flocks are often maintained for four or five
months under stall-fed production, then handed to a
Indonesia Malaysia Nepal Philippines Thailand Vietnam
Chopan (professional shepherd) for grazing in alpine
pastures from April to November (Madan 1996).

24
 Table 2.1 Small-ruminant productivity for Asian and Australian livestock systems

Livestock system Village Transhumant Commercial

Goats
Liveweight of adult (kg)(a) 22 22 –
Liveweight of immature (kg)(b) 12 12 –
Adult composition of herd (%)(c) 71 71 –

Sheep
Liveweight of adult (kg)(d) 22 22 36
Liveweight of immature (kg)(e) 12 12 25
Adult composition of herd (%)(f) 60 60 76
Wool production (kg/adult/year)(g) – – 4.5
Wool production (kg/immature/year)(g) – – 2.3
(a) Adult goat liveweights are derived from Ibrahim (1996) and Saithanoo et al. (1997). (b) Immature goat liveweight is derived from Saithanoo et al. (1997).
(c) Adult composition is derived from Saithanoo et al. (1997). (d) Adult sheep liveweight is derived from Meat Research Corporation (1993) for commercial
and Ibrahim (1996) for indigenous. (e) Immature sheep liveweight is derived from Meat Research Corporation (1993) for commercial and Ibrahim (1996) for
indigenous. (f) Adult composition is derived from Meat Research Corporation (1993). (g) Commercial wool production is derived from ABARE (2000).

All sheep production in Australia is on a commercial Prevalence of roundworm parasitism

basis. Spanish merino sheep are commonly raised for
wool production, while crossbred sheep types (such as The most important nematode genera of Asia and
Merino cross-breeds) and British breeds are used in Australia include Haemonchus, Trichostrongylus,
sheep-meat production. Merino sheep are typically more Strongyloides and Oesophagostomum. Roundworm
susceptible than British breeds to roundworm infection. parasitism generally increases with the onset of the wet
Australian sheep numbers have been declining over the season in most tropical countries, however, there has
past 35 years, largely in response to the declining real been only limited examination of the seasonal trend in
price received for greasy wool. Statistics indicate that host worm burden and infectivity of pasture. To gain an
the national flock contracted from 158 million head appreciation for the seasonal prevalence of Haemonchus
in 1962 (FAO 1999) to 115 million in 2000 in countries where epidemiological data are limited,
(ABARE 2000). a simulation model (Barnes et al. 1988, Barnes and
Dobson 1990 a, 1990b) was adapted for this

25
 nematode species. The model was further developed to Studies of sheep production in the tropics indicate
assess worm control options. Results of the simulations that immature and adult mortality are generally high:
are included in relevant country assessments. 40% in perinatal lambs in Morocco (Idrissa et al.
1992); 19.3% in perinatal Menz sheep in Ethiopia
It is difficult to quantify the extent to which internal
(Mukasa-Mugerwa et al. 1994); 48 and 60% in
parasites are constraining small-ruminant production in
immature and adult village sheep of northwest
Asia as few field trials have been conducted to estimate
Cameroon (Ndamukong et al. 1989a); and 29%
the size of the problem. Goat flock productivity data
of sheep in Indonesia (Batubara 1997). Few studies
from villages in Thailand (Saithanoo et al. 1997)
have been carried out in the tropics to clearly
indicate annual mortality rates of 39% for kids and
The economic impact of worm infections in small ruminants in Southeast Asia, India and Australia

identify the impact of roundworms on flock

immatures, and 7.2% for adults. For the purpose of this
productivity, although Adeoye (1994) found that
analysis, it is assumed that 1% of adult goats, and 5%
27% of sheep deaths were related to helminth
of immature goats, suffer roundworm related mortality.
infection in village sheep of southwest Nigeria.
Major assumptions relevant to the economic impact
assessment are shown in Table 2.2.

Table 2.2 Roundworm prevalence and mortality by production system

Village Transhumant Commercial

Livestock system Adult Immature Adult Immature Adult Immature

Goats
Prevalence (%)(a) – – 90 90 60 60
Mortality (%)(b) – – 1 5 1 3

Sheep
Prevalence (%)(c) 87 87 90 90 60 60
Mortality (%)(d) 1 3 1 5 1 3
(a) Disease prevalence estimates are the author’s. Transhumant mortality losses are lower due to arid and mountain agro-climates. (b) Consultant estimates
derived from overall flock productivity studies in Thailand by Saithanoo et al. (1997). (c) Disease prevalence estimates are the author’s. Transhumant mortality
losses are lower due to arid and mountain agro-climates.(d) Consultant estimates derived from experiments by Barger and Southcott (1978), Anderson
(1972, 1973), Anderson et al. (1976), Thompson and Callinan (1981), and Brown et al. (1985) in the high rainfall areas of Australia.

26
Mortality data from Australian field trials using Selected studies of productivity in parasitised goats have
roundworm susceptible merino sheep (Barger and been conducted in southern Luzon, Philippines. Que
Southcott 1978, Anderson 1972, 1973, Anderson et al. (1995) showed that dewormed and parasitised
et al. 1976, Thompson and Callinan 1981, Brown goats differed in growth by 4 kg over a period of eight
et al. 1985) have been used to estimate sheep months. Howlader et al. (1997a, 1997b, 1997c)
production losses within Asian production systems. described the pathological, parasitological and
Assumptions are included in Table 2.3. Roundworm production changes in immature goats infected
parasites cause mortality as well as production losses in artificially with H. contortus. The growth of kids
small ruminants that recover from the effects of infection. born of infected mothers was also affected.
During the period of infection, milk production, growth
Adult sheep are generally considered to have greater
and manure production are typically reduced. The
natural resistance to the impact of internal parasites and
severity of reduced productivity is a function of stock
their production losses are assumed to be lower than
age, breed, physiological status and level of nutrition.
those of immature animals.
A set of production-loss tables have been compiled
(Table 3) to estimate the losses associated with
roundworm infection.

Table 2.3 Annual production losses in disease-affected small-ruminants

Village Transhumant Commercial

Livestock system Adult Immature Adult Immature Adult Immature

Goats
Liveweight loss (kg/hd/yr)(a) 0.7 0.4 0.7 0.4 0.7 0.4

Sheep
Liveweight loss (kg/hd/yr)(b) 0.8 1.2 0.8 1.2 0.8 1.2
Wool loss (kg/hd/yr) 0.2 0.2 – – – –
(a) Meat losses of 0.7 kg for adult goats and 0.4 kg in immature goats are consultant estimates derived from study by Que et al. (1995). In this study it was
found that treated goats were 3.6 kg heavier than controls. It was assumed that 10% of this loss estimate would be experienced by average village goats.
(b) Meat losses of 0.8 kg for adult sheep and 1.2 kg in immature sheep are consultant estimates derived from studies by Barger and Southcott (1978) and
winter rainfall trials by Anderson (1972,1973), Anderson et al. (1976), Thompson and Callinan (1981) and Brown et al. (1985). (c) Wool losses of 0.2
kg for adult sheep and 0.2 kg in immature sheep are consultant estimates derived from studies by Barger and Southcott (1978) and winter rainfall trials by
Anderson (1972,1973), Anderson et al. (1976), Thompson and Callinan (1981) and Brown et al. (1985).

27
 National economic loss and Small ruminant
populations are
control costs especially high in
Muslim countries
Production losses, estimated for each representative
where few pigs
livestock system, are aggregated to country level
are raised.
using national small-ruminant flock size information
(FAO 1999). National production losses are multiplied
by livestock product prices to estimate the aggregate
economic value of losses. The annual costs of Of the total roundworm-inflicted production loss
The economic impact of worm infections in small ruminants in Southeast Asia, India and Australia

roundworm parasites in selected Asian countries are estimated for Indonesia, $7.1 million was attributable to
shown in Figure 2.2. Of the target countries in the goat production and $5.6 million to sheep production.
project, the aggregate costs of roundworm parasites The estimated loss for sheep production is significantly
are greatest for Indonesia, where it was estimated larger than that calculated by Temaja in 1980. The
that the disease cost $US 13 million in 1999. increase may be a result of increased flock size and
product prices over the past 20 years.
Small ruminant producers in Nepal and the Philippines
Figure 2.2 Annual economic impact of
were estimated to experience the next largest economic
roundworms in target countries
loss from roundworms. Economic loss estimates are
largely proportional to numbers of small ruminants.
15
Roundworm-loss estimates have also been updated for
Sheep India and Australia. These countries have large small-
Goats
ruminant flocks and, hence, substantial annual economic
$US million (yr)

10
losses: $103 million and $111 million, respectively.
The Australian cost estimate is similar to that calculated
5
by McLeod (1995), but has decreased with lower wool
prices and a smaller flock. Strategic parasite control
0 programs have been developed for both India and
Indonesia Malaysia Nepal Philippines Thailand Vietnam Australia. Lubulwa et al. (1996) quantified large

28
economic returns from the development and extension SPC adoption gains would also deliver substantial
of improved roundworm control in western India, while benefits for farmers in the Philippines and Nepal.
Collins and Poulter (1990) and McLeod et al. (1992) Given that SPC recommendations will be formulated for
estimated substantial economic benefits from the Nepalese farmers in the mid-hills, transhumant producers
development of Wormkill and Drenchplan strategic are not likely to capture substantial benefits. Changes
roundworm control programs in the summer and in SPC adoption level and flock size substantially affect
winter rainfall areas of Australia. estimated economic benefits. Consequently, on-farm
research should be carried out at benchmark sites,
representative of major agro-ecological zones, to
Potential economic benefits develop SPC recommendations that maximise adoption.
from SPC adoption Studies have shown that improved parasite control
generates financial benefits (Misniwaty et al. 1994)
Preliminary simulation analysis suggests that production but adoption remains low. Constraints to the adoption
losses associated with roundworm parasitism could be of SPC need to be identified and innovative approaches
substantially reduced by adopting improved management to promote SPC practices investigated.
recommendations. At this early stage of the SPC project
it is counterproductive to suggest the most desirable
combination of management practices, as this strategy
is still to be formulated. However, if an SPC package Figure 2.3 Annual potential benefit from
could be devised that would reduce the effect of these SPC adoption
parasites by 15% for adopting farmers, and 10% of
sheep or goat owners were also to adopt the package, 200 Sheep
the economic benefits outlined in Figure 2.3 would Goats
be realised. 150
$US thousnads

Indonesia would gain the largest economic benefits 100

from 10% adoption of an SPC program that reduced
productivity losses by 15%. Based on current prices and 50
prevalence data included in the analysis, Indonesian
farmers would capture $0.2 million in annual benefits. 0

Indonesia Nepal Phi lippines Vietnam

29
 Spreadsheet model Australian Bureau of Agriculture and Resource Economics.
2000. Australian commodities. vol 7(2) June,
A spreadsheet-based model, PBASE (Excel 97, Microsoft Canberra, ABARE.
Corporation), has been developed to integrate flock Barger, I.A. and Southcott, W.H. 1978. Parasitism and
size, disease prevalence and production loss components production in weaner sheep grazing alternately with
of the economic impact assessment procedure and cattle. Australian Journal of Experimental Agriculture
evaluate total annual costs of roundworms within target and Animal Husbandry, 18(92), 340–346.
countries. Preliminary data for Nepal, Australia, Thailand,
Barnes, E.H. and Dobson, R.J. 1990a. Population
Malaysia, Vietnam, India, Philippines, and Indonesia dynamics of Trichostrongylus colubriformis in sheep:
The economic impact of worm infections in small ruminants in Southeast Asia, India and Australia

have been entered and up-to-date data for relevant mathematical model of worm fecundity. International
systems need to be included. The model is supported Journal for Parasitology, 20(3), 375–380.
by a help system that supplies operational and data
Barnes, E.H. and Dobson, R.J. 1990b. Population
background information to guide spreadsheet users.
dynamics of Trichostrongylus colubriformis in sheep:
computer model to simulate grazing systems and
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goats in two groups of villages in Southwest Nigeria.
P.J. 1988. Predicting populations of Trichostrongylus
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colubriformis infective larvae on pasture from
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Parasitology, 18(6), 767–774.
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in a winter rainfall region. I. Epizootiological studies
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Anderson, N. 1973. Trichostrongylid infections of sheep
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the Australian Agricultural Economics Society. Brisbane,
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Anderson, N., Morris, R.S. and McTaggart, I.K.
De Haan, C. and Bekure, S. 1991. Animal health
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the anthelmintic control of helminthiasis in weaned
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No. 134, Washington DC, World Bank, 49 p.
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Food and Agriculture Organization of the Lubulwa, G., Gray, D., Patten, K. and Nimbkar,
United Nations. 1999. Livestock statistics C. 1996. Project development assessment: prolific
(http://apps.fao.org/cgi-bin/nph-db), Rome, FAO. worm-resistant meat sheep for Maharashtra, India and
Australia. Canberra, ACIAR Economic Evaluation Unit,
Gray, G.D., Yee, C.A.T., and Villar, E.C. 1999.
Working Paper Series No. 24, 58 p.
Philippine literature on helminth control for small
ruminants. SPC Working Paper No. 2, Los Baños, McLeod, R.S. 1995. Costs of major parasites to the
Philippines. ILRI, 20 p. Australian livestock industries. International Journal
for Parasitology, 25(11), 1363–1367.
Howlader, M.M.R., Capitan, S.S., Eduardo, S.L.
and Roxas, N.P. 1997a. Effects of experimental McLeod. R.S., Collins. D.J., Barnes. E.H. and Dobson.
Haemonchus contortus infection on red blood cells R.J. 1992. Estimating the gains of strategic nematode
and white blood cells of growing goats. Asian- control. Paper presented to the 36th Annual Conference
Australasian Journal of Animal Sciences 10(6), of the Australian Agricultural Economics Society.
679–682. Brisbane, the University of Sydney.
Howlade,r M.M.R., Capitan, S.S., Eduardo, S.L., Roxas, Madan. M.L. 1996. Small ruminant production in India.
N.P. and Sevilla, C.C. 1997b. Effects of stomach In: Le Jambre L.F. and Knox M.R. ed., Sustainable
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born of infected mother goats. Asian-Australasian Proceedings No. 74, 13–20.
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Meat Research Corporation. 1993. Data compendium
Howlader, M.M.R., Capitan, S.S., Eduardo, S.L., Roxas, for MRC benefit–cost evaluations of submitted projects.
N.P. and Sevilla, C.C. 1997c. Performance of Consultant Report, Sydney, MRC.
growing goats experimentally infected with stomach
Misniwaty, A., Doloksaribu, M., Mirza, I. and Muljadi,
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A. 1994. Evaluation of anthelmintic distribution by
Journal of Animal Sciences 10(5), 534–539.
animal health delivery networks in Membang Muda,
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in Malaysia. In: Le Jambre, L.F., Knox M.R. ed., Paper No. 161, 15 p.
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Sherington, J. and Mutiga, E.R. 1994. Birth weight
Idrissa, A.H., Ward, G.E., Johnson, D.W., Benkirane, as a risk factor for perinatal lamb mortality, and the
A. and Fassi-Fehri, M.M. 1992. Bacteriological effects of stage of pregnant ewe supplementation
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Preventive Veterinary Medicine,12, 35–46. Preventive Veterinary Medicine, 19, 45–56.

31
 Ndamukong, K.J.N., Sewell, M.M.H. and Asanji, M.F.
Further reading
1989a. Disease and mortality in small ruminants in
the north west province of Cameroon. Tropical Animal Barton, N.J. and Brimblecombe, C.J. 1983. The effects
Health and Production, 21, 191–196. of anthelmintic treatment and season on the quantity
and quality of wool grown by merino sheep.
Ndamukong, K.J.N., Sewell, M.M.H. and Asanji,
Australian Journal of Agricultural Research, 34(5),
M.F. 1989b. Management and productivity of small
557–568.
ruminants in the north west province of Cameroon.
Tropical Animal Health and Production, 21, 109–119. Batabara, A. 1997. Studies on genetic resistance
of Sumatra breed and hair sheep crossbreds to
Perry, B.D. and Randolph, T.F. 1999. Improving the
experimental infection with Haemonchus contortus
The economic impact of worm infections in small ruminants in Southeast Asia, India and Australia

assessment of the economic impact of parasitic

in north Sumatra, Indonesia.
diseases and of their control in production animals.
Veterinary Parasitology, 84(3–4), 145–168. Elder, J.K., Dunwell, G.H., Emmerson, F.R., Kearnan,
K.S., Waters, K.S., Knott, S.G. and Morris, R.S.
Que, E.I., Tongson, M.S. and Acedo, R.A. 1995.
1979. A survey concerning cattle tick control in
Cost–benefit analysis of deworming livestock at
Queensland—producer attitudes. In: Johnston L.A.Y.,
barangay level I. Deworming of goats at barangay
and Cooper M.G. ed., Ticks and Tick Borne
level. Journal of the Philippine Veterinary Medical
Diseases: Proceedings of a symposium held at the
Association, 1(1), 13–17.
56th Annual Conference of the Australian Veterinary
Saithanoo, S., Pattie, W.A. and Norton, B.A. 1997. Association, Townsville, 14–18 May, 1979,
Simulation models of breeding systems for village Sydney, Australian Veterinary Association.
goat production in southern Thailand. In: PSU Goat
Gatenby, R.M. 1986. Sheep production in the tropics
Research Publications 1985–1997, No. 2528–2540,
and sub-tropics. Tropical Agriculture Series, Essex,
Thailand, Prince of Songkla University.
Longman Group Ltd., 121–144.
Temaja, T. 1980. Pedoman pengendalin penyakit menular,
Howlader, M.M.R., Capitan, S.S., Eduardo, S.L.,
Jilid II, Direktorat Kesehatan Hewan, Direktorat
Roxas, N.P. and Sevilla, C.C. 1996. Effect of
Jenderal Peternakan, Departmen Pertanian, 83–99.
experimental Haemonchus contortus infection on
Thompson, R.L. and Callinan, A.P.L. 1981. The effects hemoglobin concentration and packed cell volume
of nematodiasis on weaner sheep in Western of does. Asian-Australasian Journal of Animal
Victoria. Australian Journal of Agricultural Research, Sciences 9(5), 597–601.
32(6), 975–985.
Merkel, R.C. and Subandriyo. ed., 1997. Sheep and
goat production handbook for Southeast Asia. 3rd
ed. Davis, University of Califonia Davis, 213 pp.

32
Morris, R.S., Anderson, N. and McTaggart, I.K. 1977. Over, H.J., Jansen, J. and van Olm, P.W. 1992.
An economic analysis of two schemes for the control Distribution and impact of helminth diseases of
of helminthiasis in breeding ewes. Veterinary livestock in developing countries. Rome, FAO Animal
Parasitology, 3, 349–363. Production and Health Paper No. 96. 221 pp.
Msellati, L. and Tacher, G. 1991. Animal health and Pearce, E.A. and Smith, C.G. 1998. The Hutchinson
economics. Paris, Insitut d’Elevage et de Veterinary world weather guide. Oxford, UK, Helicon.
Medicine, CIRAD.

33
3. Developing and testing integrated approaches to
sustainable parasite control in small ruminants with
farmers in the Philippines, Vietnam, and Indonesia
A.M.P. Alo

Introduction
During the past 10 years there has been a big push to Ruminant Gastrointestinal Parasites project, implemented
introduce or strengthen a user perspective in adaptive in the Philippines, Indonesia, Vietnam, Lao-PDR and
agricultural research. Technology development is said Cambodia. In this component project, farmers are
to be a complex, multi-stranded, and multi-directional offered the opportunity to conduct research on integrated
process, involving many actors, other than scientists, in worm control in goats. Specifically, technologies
the formal research system (Cramb 2000). The evolution developed through the Sustainable Endoparasite Control
of a particular technology depends not only on its (SPC) for Small Ruminants Project (ACIAR 97133) are
scientific merits but also on the actions of development offered as a basket of options for testing by farmers.
coalitions — loose groupings of actors who combine
This chapter discusses how worm control technologies
their resources to push for a particular path of technical
for small ruminants were developed and tested in three
change (Biggs and Smith 1998). Thus there is a need
TAG 443 participating countries — Vietnam, Indonesia
for active participation of stakeholders to generate
and the Philippines — with particular emphasis on the
technologies that are not only ‘well-developed’ but
Philippines where project analysis is most advanced.
also adopted in a sustained manner (Gabunada et
Although the paths taken by the countries were different,
al. 2003).
common lessons point to one thing: it is extremely
These factors were considered in the ILRI-IFAD Technical valuable to involve the beneficiaries of technology
Assistance Grant 443 (TAG 443) project entitled development in all phases of a project. In this case, not
Development and Testing of an Integrated Approach only did it accelerate the adaptation and advancement
to the Control of Gastrointestinal Parasites in Small of new farming practices but it also improved the
Ruminants in Southeast Asia. A crucial component of livelihoods of the participating small-ruminant keepers.
TAG 443 was the Participatory Diagnosis of Small

35
 The participatory technology ‘good impact’ were packaged as best-bet options for
sustainable parasite control. Problems detected during
development process the testing stage were also investigated. More problems
At each focal site in Vietnam, Indonesia and the emerged after each cycle, so the process of technology
Philippines the process began with participatory development (testing, monitoring and evaluating,
problem diagnosis and the matching of farmers’ modifying and refining) was repeated several times.
The best-bet options were then offered to other farmers
Developing and testing integrated approaches to sustainable parasite control in small ruminants with farmers

needs with existing technological options. At this

point the Vietnamese project team took a different interested in replicating the experiments of focus farmers.
pathway as summarised in Figure 3.1. These farmers, however, were not researcher-guided
but allowed to decide how things best suited their
conditions (Binh et al. 2003).
Vietnam
There was no ACIAR-SPC project implemented in Indonesia and the Philippines
Vietnam. So, using SPC literature from different countries,
the Vietnamese project selected and evaluated specific In contrast, in the Philippines and Indonesia, technology
approaches, both on-station and on-farm, to generate testing was farmer-planned, designed and managed.
a basket of technologies to offer farmers. In essence, This meant that farmers, largely independent of the
the Vietnamese project was initially researcher-managed project team (Alo 2003, Subandriyo 2003):
although jointly planned and assessed by farmers ■ designed their projects and mixed and
and researchers. matched options to address their needs
Vietnamese farmers selected options that suited them ■ managed their own on-farm trials
from the initial basket of technologies and research
■ found needed resources
plans were generated by combining farmers’ local
knowledge with the technical know-how of the ■ modified the technologies to fit their
researchers. Most research was done on farms but some, resources and capabilities.
such as evaluating the effectiveness of medical plants
Participatory site appraisal was the first stage of the
on larvae, was done in the laboratory. A technical team
process. A series of consultations was conducted
helped farmers with their experiments by facilitating
with various local government units, SPC experts and
group discussions and helping collect and analyse
farmers. These meetings ensured that key stakeholders
data. Focus (treatment) and non-focus (control) farmers
were aware of the realities surrounding goat production
then came together with the technical team to jointly
in the focal villages and the potentials of each SPC
evaluate the experiments. Suitable technologies with
technological intervention identified.

36
Figure 3.1 Technology development paths taken by TAG 443-Philippines, Indonesia and Vietnam
(BT = basket of technologies)

Upscaling

Farmer
Dissemination
Managed
Workable BT

Farmer BT
On-farm
Trials
Technology
Technology Modification
Selection
PM&E Upscaling
Experience
sharing
Training
Researcher
Managed Best-bet BT
Initial BT Technology
Selection

STEEP
Screening
Refinement On-farm
LabTrials
Tech-Needs Trials
Matching
Problems

Solution BT PM&E
Identification Development

SPC Vietnam
Problem
Identification Consultation Indonesia
Philippines
Participatory
Participatory
Research Diagnosis and
Needs Matching

37
 Once the initial basket of technology options was of options generated in Vietnam, Indonesia and the
developed, it was subjected to STEEP screening for: Philippines were almost the same, including strategies
for improved management of:
■ Social acceptability
■ Technical feasibility ■ disease — strategic deworming using commercial
anthelmintics (with or without medicated feed
■ Economic viability
supplement mineral block); biological control of
Developing and testing integrated approaches to sustainable parasite control in small ruminants with farmers

■ Environmental soundness endoparasites using ducks, fungi and earthworms

■ Political acceptability
■ grazing — rapid rotational grazing
Field-based training courses were then held to inform
■ nutrition and feeding — establishment of forage
farmers about the options available to help solve their
gardens, tree and shrub leaf supplementation,
problems. Farmers were invited to select any technology
concentrate supplementation, stall-feeding
option they wanted to try on their farm. It was made
clear to them that along with this opportunity came the ■ breeding — introduction of exotic upgrades,
responsibility of finding the needed resources and of use of large local breeds, controlled breeding
managing their chosen project. Farmers were not
■ housing and confinement — well-designed housing
forced to try approaches that did not match their
with partitions, elevated slatted flooring, waste pits,
beliefs, resources or capabilities.
year round or rainy season confinement
Participatory monitoring and evaluation were used to
■ sanitation — effective waste management.
assess the dynamic process with farmers choosing an
initial technology-mix, testing the options on-farm and The options offered provided potential solutions to
adapting them until they arrived at the mix of options the major goat production problems of farmers, the
that best suited their circumstances. Results were used foremost being mortality from poor management
to select a group of technologies that farmers felt were (Alo 2003; Subandriyo 2003; Binh et al. 2003).
best suited to them and that could be scaled up or The project teams in Vietnam and Indonesia are still
disseminated to other farmers and communities — at the participatory monitoring and evaluation stage.
a farmer-generated basket of technologies. Although some preliminary results from Vietnam have
been collected, no detailed assessment has been
Baskets of technologies offered conducted. The Philippine project has completed
The main aim of the project is to control worms but this stage and their results have been analysed.
the technology baskets developed were holistic and
considered all aspects of goat management. The baskets

38
Participatory technology development
in TAG 443-Philippines

Community-based approach
The problem of parasitism among small ruminants
markedly constrains farm productivity in the Philippines.
The challenge is to empower farmers with knowledge
about goat production and health, to improve
productivity, minimise worm infestation and ensure
farmers receive the economic returns due to them. Farmers, extensionists and researchers can work together
This is best achieved through the active participation to plan and conduct experiments. (A.M. Alo)
of farmers in planning, field validation and evaluation,
thus the Philippine team supported the central role of
established in the provinces of Cebu and Pangasinan
the farmers in the TAG 443 project.
(the provinces with most goats). After some capacity
A community-based integrated approach to goat worm building the groups identified a set of criteria to select
control was employed. The project’s activities can be farmer cooperators.
classified into:
After farmer cooperators were selected social
■ selecting focal sites mobilisation (field trips, on-farm training, and technology
■ identifying farmer cooperators workshops) began. This led to the development of
baskets of technology options from which farmer
■ mobilising the community socially
cooperators selected technologies for testing. Farmers’
■ creating and evaluating baskets of options.
experiences and evaluation were the basis for adoption,
Focal site selection involved three levels of screening: rejection or modification of technologies.
regional, followed by provincial and then municipal
or village level. Once focal sites were identified, the Process of technology testing
project started to be institutionalised at each location.
Field trials in the Philippines were not all conducted at
Local working groups, consisting of representatives once. Preceding the testing was a week-long, hands-
from the Department of Agriculture-Regional Field Unit, on workshop on SPC technologies. This technology
Provincial Veterinary Office, the municipal/city training occurred during the rice-planting season in
agriculture office, municipal/city planning and the village of Tobor (one of the three focal sites) so
development office, and the village council, were farmers there deferred testing until cropping chores

39
 were finished. One cooperator even deferred adoption were required to note, during the initial month, the
of rapid rotational grazing to October 2001 as he did length of time they spent on each activity, the kind
not have the budget for the divisional fences required. of feed they collected and an estimate of the weight
of forage per feeding. The farmers had the freedom to
Testing was deferred at most sites because most farmers
choose the forages they wanted to use for their animals.
were not immediately able to construct a pen, the primary
prerequisite of all the baskets. Hence, on-farm trials across To avoid inbreeding, the farmers were asked to
Developing and testing integrated approaches to sustainable parasite control in small ruminants with farmers

sites officially started in July 2001, or two months after exchange bucks or upgrade their breed by using
the last farmers’ training workshop. an Anglo Nubian buck lent by the local government
unit to the site.
Initially, farmers were asked to construct a pen or
remodel their existing shed to meet the project’s Each month, the local working group (i.e. representatives
recommendations of: from local government agencies in the concerned region)
recorded animals’ weights and collected faecal and
■ an elevation of at least 1m from the ground
blood samples. Samples from Cebu were analysed in
■ walls and roof the diagnostic laboratory of the regional Department
■ feeders, salt lick tubes and brooder boxes of Agriculture and those from Pangasinan at Central
■ a separate kidding pen Luzon State University. For accurate identification, all
■ a well-drained position with a share of the animals were eartagged. Larval development assays
morning and afternoon sun. were performed at the diagnostic laboratories,
as required and when the facilities and expertise
Each farmer was given the freedom to design his own were available.
pen or to modify other designs. Each pen was then
evaluated by all project participants using a score sheet. Results, including faecal egg count (FEC), blood
Everyone benefited from the exchange of ideas and packed cell volume (PCV) and recommendations from
ultimately constructed the pen most appropriate to the project’s veterinarian, were provided to farmers
their circumstance. after every analysis. Part of the agreed participatory
monitoring and evaluation protocol was the regular
After constructing the pen, farmers were asked to confine sharing of experience by the farmers with the
their animals either all day long (complete confinement) secondary stakeholders (i.e. the local government unit
or just at specific times of the day or night (partial representatives) and the team. During these sessions, the
confinement), depending on the chosen technology mix. project researchers interpreted the worm profile per farm
About a month before the rainy season started, the as the farmers narrated their experiences, experiments
local government technician dewormed all the ruminants and lessons learned. These sessions doubled as
in the community to ensure that they were clean before in-course assessment periods.
testing started. To monitor the feeding activities, farmers

40
Subsidies/incentives given to farmers
for testing
Unlike traditional government programs, this project
did not give any incentives to farmers for testing the
technology options. From the start, it was emphasised
that this was not a goat dispersal project and that loans
would not be provided. The only benefit that the project
promised was knowledge empowerment through the
conduct of technology-based learning workshops.
However, to ease the financial burden on the farmers,
the local government units provided inputs such as
dewormers and forage seeds at the start of the project. Researchers and farmers both make important contributions
to developing new ideas and technologies. (G.D. Gray)
In Liloan, a focal site in the Visayas, the local government
units even constructed animal housing for four of the
six cooperators, with the agreement that costs be
repaid after a set period of time. immediately sell or slaughter affected animals to prevent
further losses. Farmers made little attempt to consult
Although farmers initially found it difficult to operate
veterinarians or seek advice from livestock experts,
independently (especially in Liloan), after almost two
primarily because goats were not a priority commodity
years they have demonstrated that they no longer need
or a significant program of the local government.
to rely on the local government units.
TAG 443-Philippines introduced baskets of technology
Farmer-generated technology baskets options revolving around worm control but including
strategies for all aspects of goat production management.
Free grazing or tethering of goats was the traditional Rather than choosing a single technology, farmers mixed
practice used by cooperators at the three project sites. and matched options to best fit their needs. Since each
Goats were allowed to graze freely or were tethered combination was chosen to suit individual conditions
in available communal pasture during the day and they were identified as farmer-generated baskets of
placed under a tree in the backyard or makeshift shelter technologies. This differs significantly from the traditional
at night. Housing for goats, although provided by a approach of experts coming to a village with ready-
few, was still considered an innovation at all the sites. made technology plans. The project’s strategy gave
Hence, worm infestation in goats was generally high. researchers opportunities to understand each farm and
Worm-related disease was the primary cause of gave the clients freedom to choose options based on
mortality and to cope with this farmers were forced to their perceptions and needs.

41
 Table 3.1 Farmer-generated baskets of technologies (FBTs)

FBT 1: Complete confinement is the banner technology of this basket. Specifically, animals were
Complete confinement completely confined during the rainy season but were allowed to graze freely in summer.
+ strategic deworming Animals were housed and fed grasses in stalls. Leaves of local trees and shrubs were given
as supplement. Goats were strategically dewormed a month before the onset of the rainy
season and the second dose, if necessary, followed at the peak of the rainy months. A
Developing and testing integrated approaches to sustainable parasite control in small ruminants with farmers

medicated urea molasses mineral block (MUMMB) was supplied within two months of the
rainy season and an improved buck was introduced in the herd to further upgrade their stocks.
FBT 2: Rapid rotational grazing is the primary component of this basket. However, for another farmer
Rapid rotational grazing who tested this on their pasture land, rotational herding was done (that is, continual movement
+ strategic deworming of a herd over a large area). For rapid rotational grazing, the pasture was divided into
10 paddocks and animals transferred from one paddock to another after 3.5 days. They
were housed at night and during inclement weather. Just as in FBT 1, grasses were cut and
carried to the stalls, tree leaves used as supplement, MUMMB supplied for two months of the
rainy season, strategic deworming employed, and an improved buck introduced.
FBT 3: This basket is the closest to the farmers’ traditional practice. Partial confinement and strategic
Partial confinement + deworming are its main components. Animals were confined at night and during inclement
strategic deworming weather. However, when the weather was good, they were either tethered and transferred
from one site to another predetermined non-grazed site every 3.5 days, or allowed to graze
freely. Even during rainy months, animals were allowed out of the pen so long as it was not
raining and the ground was dry. Animals were supplemented with tree leaves and shrubs upon
return to the pen, strategically dewormed, MUMMB-supplemented and mated to an improved
buck to further upgrade the stocks.

Ultimately, after months of testing, farmers came up with Resource requirements of the farmer-
three baskets of technologies (Table 3.1). These were
generated baskets of technologies
generated through a dynamic process with farmers
choosing an initial technology mix, testing it on their Housing, as explicitly detailed by Brown et al. (2003),
farms and making modifications or refinements until they was a requirement of all of the baskets. Most cooperators
arrived at the one that best suited their circumstances. adopted a housing design introduced by the project
with some farmers adapting and improving an adopted
design. Houses were made from cheap local materials:

42
wood, bamboo and used galvanised iron. Many
cooperators could obtain some of these materials
at no cost, however, for purposes of analysis, these
were assigned an estimated value to arrive at a more
accurate picture of the cost of the technology mix.
Some cooperators and members of their families
supplied the labour in the construction while others
hired labour to help. Whether family or hired labour
was used, a value was assigned to represent the
opportunity cost of labour.
Stall-feeding is a component technology common
to all farmer-generated baskets of technologies.
However, this practice is most intensive in FBT 1
Identifying market prices, trends and the demands of
with animals being completely confined and thus
consumers is essential for good technology development.
entirely dependent on gathered feeds. Labour for
(K.C. Patawaran)
gathering grasses and tree leaves and shrubs is the
most important resource required for this practice.
All cooperators opted to improve their stock using
Feed was abundantly available at the focal sites
improved bucks of the Anglo Nubian bloodline. Anglo
and could be freely gathered.
Nubian stock grows faster than traditional stock and
All of the farmer-generated baskets of technologies marketable size can be achieved after a much shorter
included chemical deworming. Initially, cooperators growing period. In addition, it has better reproductive
followed strategic deworming, which consisted of performance. Improved breeding could be done by
providing the animals with chemical dewormer a month purchasing an improved buck and making it part of the
before onset and during the peak of the rainy season. herd, by hiring a buck for natural insemination or by
However, cooperators later decided to deworm only using artificial insemination.
before the rainy season, primarily because animals were
confined and tree leaves (stall fed) with anthelmintic Baskets tested and criteria for adoption
action were available. Chemical dewormers were Of the 16 cooperators, only three were willing to test
provided to farmers at no cost through the local FBT 1 (complete confinement) at the start of the process.
government units but a value was assigned to determine Most farmers (11 out of 16) initially chose FBT 3 (partial
the costs incurred by farmers if they were required to pay. confinement), as this was most similar to their traditional
The three technology mixes also used MUMMB as a way of raising goats. However, eight of the original 11
dewormer, but only during the initial stage of the project. farmers who opted for FBT 3 eventually shifted to FBT 1.

43
 Reasons cited for rejecting partial confinement and ■ Better social relationships — once goats are
opting for complete confinement were as follows: confined, there is less conflict with neighbours as
the goats are prevented from trampling on other
■ Better time management — complete confinement
people’s crops and gardens.
allows more time for other chores and commercial
enterprises. ■ Better nutrition management — farmers who tried
FBT 1 believed that they were better able to choose
■ Better disease management — as reflected in
Developing and testing integrated approaches to sustainable parasite control in small ruminants with farmers

appropriate forages and balance the nutrition for

their monthly FEC-PCV monitoring sheets, fewer
their goats with stall-feeding than with tethering.
incidences of morbidities (worm and respiratory-
Moreover, once they had learned about the use of
related) were recorded, as goats were prevented
tree leaves and shrubs, they were able to establish
from feeding in contaminated pastures and protected
forage gardens near their goat sheds, reducing
by the pens from the harsh weather. Fewer deaths
the need to transport forages from field to shed.
were also observed.
Two of the three farmers who began with, and stayed
■ Ease of operation — farmers do not have to
with, FBT 3 also wanted to shift to FBT 1, but neither
bring goats to grazing areas four times a day,
had the resources to do so. One was a widow tending
run to secure them when it rains and haul them
a store, without any house help and the other did not
back when the rain stops. Farmers are no longer
have enough money to expand his animal pen. Only
exhausted from looking after grazing goats and
one farmer was completely happy with FBT 3 and had
looking for pastures with enough green grasses.
no plans to shift. This farmer had almost 40 goats in
■ Pastureland need not be available — farmers December 2002 and unlimited access to 5 ha of
without much land can run a goat enterprise pasture land near his homestead. Although he has
through complete confinement; available land occasional problems with parasitism, he feels that his
can be used for other crops throughout the year, animals are better nourished through his practice of
hence can contribute to higher farm productivity. rotational tethering in the field.
■ Not labour intensive — when goats are confined, Only two farmers were willing to try FBT 2 — rapid
only one person is needed to gather feed, clean rotational grazing. Both had access to vast lands that
the pen, give water and perform other minor chores. could be divided, if not with fences, by stakes. They
When animals are allowed to graze, at least also had surplus manpower to help transfer animals
three people are needed to ensure that the herd is from paddock to shed and back to paddock. Moreover,
in one place and to bring them home without loss. since their stock sizes were quite large, totally confining
all the animals and stall feeding them one by one was
seen as impractical.

44
Resource endowment (e.g. labour, capital, land) served
as the primary consideration for farmers when choosing
a particular technology mix. This was followed by ease
of operation, the effect of the technologies on the
animals and the effect on social relations.

Modifications made by farmers

After testing technologies in the field, some farmers were
keen to adapt the options to better suit their needs and
situation. Pen design and operation, in particular, were
critically assessed and adapted by farmers. Some Increasing pen elevation makes it easier to collect dung.
modifications are listed in Table 3.2 and shown in
the photos below.

Table 3.2 Problems identified by technology

testing and corresponding
modifications made by farmers
Emerging problem Modifications made

Difficulty in collecting Increased elevation of pen

dung beneath pen 1–1.2 m
Installation of catching net
Difficulty in controlling Construction of more
breeding ‘goat rooms’ or partitions
Mineral block eaten Reshaping of block to
by goats simulate salt lick
Difficulty in hardening Rolling of block on hot cemented
mineral block floor for three consecutive days
and every other day thereafter

Farmers can easily modify technologies if they see

increased survival of kids and increased income;
urea mineral blocks (above). (K.C. Patawaran)

45
 Benefits to farmers from participatory Table 3.3 Biological benefits from
technology development technology testing
Philippines Vietnam
Decreased morbidity and mortality Increase in stocks 192% 69%
and increased stocks
Decrease in morbidity Jan 2001 Dec 2002
Developing and testing integrated approaches to sustainable parasite control in small ruminants with farmers

In the Philippines and Vietnam, stock sizes increased 53.0%

as farmers tested the FBTs. The increase in stocks can
2.0%
be attributed to a decrease in worm-related diseases
% change 96.2% 58%
and mortalities (Table 3.3), which, in turn, was due to
improved competence in goat management. The data Decrease in mortality Jan 2001 Dec 2002
imply that adoption of FBTs was effective in controlling 56.0%
worm-related production losses.
2.0%
% change 96.4% 51%
Cost–benefit
(Alo et al. 2003, Binh et al. 2003, Venturina et al. 2002)
The FBTs had a positive financial impact as indicated
by the net incremental income figures listed in Table 3.4.
These figures consider both the benefits and costs Table 3.4 Cost–benefit of technology testing
associated with the technology mixes. As stock numbers
increase, and the initial costs of establishing the Farmer-developed basket Net incremental
of technologies income 2001–02
enterprise are reduced, income continues to rise.
FBT 1 complete confinement 4, 872 ($97.44)
These improvements are large considering that most
cooperators started with a small number of stock (some FBT 2 rapid rotational grazing 16, 840 ($336.80)
with just three animals). The number of females in the FBT 3 partial confinement 3, 702 ($14.04)
initial herd determined, to a large extent, the net benefit
derived from the project. As discussed earlier, the
primary benefit derived from the FBTs was a reduction
in mortality rate. Therefore, as female stocks multiplied
it became possible to engage in breeding (Brown
et al. 2003).

46
Increased personal competence Table 3.5. Farmer knowledge improvements
The human and social dimensions also showed from technology testing
rewarding improvements. Knowledge levels improved Mean knowledge
by 548% and attitude by 75%. Farmers also developed
Tobor Danao Liloan
their skills in managing and increasing their stock,
establishing forage gardens, designing animal pens, Jan 2001 11.2 3.5 2.2
experimenting (testing, observing, and deducing) with Dec 2002 24.7 22.75 23.6
different options, detecting parasitism and administering (%) rate of change 120.0 550.0 972.7
proper deworming protocols (Alo et al. 2002). Mean change 547.6%

Improved social competence

Farmer participation in technology testing also
■ Commercial visibility — participating farmers have
affected the way farmers dealt with people outside
also gained recognition as commercial sources
their households and the way their social environment
of good stock. The farmers take pride in having
treated them. Specifically, there were marked
established a better price for goat meat. In Tobor,
improvements in the following:
the farmers united to peg the price to P100/kg
■ Farmer-to-farmer extension activities — other farmers liveweight during lean months and P150/kg during
who saw the improvements on participating farms peak season. As they have been known to produce
sought advice and the farmer cooperators were able good quality stock, buyers now accept the price
to teach them what they had learned. Of the 284 that they set.
people who visited the 16 cooperators, 99 pursued
■ Community strength — the common experience
similar goat enterprises in their villages. This can be
generated a strong bond between the participants.
expressed as a 35% influence on the cooperators’
In Tobor, farmers felt that they could now mobilise
social environment and 450% increase in
each other for support. In establishing their forage
technology testers.
garden, for instance, they were able to get seeds
■ Departure from local government unit dependency from the local government unit, from the project
syndrome — initially, some farmers at one site and even from one of the cooperators who had
depended largely on their local government unit established a Napier garden (i.e. Pennisetum
for support for de-wormers, detection of parasites, purpureum, a large grass that grows in bamboo
forage garden materials and even housing materials. like clumps and is used for forage and windbreaks).
As their competence improved, there was marked They are now united by the common goal of making
departure from this dependency (Table 3.5). their individual village a respected source of goats.

47
 ■ Personal confidence and wealth — the confidence References
levels of all cooperators have increased from the
lowest to the highest rating: they believe they can Alo, A.M.P. 2003. Basket of option development and
make their goat enterprises booming businesses in evaluation: an analysis of the efforts of TAG 443
participating countries. Report submitted in preparation
the near future. Farmers felt extremely wealthy after
for 2003 ILRI-IFAD Steering Committee Meeting. Los
two years with the project, not just because they
Baños, ILRI.
were able to sell goats, but primarily because they
Developing and testing integrated approaches to sustainable parasite control in small ruminants with farmers

were able to reduce mortality. Above increase in Alo, A.M.P., Villar, E.C., Gabunada, F.G. Jr, Venturina, V.M.,
income, they valued the experiences, knowledge, Cruz, E.M., Lambio, E.T. and Salgado, T.R. 2002.
contacts and skill that they gained and the Community-based integrated approach to goat worm
control: a modality for community empowerment?.
opportunities all these initial gains might bring them.
In: Recent developments in animal production—2002:
Moreover, they were enormously proud to have
Proceedings of the Philippine Society of Animal
helped pull 35% of their community out of poverty.
Science 39th National and 20th Visayas Chapter
Scientific Seminar and Annual Convention, Cebu
City, 23–25 October 2002. 18–xx.
Conclusions
Biggs, S.D. and Smith, G. 1998. Beyond methodologies:
■ Within the participating communities there coalition-building for participatory technology
was a transformation from individual to group development. World Development, 26(2), 239–248.
empowerment. Personally and socially the farmer
Binh, D.V., Ly, N.D., Gray, D.G., Saithanoo, S. and
cooperators increased their capacity and strength
Sani, R.A. 2003. Participatory testing technology
to do things for themselves. They were able to
options in Vietnam. Report submitted in preparation
influence 35% of their community (99 other farmers) for 2003 ILRI-IFAD Steering Committee Meeting.
and help them to try the new technologies. Los Baños, ILRI.
■ With the development of the right mix of Brown, E.O., Alo, A.M.P., Cruz, E.M., Venturina,
technologies by the actual technology-users, V.M., Villar, EC, Gabunada, F.G. Jr and Lambio, E.T.
researchers need not push for their adoption. 2003. Financial analysis of the basket of technology
The technologies will spontaneously diffuse, from options for goat worm control. Draft paper submitted
farmer to farmer, throughout the entire community, for inclusion in the TAG 443-Philippines M&E report.
pulling more and more families out of poverty Los Baños, ILRI.
(Alo et al. 2002).
■ This project clearly demonstrates that farmers can
be active participants who can bring intellectual
contributions to the development process.

48
Cramb, R.A. 2000. Processes influencing the successful Subandriyo. 2003. Participatory diagnosis and site
adoption of new technologies by smallholders. selection in IFAD TAG 443. Report submitted in
In: Stur, W.W., Horne, P.M., Hacker, J.B. and Kerridge, preparation for 2003 ILRI-IFAD Steering Committee
P.C., ed., Working with farmers: the key to adoption Meeting. Los Baños, ILRI.
of forages technologies. Canberra, ACIAR Proceedings
Venturina, V.M., Cruz, E.M., Alo, A.M.P., Lambio, E.T.,
No. 95, 11–22.
Villar, E.C., Gray, D.G. and Gabunada FG Jr. 2002.
Gabunada, F.G. Jr, Alo, A.M.P., Villar, E.C., Venturina, Assessment of farmer-developed worm control options
V.M., Cruz, E.M. and Lambio, E.T. 2003. Harnessing in goats under smallholder management systems
essential agencies to sustain efforts on goat worm In: Recent developments in animal production—
control: experiences of the TAG 443-Philippines 2002: Proceedings of the Philippine Society of
project. Draft paper submitted for inclusion in the Animal Science 39th National and 20th Visayas
TAG 443-Philippines M&E report. Los Baños, ILRI. Chapter Scientific Seminar and Annual Convention,
Cebu City, 23–25 October 2002.

49
4. Anthelmintic resistance in small ruminant parasites:
implications for smallholders in Southeast Asia
G.M. Hood

Introduction
In developed countries where anthelmintics have been This chapter reviews the current status of anthelmintic
continuously used for the past 30 years, resistance to resistance in Southeast Asia, and examines the
broad-spectrum anthelmintics is now widespread, and implications for smallholders, for whom anthelmintics
threatens the viability of sheep and goat enterprises offer one key to the control of parasitism and the
(Waller 1997a). In many parts of Southeast Asia, small development of enterprises based on small ruminants.
ruminants are raised in backyards by resource-poor Alternatives to the use of anthelmintics — such as
farmers. Broad-spectrum anthelmintics are considered nutritional strategies and grazing management —
expensive and used infrequently, except by relatively are also considered, since these have significant
wealthy farmers and on government farms. As a result, potential for reducing the selection pressure for
although anthelmintic resistance has been found in many anthelmintic resistance.
countries in the region, it has not yet reached the
alarming prevalence reported in the major sheep-raising
countries of the southern hemisphere (Waller 1997a). Anthelmintics used in Southeast Asia
Rising global demand for livestock products (Delgado Almost all of the anthelmintic groups used in developing
et al. 1999), however, makes intensive and semi- countries are also available in Southeast Asia (see
intensive production of small ruminants an increasingly www.worminfo.org/anthelbase). However, their
attractive enterprise for smallholders in Southeast Asia. availability to smallholders depends on the wealth of
This development is likely to increase stocking rates, the local community, proximity to drug stores, and the
with a concomitant rise in the intensity of parasitism. whims of local government units, which sometimes
Anthelmintics comprise a powerful tool in the suite provide free or subsidised anthelmintics for smallholders.
available for controlling gastrointestinal parasites, and In the Philippines, benzimidazoles are widely available,
so conservation of their efficacy is an important goal levamisole/tetramisole products are harder to find,
for livestock development agencies in Southeast Asia. and macrocyclic lactones are available primarily from

51
 veterinarians or drug stores in large towns. For example, is also likely to occur through the use of poor quality
a recent survey of 19 drug stores (Patawaran et al. generic products. The quality of anthelmintics used
2003) found that benzimidazoles were available and in Southeast Asia has not been assessed, but studies in
recommended in 95% of stores, levamisole/tetramisole Africa (van Wyk et al. 1997, Wanyangu et al. 1996)
products in 63%, and the macrocyclic lactone group sold indicate that some generic products have sub-optimal
in smaller quantities (16% of stores). Narrow spectrum concentrations of the active ingredient.
drugs and piperazine and its derivatives were also
available. There seems to be a bias among veterinarians
and other experts toward benzimidazoles: 106 of 119 Tests for anthelmintic resistance
Anthelmintic resistance in small ruminant parasites: implications for smallholders in Southeast Asia

Philippine experts surveyed by Ancheta et al (2004) Most investigators in Southeast Asia have used the in
recommended the use of benzimidazole products, vivo faecal egg count reduction test (Coles et al. 1992)
while only one recommended levamisole/tetramisole, to detect anthelmintic resistance. This intuitive test is
even though the most popular benzimidazole product readily applied in large flocks and herds (more than
(albendazole) can be toxic to pregnant goats. In other 15 animals) but needs a follow-up visit for the second
countries, levamisole and tetramisole, which are sample, and can overestimate the prevalence of
comparable in price to the benzimidazoles, are levamisole resistance (Grimshaw et al. 1996, Maingi
both recommended and readily available. et al. 1998). It is also less precise than in vitro methods
Most poor livestock keepers do not buy anthelmintics (Le Jambre 1996). The in vitro egg hatch essay (Le
for strategic drenching programs. Instead they use ad Jambre 1976) is useful for detecting benzimidazole
hoc treatments for sick animals or locally grown herbal resistance, and has been used in peninsular Malaysia
remedies. When anthelmintics are used, it is likely to (Rahman 1993). A new in vitro test, the larval
be at sub-optimal doses. Drug stores in Southeast Asia development assay (Hubert and Kerbouef 1992, Lacey
usually stock broad-spectrum anthelmintics in small, often et al. 1990), has been used in recent work in Indonesia
single dose, packages because smallholders can rarely and the Philippines (Ancheta et al. 2004, Beriajaya
afford to treat more than one or two animals. Single- et al. 2003, Venturina et al. 2003). It has two principal
dose preparations can lead to under-dosing if used for advantages over other methods: first, it provides
heavy animals. For example, 220 mg mebendazole quantitative results for levamisole and benzimidazoles,
capsules are only sufficient for 18 kg animals, and 2 g and a qualitative result for the macrocyclic lactones;
sachets of levamisole hydrochloride for 20 kg animals. second, it needs just a single sample — no follow-up
The availability and high price of these products, visit is required. The second feature means it can be
in combination with low levels of literacy and poor used in smallholders’ flocks and herds or at markets and
understanding of dose rates, means that under-dosing abattoirs (Venturina et al. 2003). It should therefore
is probably frequent in Southeast Asia. Under-dosing now be possible to obtain accurate estimates of the
prevalence of anthelmintic resistance.

52
Prevalence of anthelmintic resistance
Most of the sheep and goat producing countries
of Southeast Asia have reported some degree of
anthelmintic resistance. In Indonesia, which has the
largest population of small ruminants, low levels of
resistance to benzimidazoles have been detected
on the island of Java (Beriajaya et al. 2003), but no
resistance was detected to benzimidazoles, levamisole
or ivermectin in surveys conducted in Sumatra (Dorny et
al. 1994b). In the Philippines, benzimidazole resistance
was first reported in Haemonchus contortus in Mindanao
(Van Aken et al. 1994), and has since been reported
from many locations throughput the Philippine islands Faecal egg count reduction tests, egg hatch and larval
(Ancheta and Dumilon 2000, Venturina et al. 2003). development assays can be used to identify resistant
Resistance to levamisole is apparently less common, worms. (G.D. Gray)
probably reflecting usage patterns (Ancheta et al. 2003).
Farmers in Malaysia and Thailand are relatively wealthy The study of Dorny et al (1994a) is one of the few in
compared with those in other countries of the region, Southeast Asia to yield an estimate of prevalence based
and anthelmintics are therefore used more often. Studies on a random sampling procedure. The survey included
on small numbers of goats in Thailand (reviewed in a substantial proportion of the national goat population
Kochapakdee et al. 2002) indicate that benzimidazole (2.3%) and is therefore likely to have yielded a good
resistance is present, but that resistance has not yet estimate of prevalence — albeit using a selection
emerged to levamisole or the macrocyclic lactones. procedure that is not convincingly random. Other
In nearby peninsular Malaysia, however, suspicions estimates of prevalence in Southeast Asian countries
of resistance to benzimidazoles and levamisole were depend on purposive sampling (i.e. targeted, non-
first reported by Dorny et al (1991), benzimidazole random sampling) schemes, and have almost certainly
resistance was confirmed in 1991 (Dorny et al. 1993) yielded biased estimates. In particular, government
and levamisole and ivermectin resistance were reported and large commercial farms, which notoriously use
by Sivaraj and Pandey (1994). Subsequently, national suppressive treatments, are over-represented in almost all
surveys found 50% of sheep farms and 75% of goat surveys (e.g., Ancheta et al. 2003, Chandrawathani
farms had benzimidazole resistance, and resistance to et al. 1999). There is, therefore, a clear need for active
levamisole, closantel and ivermectin was also detected surveillance of anthelmintic resistance using statistical
(Dorny et al. 1994a). sampling procedures (Cochran 1977).

53
 (a potential larval refuge) is correlated with decreased
efficacy (Ancheta et al. 2004). Beriajaya et al (2003)
have shown that resistance is easily transferred to
smallholders by dispersal of stock from government
farms. The quantitative importance of stock transfer
remains unknown. Refugia — locations where eggs
and larval nematodes escape exposure to anthelmintics
— are more common in the humid tropics than in major
sheep producing regions of the world, and so dilution of
emergent resistance alleles should be expected. It would
Anthelmintic resistance in small ruminant parasites: implications for smallholders in Southeast Asia

nevertheless be prudent for managers of government

farms to apply quarantine drenching treatments before
Introducing anthelmintic resistance by transfer of stock dispersing stock to smallholders. Quarantine treatment
is a potentially significant threat to smallholders. with several efficacious anthelmintics, either serially or
as a mixture, should minimise the risks of transfer of
worms carrying alleles for anthelmintic resistance.
Risk factors and transmission
Other risk factors such as farm size and size of animal
of anthelmintic resistance management group have also been identified (Ancheta
Worldwide, two factors have emerged as having et al. 2004, Venturina et al. 2004), but such factors
the greatest predictive value for anthelmintic resistance: are invariably colinear with drenching frequency and
frequency of treatment and transfer of stock. Of these, are therefore difficult to interpret.
high frequency of treatment is of overwhelming
importance (Martin et al. 1984) and has also
been most consistently associated with anthelmintic Implications for development
resistance in Southeast Asia (Ancheta et al. 2003, of small ruminant enterprises
Chandrawathani et al. 1999, Dorny et al. 1994a).
Gastrointestinal parasitism is widely regarded as
Importation of anthelmintic resistance by transfer of
the most serious constraint to the development of small
stock is a potentially significant threat to smallholders
ruminant enterprises in the humid tropics (Carmichael
because government and commercial farms, which
1993). Indeed, it can be argued that the tiny
serve as sources of stock for the larger smallholder
populations of sheep and goats in most Southeast Asian
sector, use anthelmintics intensively to reduce parasite
countries have already reached a carrying capacity
burdens and maintain high productivity of grazing sheep
dictated, not by feed resources, culture or markets, but
and goats. Recent evidence shows that importing
of stock and restricting access to shared grazing by intense challenge from gastrointestinal parasites.

54
To assess the impact of resistance on smallholders
we need to consider the three main farming systems
under which small ruminants are raised in Southeast
Asia: traditional tethering, stall-feeding, and extensive
grazing systems.

Traditional tethering
Tethering, mainly of goats, in backyards, on
wastelands, on crop residues and on roadsides is
practised throughout Southeast Asia. It is the dominant
method used for goats in the Philippines, and seems
designed to maximise the impact of coccidiosis and
helminthosis by ensuring close contact with faeces.
Faecal egg counts are higher in tethered animals
Laboratory procedures need to to be standardised and
than in grazed animals (Magona and Musisi 2002).
well managed. (G.D. Gray)
Also, the inability of tethered animals to select forages
probably decreases nutrient supply (Muir et al. 1995),
which is known to enhance the pathogenicity of The collected manure is composted with rejected feed
gastrointestinal parasites (Coop and Kyriazakis 1999). and used in a tightly integrated crop–livestock system
(Tanner et al. 2001). If grazing is precluded and houses
Tethered goats and sheep are primarily raised by are well designed, it is possible to reduce exposure to
the poorest smallholders. They are usually raised as a parasites under stall-feeding conditions (see Chapter 3),
sideline to cropping and receive little care. The owners but increases in parasitism and faecal egg counts in
cannot afford the suppressive anthelmintic regimes stall-fed systems frequently occur. For example, Knox
needed to minimise parasitism and have limited access (1990) reports higher worm burdens in stall-fed sheep
to livestock extension services (and furthermore do not in West Java (Garut) than in grazed lowland sheep
actively seek such services). Anthelmintic resistance is near Cirebon. Likewise, in Tanzania, diarrhoea and
consequently of negligible importance in this system. gastrointestinal parasitism were significantly higher in
stall-fed than grazed goats (Kusiluka et al. 1998).
Stall-feeding Exposure to helminth larvae in stall-fed animals probably
occurs through faecal contamination of floors and
Stall-feeding systems are dominant in the uplands of Java
feeding troughs (Kusiluka et al. 1998). Larvae are also
where most of Southeast Asia’s small ruminants are
introduced via forages, especially grasses, that are
raised. The houses used in these systems have a raised,
cut low to the ground (Nguyen Kim Lin et al. 2003).
slatted floor to allow faeces and urine to drain away.

55
 The area around houses is likely to be rich in helminth Holistic research is sorely needed for stall-feeding
larvae and provides another source of infection for stock systems. Such research should, at the very least, model
that are allowed to graze occasionally. the interactions between parasites, forages, livestock
and soil properties. As an example of the need for such
Javanese smallholders who practise stall-feeding do not
commonly use anthelmintics (Beriajaya, pers. comm.), research, consider the current upsurge in applied
but the combination of stall-feeding and anthelmintic research on the use of plants containing condensed
treatment can significantly improve productivity (see tannins to reduce parasitism in goats (e.g. Kahiya et
Chapter 3). A suppressive anthelmintic regime is used al. 2003, Nguyen Kim Lin et al. 2003). Cassava is
in one of the most productive stall-feeding systems for one such plant with high levels of condensed tannins.
Anthelmintic resistance in small ruminant parasites: implications for smallholders in Southeast Asia

goats — the SALT 2 demonstration maintained by the It can sustain high growth rates in goats (Nguyen Kim
Mindanao Baptist Rural Life Center in the Philippines Lin et al. 2003), but also rapidly depletes soil nutrients.
— in which more than a dozen milking goats and Leguminous forages, on the other hand, replenish soil
their offspring are raised on less than a hectare of nitrogen and have high levels of condensed tannins but,
forages (Laquihon and Pagbilao 1998, Partap and on fertile soils, produce less biomass per hectare than
Watson 1994). grasses or cassava. The optimum choice of forages
in any particular situation will depend on complex
The value of anthelmintics in stall-feeding systems, and
interactions among soils, livestock and parasites,
consequently the likely impact of resistance, is an open
and the economic factors that drive decision making.
question. Much research on helminths and the use of
anthelmintics in the humid tropics has used grazing stock;
the portals by which housed stock acquire infection and Extensive grazing systems
the interaction with control and treatment methods has Large-scale grazing of small ruminants is not commonly
been little studied. With good housing design, rigorous practised in Southeast Asia. For many years, intensive
enforcement of zero-grazing, and attention to the height research by the Small Ruminant Collaborative Research
at which forages are cut, it seems likely that stall-fed and Support Program (SR-CRSP) in Indonesia explored
animals could be maintained with limited or no recourse possibilities for increasing the productivity of grazing
to anthelmintics. It is also relatively simple to provide sheep and goats under plantation conditions in Sumatra
housed stock with strategic nutritional supplements and elsewhere (Horne et al. 1995, Iniguez et al.
to improve resistance to parasites, or with biological 1991). SR-CRSP research showed that — with effective
control agents such as nematophagous fungi (Waller anthelmintics and suppressive drenching programs —
and Faedo 1996). Including tree leaves in the diet it is indeed possible to graze small ruminants in the
— and perhaps those with high levels of condensed humid tropics and achieve high productivity (Horne et
tannins — could also help control parasitism and
al. 1995). But adherence to the required drenching
provide smallholders with a sustainable means of
income generation.

56
programs is difficult to maintain, and the growth of
small ruminant enterprises in Sumatra has occurred
primarily using stall-feeding systems (Sinulinga et al.
1995). In nearby Malaysia, some plantation owners
have turned to cattle, rather than small ruminants,
to avoid crippling losses from pneumonia and
helminthosis (Ibrahim 1996).
The emergence of anthelmintic resistance dims prospects
for unmanaged grazing of small ruminants in the humid
tropics. Resistance has yet to be reported from Sumatra,
but surveys of smallholder farms are being conducted
in South Sumatra in 2003 (Beriajaya, personal
communication), and experience elsewhere suggests that Training of extensionists and veterinarians increases their
the regimes used, for example, at Sungai Putih (Horne awareness of the resistance problems and the tests
et al. 1995), will inevitably lead to resistance. available. (K.C. Patawaran)

Grazing management could help reduce dependence

on anthelmintics in the humid tropics. A drench and move Conclusions
policy was used in the SR-CRSP research to minimise
dependence on anthelmintics, although reinfestation The population of small ruminants in Southeast Asia is
with worms to pre-treatment levels is reported to have unlikely to increase without major changes in current
practices to control worms. Improved practices are
occurred within four to six weeks (Horne et al. 1995).
discussed in this volume and have been amply reviewed
A particularly promising grazing strategy is rapid
elsewhere (eg, Waller 1997b). For immediate practical
rotational grazing (Barger et al. 1994) in which ten
implementation by smallholders, however, the strategy
plots are grazed in sequence for three and a half days
that stands out is wider adoption of stall-feeding systems.
at a time. This schedule ensures that stock are moved
Stall-feeding is growing in popularity in the Philippines
before eggs mature to the L3 stage, and do not return to
(see Chapter 3), Malaysia (Chandrawathani, personal
the same plot for more than a month. Owners of large communication), and Sumatra (Sinulinga et al. 1995).
flocks and herds might have the necessary discipline For smallholders, stall-feeding has many advantages
and fencing to adhere to such a rigorous grazing over grazing systems including:
schedule. For smallholders, however, the technique
has generally proved impractical (see Chapter 3).
■ a ready collection point for manure and urine
which is recycled as fertiliser for crops
■ parasitism and mortality rates being minimised

57
 ■ grazing damage to crops and fragile soils References
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5. Appropriate breeds and breeding schemes for sheep
and goats in the tropics
R.L. Baker and G.D. Gray

Introduction
The purpose of this chapter is two-fold. First, the just one component of adaptability) and productivity.
information available on breeds of sheep and goats Particular emphasis is placed on the need to better
that are resistant or resilient to helminthiasis (mainly the understand different farming systems in the tropics,
GI nematodes) infections are reviewed. This is important their production objectives and the different constraints
information for inclusion of appropriate breeds in to increasing productivity before embarking on genetic
integrated endoparasite control programs, which may improvement programs.
include resistant breeds or genotypes, improved nutrition,
strategic drenching, improved management (e.g.
housing animals in the wet season) and rotational Sheep and goat breeds that are
grazing (Barger 1996, Waller 1997, Alo et al., this resistant or resilient to endoparasites
volume). However, most of the breeds of sheep and
goats that have been identified as resistant or resilient Resistance to infections with endoparasites is defined as
are tropical indigenous ones. Many people, including the initiation and maintenance of responses provoked
in the host to suppress the establishment of parasites
smallholder farmers in the tropics, often perceive these
and/or eliminate parasite burdens. Resilience (or
relatively small indigenous breeds to be ‘unimproved’
tolerance) is defined as the ability of the host to survive
with low genetic potential for increased production.
and be productive in the face of parasite challenge
Almost invariably, larger breeds with higher growth
(Woolaston and Baker 1996). For livestock challenged
rates are assumed to be more productive and often
with GI nematode parasites the degree of resistance
the larger breeds are exotic breeds that are poorly
has usually been assessed in terms of worm counts at
adapted to tropical conditions. Therefore, the second
necropsy or faecal egg counts (FEC) during an infection
part of this paper discusses how practical breeding
period in live animals. In lambs it is well documented
programs in the tropics might be developed taking
that faecal egg counts are highly correlated with worm
into account both adaptability (disease resistance is
counts (Woolaston and Baker 1996). Resilience has

63
 been defined in terms of productivity (e.g. live-weight With a few exceptions most of these studies were
gain or wool production) under nematode challenge carried out in temperate environments in North America,
compared to productivity in non-infected animals (Albers Europe and Australasia. Some of the important
et al. 1987). In New Zealand, resilience has been conclusions from reviewing these publications
defined as the number of anthelmintic treatments are the following:
needed over a given period of pasture challenge
■ Host resistance to H. contortus has been
(usually several months) with nematode parasites
most commonly found. There is also evidence
(Bisset and Morris 1996). Packed red cell volume
for resistance to Ostertagia spp. and
(PCV) and mortality rates have also been used as
Trichostrongylus spp.
proxies for resilience (Baker et al. 2003). When
sheep are infected with the blood-sucking parasite ■ Resistance has been demonstrated both with
Haemonchus contortus they become anaemic and artificial infection and natural pasture challenge.
this is measured by PCV, which is a good indication Usually with natural challenge animals are exposed
of how the animal is managing to cope with the to several parasite genera with one or two
pathogenic effects of the parasite and to survive predominating.
Appropriate breeds and breeding schemes for sheep and goats in the tropics

when infected. However, other studies (e.g. Albers

■ Faecal egg counts (FEC) have generally been
et al. 1987) treated both FEC and PCV as two
used to measure resistance, but worm counts after
different measures of resistance.
necropsy have also been made. Resilience has
Much of the recent research on genetic resistance to GI usually not been assessed, but PCV has been
nematode parasites (endoparasites) in sheep and goats commonly measured and can be used as a proxy
has concentrated on quantifying within-breed genetic for resilience when H. contortus is the predominant
variation and selection of resistant (high responder) and nematode parasite. Production traits and mortality
susceptible (low responder) lines of sheep as reviewed rates have been recorded less frequently.
by Gray (1991), Gray and Woolaston (1991), Gray
■ Resistance has been demonstrated in both lambs
et al. (1995), Woolaston and Baker (1996) and Baker
and mature animals (ewes, rams and wethers).
et al. (2001, 2003).
■ It appears unlikely in sheep that differences in
However, there have been many reports since the
feeding behaviour among breeds is a major cause
mid-1930s of variation among breeds of sheep in
of resistance since many breeds have been shown
resistance to GI nematodes, particularly to Haemonchus
to be resistant both under natural pasture challenge
contortus, Trichostrongylus spp. and Ostertagia
and with indoor artificial challenge.
(Teladorsagia) spp. Gray’s (1991) review summarised
23 publications on this subject and this was expanded ■ The experimental design used in nearly all these
to 34 publications in a review by Baker et al. (1992). breed comparisons was poor. In particular, the
number of animals of each breed evaluated was

64
 too small (commonly about 5–10), very few studies
took account of variation among sires within breeds,
and sampling method was not stated. Requirements
for adequate experimental designs for breed
evaluation experiments have been comprehensively
reviewed and discussed by Dickerson (1969).
How animals are sampled and the family structure
(i.e. number of sires and progeny per sire) are
critical factors.
■ While the experimental design of many studies on
breed variation for resistance to endoparasites can
be criticised, it is reassuring to note that some breeds
have been identified as resistant in a number of
independent studies. This applies particularly to the
Introduced breeds of goat and sheep need to be assessed
Florida Native and Gulf Coast Native in the USA
for their ability to survive and reproduce in all conditions;
(Loggins et al. 1965, Bradley et al. 1973, Zajac
Anglo-Nubian buck. (G.M. Hood)
et al. 1988, Amarante et al. 1999a, 1999b,
Bahirathan et al. 1996, Miller et al. 1998, Li et al.
2001), the Barbados Blackbelly (Yazwinski et al. in tropical environments. While both the Barbados
1979, 1981, Goode et al. 1983) and the St. Blackbelly and St. Croix are tropical breeds that
Croix (Courtney et al. 1984, 1985a, 1985b, originated from the Caribbean, all the studies relating
Zajac et al. 1990, Gamble and Zajac 1992, to them quoted above were carried out in the USA.
Zajac 1995, Burke and Miller 2003) and for these However, there was anecdotal evidence in the
breeds it can be concluded that they are relatively Caribbean that the St. Croix may have been somewhat
resistant to GI nematodes. resistant to endoparasites (Hupp and Deller 1983).
In Southeast Asia nearly all the recent breed comparison
■ Most of the breeds identified as being relatively studies for sheep and goats (Table 5.1) suffer from the
resistant are indigenous or ‘unimproved’ breeds. same deficiencies in experimental design noted in the
This presumably reflects the fact that these breeds earlier reviews. However it is pertinent to note that the
have been under natural selection for resistance St. Croix has been shown to be resistant in studies in
for many centuries with no anthelmintic treatment. both Indonesia and the Philippines under very different
climatic (hot and humid) and management conditions
In the past 10 years or so there has been increased
than those used in the original studies carried out in
interest in characterising a number of indigenous tropical
the USA. Similarly, Barbados Blackbelly crosses were
sheep and goat breeds for resistance to endoparasites

65
 Table 5.1 Sheep and goat breed comparisons for resistance to internal parasites in Southeast Asia
Resistant Other Type of Age-months
breed(s)1 (no.) breed(s)1 (no.) Traits2 infect.3 Sp.4 (sex)5 Reference

SHEEP
Sumatra(S) (90) 1/2S-1/2St. Croix(106) E N Hc 3 Subandriyo et al. (1996)
St. Croix (22) 1/2S-1/2JFT(117) (M & F) Romjali (1995)
1/2S-1/2BB (65)
Sumatra(S) (10) E, P A Hc 18–24 Romjali et al. (1996)
1/2S–1/2St. Croix(10) (Rams) Romjali (1995)
1/2S–1/2BB (10)
1/2S–1/2JFT(10)
1/2S–1/2BB (10) Sumatra(S) (9) PPR N Hc 24 Romjali et al. (1997)
1/2S–1/2St. Croix(9) (Ewes)
Appropriate breeds and breeding schemes for sheep and goats in the tropics

1/2S–1/2JFT(7)
1/2Djallonke–1/2 Malin wool sheep E N Hc 3–12 Pandey (1995)
Malin wool sheep (M & F)
1/4 Djallonke–3/4Malin E N Hc 0–14 Sani (1994)
1/2 Dorset–1/2Malin (M & F)
St. Croix (39) Katahdin (27) E, P N Hc 3–8 Suba et al (2002)
Rambouillet (10) (M & F)
Philippine Native (30)
Indonesian Thin St. Croix (12) FC A Fg 6–12 Roberts et al. (1997a)
Tail–ITT (24) (M & F)
ITT (20) FC A Fh 6–12 Roberts et al. (1997a)
Merino (12) (M & F)
ITT (20) ITTxSt. Croix (20) FC A Fg 9–12 Roberts et al. (1997b)
St. Croix (10) (M & F)
1/2 Garole (G)–1/2 B, D, 1/2 E N Hc 3–7 Nimbkar et al. (2003)
Deccani (D) or B–1/2 D (192) (M & F)
1/2 Bannur (B) (75)
1/2 Garole (G)–1/2 B, D, 1/2 E, P A Hc 6–11 Nimbkar et al. (2003)
Deccani (D) or B–1/2 D (171) (M & F)
1/2 Bannur (B) (65)
continued over
66
 Table 5.1 continued
Resistant Other Type of Age-months
breed(s)1 (no.) breed(s)1 (no.) Traits2 infect.3 Sp.4 (sex)5 Reference

GOATS
Thai Native(12) 1/2TN–1/2AN(8) E, P, W A Hc 3–6 Pralomkarn et al. (1997)
3/4TN–1/4AN(8) (M & F)
Philippine Native (25) Anglo-Nubian (25) E, P N Hc 20+ Suba et al. (2000)
Boer (25), Saanen (25) (Does)
PN (41) Anglo-Nubian (47) E, P N Hc 8 Suba et al. (2002)
Boer (50) Saanen (14) (M & F)
(1) No. = number of records; BB = Barbados Blackbelly; JFT = Javanese Fat Tail; ITT = Indonesian Thin Tail (thin tail sheep from both Sumatra and Java); TN
= Thai Native; AN = Anglo-Nubian; PN = Philippine Native. (2) E = eggs per gram; P = packed red cell volume; W = worm count; FC = fluke count. (3)
N = natural infection from pasture; A = artificial infection. (4) Sp = parasite species; Hc = Haemonchus contortus; Fg = Fasciola gigantica; Fh = Fasciola
hepatica. (5) M = males; F= females

shown to be resistant in Indonesia. Although there is comprehensive studies carried out by the International
no strong evidence from the studies summarised in Livestock Research Institute (ILCA 1991, Baker et al.
Table 5.1 from Indonesia that the Indonesian Thin Tail 1999, 2002, 2003). We can now confidently conclude
sheep are resistant to H. contortus, some recent reviews that the Red Maasai breed is both resistant and resilient
(Subandriyo 2002, Raadsma et al. 2002) show that to endoparasites and particularly to H. contortus. In
this breed is more resistant than susceptible Merino addition to the sheep breeds that have been reasonably
sheep, but not as resistant as the St. Croix. In two small comprehensively characterised as resistant to GI
studies in Thailand and the Philippines native indigenous nematodes there are other interesting tropical breeds
goats were more resistant than Anglo-Nubian crosses or that may be resistant. This is based almost entirely on
purebred Anglo-Nubian and Saanen goats (Table 5.1). the anecdotal evidence that these breeds survive and
There is also some preliminary evidence in the thrive in the stressful environments where they are found
Philippines that Boer goats may be somewhat under severe disease challenge. These include the
resistant to endoparasites. West African Djallonke sheep which may be resistant to
both endoparasites and trypanosomiasis (Baker 1995,
Sheep-breed comparisons that have been carried out in
Osaer et al. 1999) and the Garole sheep in India
Africa are summarised in Table 5.2. In the case of the
(Ghalsasi et al. 1994). A study done in Maharashtra,
Red Maasai breed from East Africa there is an interesting
India (summarised in Table 5.1), comparing the
progression from the small studies originally undertaken
resistance to H. contortus of F1 Garole crossbred lambs
by Preston and Allonby (1978, 1979) to the
with that of Bannur, Deccani and 1/2 Bannur–1/2

67
 Deccani lambs, found that lambs with 50% Garole sheep, different feeding behaviour can account for
genes were significantly more resistant than the other differences in resistance. Saanen goats were shown
breeds and crosses tested and lambs with 50% or to have lower egg counts over a five-month period
more Bannur genes ranked second in resistance than Angora goats in an environment where both
(Nimbkar et al. 2003). It is worthy of note that the pasture and browse were available. This difference
Carribean St. Croix sheep originated from West was mainly explained by the fact that Angora goats
Africa and are probably related to the West African were predominantly grazers while Saanen goats
Djallonke sheep (Bradford and Fitzhugh 1983). were predominantly browsers.
It is also interesting that the Javanese Thin Tail and
Virtually all the research on genetic variation to
the Garole might be related since they both carry the
endoparasites in sheep and goats has concentrated on
FecB (Booroola) gene for prolificacy (Davis et al. 2002).
the nematode parasites. In many areas of the tropics and
The evidence for genetic variation for resistance to temperate regions of the world liver fluke (trematode)
endoparasites among goat breeds is limited (Tables infections (Fasciola hepatica and Fasciola gigantica)
5.1 and 5.3) and most of these studies suffer from are also an important constraint to sheep and goat
Appropriate breeds and breeding schemes for sheep and goats in the tropics

the same shortcomings in experimental design noted production (FAO 1992). While it is well documented
for sheep. As for sheep, it is usually the indigenous that sheep can mount an effective immune response
goat breeds (e.g. the Alpine goats in France and the (self-cure) to nematode parasites, it has been demonstrated
Small East African in Kenya) that are more resistant. that they are unable to acquire resistance to liver flukes
It is possible that the mechanisms or level of resistance (e.g. Haroun and Hillyer 1986, Boyce et al. 1987).
may be different in sheep and goats since, as goats This may be why there has been little research on genetic
are predominantly browsers, they are likely to have resistance to liver fluke infections and few studies
been under less intense natural selection for resistance published. Boyce et al. (1987) found significant breed
(Baker et al. 2001). Indeed, it is known that goats are differences in faecal egg counts and fluke counts after
innately more susceptible to nematode parasites than five breeds of sheep were experimentally infected with
sheep when they only have pasture available to graze F. hepatica. Barbados Blackbelly sheep were the most
(Pomroy et al. 1986), but the degree of susceptibility susceptible to infection while St. Croix and Florida
can differ for different parasite species (Gruner 1991). Natïve sheep were the most resistant. While none of
In those areas where browse is freely available it is the breeds demonstrated an ability to resist re-infection
often observed that the prevalence of endoparasites with F. hepatica, clear breed differences were detected
is higher in sheep than goats (Vercruysse 1983, in response to the primary infection. Wiedosari and
Papadopoulos et al. 2003). This may not tell us Copeman (1990) reported relatively high resistance to
anything about the relative resistance of sheep and F. gigantica in Javanese Thin Tail sheep, although there
goats to endoparasites, but could just reflect different was no contemporaneous breed comparison. Roberts
feeding behaviour, i.e., sheep are predominantly et al. (1997a, 1997b) compared the resistance to
grazers while goats are predominantly browsers. Hoste F. gigantica of Indonesian Thin Tail sheep (sampled
et al. (2001) also demonstrated that for goats, unlike from Java and Sumatra) with St. Croix sheep and F2
68
and F3 crosses between these breeds (Table 5.1).
They concluded that the Indonesian Thin Tail sheep
were more resistant than St. Croix sheep and that
resistance may be controlled by a major gene with
incomplete dominance. In contrast, the Indonesian
Thin Tail sheep were as susceptible to F. hepatica as
the Merino sheep that they were compared with
(Roberts et al. 1997a).

Adaptation and productivity of

sheep and goats in the tropics The Bach Thao goat in Vietnam is a synthetic breed
created in the early 20th century. (G.D. Gray)
It is now well documented that indigenous livestock that
have evolved over the centuries in the diverse, often
stressful tropical environments, have a range of unique Menz and Horro sheep evaluated in the highlands of
adaptive traits (e.g. disease resistance, heat resistance, Ethiopia (Tembely et al. 1998, Rege et al. 2002).
water tolerance, ability to cope with poor quality feed, However, under artificial challenge there was some
etc) which enable them to survive and be productive evidence that the Menz may be somewhat more
in these environments (Fitzhugh and Bradford 1983, resistant than Horro lambs (Haile et al. 2002). The
Devendra 1987, Baker and Rege 1994). In some most dramatic and most economically important breed
cases the physiological basis of adaptation has been effect in this study was for mortality rate for which the
investigated in great detail, as illustrated by the detailed overall cumulative mortality from birth to 12 months of
review of the physiological basis for the superior age was 37.3% for the Menz and 67.6% for the Horro
digestive capacity, efficient nitrogen economy and lambs. Mukasa-Mugerwa et al. (2000) investigated
efficient use of water in desert goats (Silanikove 2000). the causes of lamb mortality and found that the most
However, more commonly this detailed assessment is important cause of death for lambs from birth to
not available, but it is still possible to infer ‘adaptability’ 12 months of age was pneumonia, which accounted
by measuring total flock productivity, efficiency or net for 54% of all deaths. Endoparasite infections as a cause
benefits of different breeds (e.g. Fitzhugh and Bradford of mortality were of limited importance in both breeds
1983, Bosman et al. 1997, Ayalew et al. 2003). Some (accounting for about 10% of deaths). Mukasa et al.
recent studies will be described to illustrate this point. (2002) reported the reproductive performance of the
ewes in this experiment and overall flock productivity.
A study (summarised in Table 5.2) shows that under Menz sheep had a significantly higher weaning rate
natural pasture challenge there was no difference in (lambs weaned per ewe mated) than the Horro ewes
resistance to endoparasites between the indigenous

69
 Table 5.2 Sheep breed comparisons for resistance to internal parasites in Africa
Resistant Other Type of Age-months
breed(s)1 (no.) breed(s)1 (no.) Traits2 infect.3 Sp.4 (sex)5 Reference

Red Maasai (16) Merino (16) E, W A Hc 24–36 Preston & Allonby (1978)
Corriedale (16) (wethers)
Hampshire (16)
Red Maasai (10) BH Somali (10) E, W, S N Hc wethers Preston & Allonby (1979)
Merino (10)
Dorper (10)
Corriedale (10)
Hampshire (10)
Red Maasai (10) Dorper ewes (60) E, W,S N Hc wethers Preston &Allonby (1979)
Horro (32) BH Somali (32) E, P, W, N Hc 6–12 Asegede (1990)
Appropriate breeds and breeding schemes for sheep and goats in the tropics

Arsi (32) Adal (32) S, Bw (M & F)

Red Maasai (17) Dorper (17) E, P, S, SP, A Hc 6–8 Mugambi et al. (1996)
Eos, WG (entire males)
Red Maasai (15) BH Somali (15) E, P, S N Hc, Tsp 12–24 Mugambi et al. (1997)
Dorper (15) wethers
Romney (15)
Red Maasai (15) BH Somali (10) E, P, W A Hc 24–26 Mugambi et al. (1997)
Dorper (12) wethers
Red Maasai (28) Dorper (15) E. P A, N Hc 14+ Wanyangu et al. (1997)
ewes
Menz (1439) E, P N Le, Tsp 20+ Tembely et al. (1998)
Horro (1347) ewes
Red Maasai (463) Dorper (442) E, P, S N Hc, Tsp 20+ Baker et al. (1999)
RM x Dorper (786) Bw ewes
Red Maasai (1015) Dorper (1055) E, P, S N Hc, Tsp 15+ Baker et al. (2002)
Bw ewes
continued over

70
 Table 5.2 continued
Resistant Other Type of Age-months
breed(s)1 (no.) breed(s)1 (no.) Traits2 infect.3 Sp.4 (sex)5 Reference

Red Maasai (152) Dorper (95) E, P, S N Hc, Tsp 3–6 Baker et al. (2002)
Bw (M&F)
Menz (2395) E, P, S N Le, Tsp 0–12 Rege et al. (2002)
Horro (1966) Bw (M&F)
Menz (103) Horro (49) E, P, W A Hc, Le 4–12 Haile et al. (2002)
Bw Tc (M&F)
Red Maasai (212) Dorper (318) E, P, S N Hc, Tsp 0–12 Baker et al. (2003)
RMxD crosses (1255) Bw (M&F)
Sabi (1281) Dorper (607) E, P, S N Hc, Tsp 24+ Matika et al. (2003)
Bw ewes
(1) No. = number of records; BH Somali = Black-Head Somali; RM = Red Maasai; D = Dorper; SEA = Small East African. (2) E = eggs per gram; P =
packed red cell volume; W = worm count; S = survival; Bw = body weight; SP = serum protein; Eos = peripheral blood eosinophil counts; WG = weight
gain. (3) N = natural infection from pasture; A = artificial infection. (4) Hc = Haemonchus contortus; Tsp = Trichostrongylus species; Le = Longistrongylus
elongate; Tc = Trichostrongylus colubriformis; Oe = Oesophagostomum species. (5) M = males; F= females.

(0.73 vs 0.57) and ewes which lambed in the wet and about twice greater when they lambed in the dry.
season had a significantly higher (P<0.001) weaning rate These results clearly demonstrate that, at least in this
than those that lambed in the dry season (0.76 vs high altitude environment in Ethiopia, Menz sheep are
0.53). Menz ewes showed their superiority in weaning better adapted than Horro sheep even though we are
rate over the Horro ewes more clearly when lambing still unclear about the biological determinants of this
in the wet season (0.85 vs 0.67) than when lambing in adaptation. This study, and many others like it, was
the dry season (0.59 vs 0.47). Overall flock productivity carried out on a research station, which may not
was expressed in terms of potential offtake (number of necessarily reflect the situation that applies on
sheep sold) of yearling sheep from flocks of Menz or smallholder farms.
Horro ewes lambing in either the wet or dry seasons.
Another recent study in Ethiopia, this time with goats,
Both as number of yearling sheep and total liveweight
compared the productivity of an indigenous breed with
for sale, the offtake of a flock of Menz sheep in this
that of Anglo-Nubian and indigenous goat crosses
environment was about three times greater than a flock
(Ayalew et al. 2003). This study was particularly
of Horro sheep when they lambed in the wet season,

71
 Table 5.3 Goat breed comparisonsa for resistance to internal parasites
Resistant Other Type of Age-months
breed(s)1 (no.) breed(s)1 (no.) Traits2 infect.3 Sp.4 (sex)5 Reference

Saanen (12) SEA (12) E, W, S A Hc 24–36 Preston & Allonby

Galla (12) (1978)
Alpine Saanen E N Mixed Cabaret & Anjorand
(1984)
SEA (12) Galla (9) E, P, W A Hc 10–14 Shavulimo et al. (1988)
Toggenburg x SEA (13) S, Bw (M)
Alpine Saanen E N Oc, Osp, Does Richard (1988)
Alpine (44) Saannen (30) E N Tsp, Hc Does Richard et al. (1990)
Crossbreds (26)
SEA (8) AN cross (8) E, P N Hc, Tsp 10–12 Rohrer et al. (1991)
Appropriate breeds and breeding schemes for sheep and goats in the tropics

Togg. cross (18) (M&F)

DPG (16)
SEA (228) Galla (168) E, P, Bw N Hc, Oe, 12+ Baker et al. (1998)
Tsp does
Caninde (15) E, P N Hc 12–16 Costa et al. (2000)
Bhuj (6) (F)
Angllo–Nubian (15)
Saanen 10) Angora (14) E N Tsp, Tlsp, Does Hoste et al. (2001)
SEA (349) Galla (204) E, P, S N Hc, Tsp 0–14 Baker et al. (2001)
Bw (M&F)
(a) All published goat breed comparisons with the exception of those carried out in Southeast Asia which are shown in Table 5.1. (1) No. = number of
records; SEA = Small East African. (2) E = eggs per gram; P = packed red cell volume; W = worm count; S = survival; Bw = body weight. (3) N = natural
infection from pasture; A = artificial infection. (4) Hc = Haemonchus contortus; Tsp = Trichostrongylus species; Le = Longistrongylus elongate; Tc =
Trichostronngylus colubriformis; Oe = Oesophagostomum species; Tlsp = Teladorsagia species. (5) M = males; F= females

72
interesting because it was carried out with smallholder
farmers who had previously been the beneficiaries of
both crossbred goats and training in management of
goats as part of a comprehensive livestock improvement
package (FARM-Africa 1997). It also made a much
more comprehensive study of productivity. The net
benefits of goats to a household were calculated by
aggregating the value added by physical products
(meat, manure and milk) to socio-economic benefits
(saved interest/premium on credit/insurance) and
deducting purchased inputs. The result was then
expressed as net benefit to each main limiting resource
of a household: flock metabolic size, land and labour.
There were increased net benefits per unit of land or
labour from mixed flocks (i.e. those with both indigenous
goats and Anglo-Nubian crosses) under improved Indigenous breeds (such as the Philippine native goat),
management compared with indigenous goats under are well adapted to the highly variable and low input
traditional management. This could be due to the systems of most livestock keepers. (G.M. Hood)
crossbred goat, or the improved management or both.
It was then shown unequivocally that in flocks using the
superior adaptability in this environment of indigenous
improved management package the crossbreds did
goats and the importance of assessing this adaptability,
not produce more net benefits than indigenous goats
not just in terms of physical products (i.e. meat, milk and
either in mixed or separate flocks per unit of flock
manure) but also accounting for socio-economic benefits.
metabolic weight, per unit of land or per unit of labour.
These findings explained the low adoption rate of the Another important issue when assessing flock productivity
exotic crosses by the smallholder farmers. However, is to recognise the potential importance of genotype by
the improved management package was successful environment interactions. We concluded earlier from the
in improving the net benefits to farmers with indigenous studies summarised in Table 5.2 that Red Maasai sheep
goats. Therefore, it was concluded that household were more resistant to endoparasites than Dorper sheep.
welfare could be improved in the crop-livestock, mixed These studies were undertaken in many different locations
smallholder production systems of the Ethiopian highlands in Kenya, ranging from the sub-humid coast to the
by better management of indigenous goats without semi-arid highlands. Therefore, we can safely conclude
the extra organisational effort and cost of producing that there is no genotype by environment interaction for
crossbreds. This study also demonstrated again the resistance as the Red Maasai were consistently the most

73
 but this still ignores any differences between the breeds
in input costs (e.g. health care costs will be lower in a
Red Maasai flock than a Dorper flock) or socio-economic
benefits. The reason for this interaction was that the
Dorper sheep were very poorly adapted to hot humid
conditions, which was reflected in their low growth rates,
low reproductive rates and high mortality rates. The
conclusion from this study is that breed of choice in a
hot, humid environment is the Red Maasai, while in an
arid or semi-arid environment there is little to choose
between the two breeds. The Dorper breed was
introduced to Kenya in the 1960s. It has gradually
The Philippine native sheep has been bred from Merinos increased in popularity in the semi-arid Kenyan highlands
imported from Mexico. (G.M. Hood) mainly because of its size and growth potential and is
Appropriate breeds and breeding schemes for sheep and goats in the tropics

popular with the Maasai herdsmen who cross it with

their Red Maasai sheep. Judicious crossbreeding like
resistant breed in all the studies, although the magnitude
this may be justified as long as the crosses include at
of the difference in FEC between the Red Maasai and
least 50% Red Maasai blood to maintain at least some
Dorper breed was quite variable in different studies.
degree of endoparasite resistance (Baker et al. 2003,
The productivity and efficiency of Red Maasai and
Nguti et al. 2003).
Dorper sheep evaluated in experiments at the Kenya
coast (humid environment) and the Kenya highlands
(semi-arid environment) were compared by Baker et Constraints to improving
al. (2002). There were important breed by location
interactions for growth, mortality rates and reproduction
productivity in the tropics
rates. When all these parameters were combined it was Despite the well documented fact that most indigenous
found that the indigenous Red Maasai sheep were three sheep and goats in the tropics are well adapted to their
to five times more productive and efficient than Dorper stressful environments there is still a commonly held view
sheep in the humid-coastal environment. In the semi-arid that they are ‘unproductive’ because of, for example,
environment Dorper sheep were slightly more productive their small size and high mortality rates. This has resulted
than the Red Maasai, but there was no significant in many misguided livestock improvement development
difference in flock efficiency between the breeds. In programs importing exotic breeds, which are assumed
this study efficiency was measured as kg of total meat to be more productive based on their performances in
offtake per megajoule of metabolisable energy per day, their benign temperate environments of origin. Often they

74
cannot even survive in the tropical environments into Although the more detailed characteristics of tropical
which they are introduced. Although some development sheep and goat production vary from region to region
agencies are now appreciating the importance of an around the world, some constraints are common to
integrated systems approach to livestock improvement all tropical farming systems. The three broad categories
in the tropics (e.g. Ayalew et al. 2003) this has been of constraints are ecological, biological and socio-
the exception rather than the rule. economic (Fitzhugh and Bradford 1983). Most
production systems are affected by several of these
Before initiating any livestock improvement program
and often there are important interactions among them.
it is important to have a good understanding of the
production systems and the relative importance of the Ecological constraints include land (area, topography,
different constraints to production in these systems. The altitude, soil fertility) and climate (rainfall, temperature,
amount and distribution of rainfall are often principal humidity, growing season). Of these ecological
determinants of system characteristics. For sheep and constraints only soil fertility is readily amenable to
goat production in the tropics, two important systems human intervention and then only when improvements
are mixed crop/livestock farming systems in the medium are economically justified, which is more likely to be
to high potential agricultural areas and livestock-based the case in crop/livestock systems. In some large-scale,
grazing systems in the drier (arid and semi-arid) range commercial farming systems, shelter (e.g. trees or
or desert areas. Included in the crop/livestock farming buildings) can be provided to help lower heat stress.
systems are both small subsistence level farms, large In smallholder systems in the high rainfall tropical
commercial operations specialising in cropping with environments, confinement of sheep and goats during
livestock usually playing a secondary role, and also the rainy seasons is an option, although this also means
commercial operations with reasonably large livestock that labour must be available to provide feed in a cut
enterprises. In all these systems sheep and goat and carry system.
production is often secondary in importance to crops
Biological constraints include low quantity and quality
and other livestock activities. In pastoral, transhumant
of feed supplies, lack of drinking water (particularly
and ranch farming systems ruminants graze rangelands
in the arid and semi-arid grazing areas), high disease
to produce food and income. Cattle, sheep and goats
prevalence, theft and predation and perceived poor
are often managed in common herds under the care
genetic potential.
of owners, their family members or herders. During
the day these herds may travel considerable distances Socio-economic constraints include:
in search of grazing and water. However, with few ■ labour availability and animal husbandry skills
exceptions, they are closely confined at night as a
safeguard against predators and theft. Confinement of ■ taste preference and buying power of consumers
livestock at night is also a feature of the crop/livestock ■ cost and availability of credit
farming systems.

75
 ■ marketing infrastructure ■ choosing a breeding system and breed(s)
■ government policies on prices of commodities, ■ deciding on population size and structure
trade and land tenure.
■ identifying the selection criteria and, if appropriate,
It is commonly observed that traditional livestock deriving selection indexes
management practices in the tropics, developed
■ obtaining (or estimating if not available) genetic
by trial and error through generations of experience,
parameters (e.g. heritabilities and genetic
often make efficient use of available resources with
correlations)
minimal external inputs or risk to producers. For most
indigenous sheep and goat breeds in the tropics ■ designing the animal recording system
natural selection has resulted in genetic potential for ■ estimating breeding values for the selection
adaptation taking precedence over genetic potential criteria or an index
for productivity. Therefore, in many tropical farming
systems, genetic improvement for productivity (e.g. ■ designing a mating scheme for the selected animals
increased growth rate or milk production) often should
Appropriate breeds and breeding schemes for sheep and goats in the tropics

■ designing a multiplication scheme to disseminate

only be attempted once nutritional, health, management genetically superior animals or semen
and socio-economic constraints have been resolved.
■ assessing genetic change and reviewing the
Alternatively, all the important constraints should be
breeding program regularly.
addressed simultaneously in an integrated improvement
package. A more formal way of approaching integrated Descriptions of these steps have been published
improvement has been suggested and called ‘Livestock elsewhere (e.g. Ponzoni 1992, Harris and Newman
Development Objectives’ (Djemali and Wrigley 2002). 1994) and it is not within the scope of this paper to
describe them in detail. Rather, we will discuss the steps
in which breeding for adaptability and productivity in
Genetic improvement programs tropical sheep and goats requires special consideration,
Once the production systems and constraints to with particular attention to developing breeding
production have been characterised and quantified programs for smallholder farmers. It is important to
for a particular tropical environment or region then note that although the steps outlined above appear in
there are some logical steps that should be followed a linear order, in fact there is interdependency between
to implement a genetic improvement program. many of these steps, as will be illustrated later.
This would ideally include the following: During the process of quantifying constraints to
■ defining the breeding objective (i.e. the production and developing integrated livestock
improvement goal) development objectives it may become clear that

76
development of breeding programs should not be
attempted. For example, the small desert breeds
of goats such as the Black Bedouin are exquisitely
adapted to fragile desert environments after thousands
of years of natural selection (Silanikove 2000), and
the best breeding strategy now is to let natural selection
continue without external interference with either their
genetic potential or their desert environment.

Defining the breeding objective

At the outset of planning a breeding program the
targeted livestock production and marketing system Crossing Philippine native sheep with St Croix and
Katahdin has increased body size, litter size and reduced
should be defined and then all traits that affect the
wool cover. (G.D. Gray)
profitability of that system should be identified. Decisions
about which traits to target for genetic improvement
should ideally be based on the extent to which each objectives and REVs were refined as the data on input
trait affects profitability (per head or per unit of labour costs were obtained or derived (e.g. feed costs for
or land), not on whether the trait is difficult or easy to grazing livestock) to allow the calculation of more
measure or change genetically. This is of particular comprehensive profit functions (Ponzoni 1986).
relevance to disease resistance or adaptation, which In many tropical countries the economic data needed
are not always easy to measure or change genetically to develop comprehensive profit functions will be scarce.
and so are often ignored. Historically, breeding Efforts have been made to develop these functions for
objectives and relative economic values (REV) of hair sheep in Cuba (Ponzoni 1992) and in Kenya
different traits in the breeding objective were first (Kosgey et al. 2003, 2004). Solkner et al. (1998)
derived purely in terms of economic returns for different argue strongly that ‘The decisive but most frequently
traits (e.g. the dollar values for an additional kilogram missing step in the design of village breeding programs
of meat, an additional kilogram of wool or an additional is the definition of a breeding objective’. They also
lamb weaned) without any attempt to take into account suggest that breeding objectives must be formulated
the costs of production and develop profit functions. in close collaboration with smallholder farmers with
Although these may not have been optimally designed particular attention to the importance of risk avoidance,
breeding objectives they were still a good first step particularly in marginal environments. For many
in getting breeding programs established and genetic smallholder farmers in the tropics with hair sheep
progress was achieved. Over time the breeding or goats, a simple and practical breeding objective

77
 may simply be increased financial returns from meat crossbreeding system is chosen and it has stabilised,
production per unit of limiting resource (e.g. per head, then any further genetic progress can only be achieved
per unit of land, per unit of labour) or net income (which through selection within the new crossbred population.
may include income from meat, milk and manure) from In many tropical sheep and goat production systems
the sheep or goat unit. This is also the time when a there is often scope to use both between- and within-
rational decision can be made about whether a genetic breed genetic variation in breeding programs (Baker
improvement program is justified at all in terms of 1995, 1996, Woolaston and Baker 1996).
financial returns or increased profitability of the enterprise.
Choice of the most appropriate breed or breeds to use
Reports are conflicting about the profitability of small
in a sheep or goat enterprise should be the logical first
ruminants under traditional smallholder management
step when initiating a breeding program. However,
in the tropics, with some indicating low or negative
this assumes that sufficient information is available on
profitability (e.g. Soedjana 1996, Bosman et al. 1997,
which to make rational breed choices, which very often
Seleka 2001, Kosgey et al. 2003) and others
is not the case. Historically, and especially during colonial
profitability (e.g. Upton 1985, Itty et al. 2001).
times in Africa and Asia, it was assumed that the small
Appropriate breeds and breeding schemes for sheep and goats in the tropics

However, there is strong evidence from several of the

local indigenous breeds of livestock in the tropics must
studies showing a lack of profitability that smallholder
be unproductive and many larger exotic temperate
farmers often keep sheep or goats primarily as a ready
breeds of cattle, sheep and goats were imported to
source of cash income (e.g. acting as a bank), for
rectify this perceived problem. This was almost always
socio-cultural reasons (e.g. for use in ceremonies such
a mistake and these exotic breeds did not survive unless
as weddings or funerals), as an insurance against crop
they were given a level of care (e.g. management,
failure and for manure rather than just for production
feeding, disease control) that led to expenses far above
of meat or milk. When these additional factors are
anything smallholder farmers could afford. More recently,
included in the economic analyses then the production
that is, within the past 10–20 years, there has been
systems are profitable (e.g. Bosman 1997, Kosgey
increased interest and awareness of the many unique
et al. 2004).
attributes that the indigenous hair sheep breeds and
indigenous goat breeds in the tropics have to offer.
The breeding system This is well illustrated by the studies summarised in
The three pathways of genetic improvement are Tables 1–3. For example, in Southeast Asia:
selection among breeds or populations (e.g. strains ■ St. Croix and Barbados Blackbelly sheep have
within breeds), selection within breeds and crossbreeding been used in crossbreeding programs in Indonesia
designed to exploit heterosis and/or combine the (Merkel et al. 1996, Subandriyo et al. 1996,
merits of different breeds. These genetic improvement Subandriyo 2002)
options are not incompatible, but once a particular

78
■ Djallonke, Santa Ines, St. Croix, Barbados
Blackbelly and Thai Long Tail have been
evaluated in Malaysia (Ibrahim 1996)
■ Vietnam has imported the Barbari, Jamunapari
and Beetal goat breeds from India and the Boer,
Saanen, Anglo-Nubian and Alpine goats from the
USA (Binh 2003)
■ In 1998 the Philippines imported the St. Croix,
Katahdin (a St. Croix-Suffolk stabilised cross), and
Rambouillet Merino sheep breeds, plus the Saanen,
Anglo-Nubian and Boer goat breeds from the USA.
Often, even when the merits of different breeds have
been compared, the decision should be made to utilise,
and perhaps improve, the local indigenous breed. A Shepherds in India are evaluating crosses between the
good example is the Red Maasai sheep breed in the highly prolific Garole, locally adapted Deccani and
humid climatic zones of Kenya. The two most important the high-carcase quality Bannur breeds. (G.D. Gray)
biological constraints to production in this environment
are endoparasite infections (predominantly H. contortus)
and quantity and quality of feed. There is increasing regime should be those that are more resistant and/or
evidence documenting the spread of anthelmintic resilient to endoparasites and there is no need to have
resistance in Kenya (Wanyangu et al. 1996). So, it to resort to recording FEC or PCV to ascertain this.
is important to use a breed that is resistant and/or Due consideration would have to be taken of animal
resilient to endoparasites and that needs minimal or no welfare issues in such a management system to ensure
treatment with anthelmintic drugs if kept on an adequate that mortality rates were kept to a manageable level.
level of nutrition. Smallholder farmers almost invariably Management strategies can also be developed to
rank increased size and growth potential as important permit drenching of individual animals that are clearly
traits they would like to increase in their sheep and suffering from the effects of endoparasites and will
goat flocks (Kosgey, pers. comm., Jaitner et al. 2001). die if not treated. For infections with H. contortus the
In this situation a simple and practical breeding simple FAMACHA test developed in South Africa is a
program may be to select the heaviest purebred Red useful diagnostic tool (Vatta et al. 2001). This test is
Maasai rams in a management system where they based on a colour chart with five colours depicting
are exposed to endoparasites while grazing and not varying degrees of anaemia, which are compared
drenched. Those that survive under such a management with the colour of the mucous membranes of the eyes

79
 of sheep or goats. Those animals with the palest eye weight of 42 kg. One can immediately see the large
colour are severely anaemic and should be treated. effect derived from combining the additive effect of two
Depending on the proportion of rams treated from breeds even if there is no heterosis, and this increase
birth until the age they are selected for breeding (e.g. will be achieved in one generation. However, it may
commonly about 12–15 months of age) this can be not be as simple as this. If the local breed has an annual
included in the selection process as an independent mortality rate of 20%, but the exotic breed in the new
culling level. For example, it may be possible to identify environment is not adapted and has a mortality rate of
a reasonable number of rams that were never drenched 50%, then the F1 cross with no heterosis is expected
over this period and then within this group the heaviest, to have a mortality rate of 35%. It can easily be shown
functionally sound (i.e. no structural defects) animals that this increase in mortality rate will often be of far
greater importance in terms of its effect on total flock
could be selected. Such a breeding scheme would
productivity or profitability than the increase in growth
not result in a rapid rate of genetic change in growth.
rate (e.g. Upton 1985).
If a rate of 1% per year was achieved, this would mean
that rams that averaged 30 kg at one year of age Breeds can be used in crossbreeding programs in four
Appropriate breeds and breeding schemes for sheep and goats in the tropics

initially would be 33 kg after 10 years of selection. main ways. These are substitution of an existing breed
This is not a dramatic change and many farmers are by a new breed, new breed formation based on crossing
looking for a quicker response. The easiest way to two or more breeds, specific crossbreeding in a stratified
do this is to embark upon a crossbreeding program. breeding system and rotational crossbreeding.
Combinations of these different crossbreeding programs
The benefits of crossbreeding schemes are (1) to
are also possible.
combine the merits of different breeds and (2) to utilise
heterosis (also commonly called ‘hybrid vigour’). Heterosis Breed substitution
is measured as the extra performance of the crossbred
If the new breed (B) is clearly more desirable than
over the average of the parental breeds. The increase
the original local breed (A), then one can just keep on
in performance ranges from 0 to 10% for growth traits
‘backcrossing’ with that breed until, after about four to
and from 5 to 22% for fertility and mortality traits. These
effects are additive, so for combined production traits, five generations, breed A has effectively been replaced
like weight of lamb weaned per ewe mated per year, with breed B. For example, if the original sheep breed
heterosis commonly ranges from 15 to 25%. As a simple was an indigenous hair breed and there was a desire
example, if a local breed has a mature weight of 30 kg to establish a wool industry then backcrossing with a
and another breed (maybe an exotic imported breed) breed such as a Merino or a Corriedale would achieve
has a mature weight of 50 kg, then a first cross (F1) that aim. This was exactly how the Merino and Corriedale
animal is expected to have a mature weight of 40 kg breeds were originally established in the highlands of
(half 30 kg + 50 kg) if there is no heterosis. If there Kenya where they are reasonably well adapted.
is 5% heterosis for this trait then the F1 will have a mature

80
When the same approach was followed in hot and
humid environments the new breeds were not at all
adapted and usually did not persist. It is also possible
to introduce new breeds to a country or region by
importing live animals, semen or frozen embryos
although these are more expensive options. The recent
importation of Rambouillet Merino sheep from the USA
into the Philippines is a good example of importing
a new breed that is poorly adapted to the hot humid
environment. In contrast, the St Croix hair sheep
imported from the USA into Indonesia, Malaysia and
the Philippines (Table 5.1), have proved to be much
better adapted to the hot, humid climates found in
these countries both as purebreds and in crosses
with indigenous breeds.
New breed formation
The Red Maasai sheep are resistant to worms and highly
The simplest way to form a new breed is to cross breed productive in areas of high parasite challenge. (R.L. Baker)
B with breed A to form a first cross (F1 = B x A), then
mate B x A males with B x A females (inter-se mating)
to form an F2 population and then continue the process Africa (Milne 2000). Selection can take place during the
of interbreeding to the Fn generation (often called a interbreeding phase to ultimately produce a new breed
composite or synthetic breed). This was the method used with desired characteristics — for example, improved
to produce the Coopworth (Border Leicester x Romney) reproduction and fleece weight in the Coopworth (Coop
and Perendale (Cheviot x Romney) breeds in New 1974) and minimal wool production and certain colour
Zealand and the Dorper (Black-headed Somali x Dorset patterns in the Dorper (Milne 2000). It is possible to
Horn) breed in South Africa. Usually breeds are chosen combine more than two breeds to form a synthetic, which
because they have attributes that breeders want to has the advantage of combining the attributes of more
combine into the new synthetic breed. For example, the breeds but the disadvantage is that the logistics of breeding
Dorper breed was produced to combine the adaptive are more complicated. For example, the Kenyan Dual
merits of the Black-headed Somali hair sheep with the Purpose goat was produced by interbreeding the local
growth and milk production of Dorset sheep. The final Galla and Small East African breeds with the exotic
result was a hardy meat breed that did not need shearing Toggenburg and Anglo-Nubian breeds (Mwandotto
and was productive under harsh veldt conditions in South et al. 1992).

81
 Specific and rotational crossing As a rule of thumb, a closed nucleus breeding flock
should include a minimum of about 150 breeding
These crossbreeding schemes require a reasonable
females mated to at least five breeding males with
flock size (e.g. about 50 or more breeding females)
breeding males being replaced annually with a male
so are not of interest to smallholders with small flocks.
offspring and breeding females being kept in the flock
However, they can be employed by pastoralists who
for no longer than three to four matings. However, the
often have larger flock sizes. The simplest example of
larger the nucleus flock the better as this allows larger
a specific crossing system is the use of a terminal sire
selection intensities and lower inbreeding rates to be
breed (B) on a proportion of the flock (about 30–40%)
achieved. Ponzoni (1992) recommended that a closed
to produce F1 progeny (B x A) but with the rest of the nucleus flock of 500 breeding females and seven new
flock being straight-bred (A x A) to supply female sires per year should be ‘the absolute minimum below
replacements. Often all F1 progeny are sold or which the establishment of elite nucleus flocks should
slaughtered for home consumption. Many Maasai not be contemplated’.
pastoralists in Kenya follow this sort of system by using
the Dorper breed as a terminal sire over their Red Maasai
Selection criteria and breeding values
Appropriate breeds and breeding schemes for sheep and goats in the tropics

flocks. However, the F1 female progeny can be quite

productive in the breeding flock when maintained under It is important to make the clear distinction between
reasonable feeding and management conditions. the traits in the breeding objective which are identified
Rotational crossbreeding may then be used to mate the solely on the basis of their economic importance to the
F1 females. For example, B x A F1 females could then enterprise and the selection criteria, which are the traits
be crossed back to A sires and their progeny to B sires, actually measured in the flock to predict the breeding
etc. Alternatively, a new breed (C) could be introduced objective. If, for example, the breeding objective was
and mated with the B x A females to produce 3-way increased meat production, then possible selection
cross progeny [C x (B x A)]. These 3-way crosses may criteria may be body weight taken at different ages
then all be sold or slaughtered or included back into the (e.g. at weaning or at market age), female reproduction
breeding program. Historically, this sort of trial and error rate and mortality rates. In the temperate developed
crossing of different breeds is what has probably world there may also be measurements of carcass
occurred and if productive progeny are the outcome then quality such as fatness or meatiness which can be
ultimately these can evolve into new breeds or strains. estimated on the live animal using ultrasonic
measurements. However, this is only justified if the market
rewards the producer for improved carcass quality, which
Population size and structure
is rare in the temperate developed world and almost
The important factors here include the number of males non-existent in the tropical developing world. However,
and females in the breeding nucleus which then affect in some markets (e.g. the Middle East) fat-tailed sheep
the selection intensities that can be achieved and the command a considerable premium and this trait could
inbreeding rate (Falconer 1989, Kinghorn 1995). therefore be a factor in deciding which breed to use.

82
Selection criteria need to be able to be measured, one set of parameters for a wide range of circumstances.
heritable, variable and correlated with the traits in For many disease resistance traits such assumptions are
the breeding objective. Heritability is the efficiency questionable as there is a physiological interaction
of transmission of parental phenotypic superiority to between pathogen activity and production which may
the next generation and, in theory, can vary from mask the underlying genetic relationships (see the review
zero to one, but for animal production traits it varies of Woolaston and Baker (1996) for a detailed
from zero to about 0.60. It is possible that the traits discussion of this issue with regard to resistance to
in the breeding objective may also be selection criteria. endoparasites). There is now good evidence for sheep
If, for example, the breeding objective is increased in temperate climates that resistance to a number of
milk production then the obvious selection criteria diseases (e.g. endoparasites, footrot, blowfly strike) is
to measure is milk production of the does or ewes. moderately heritable (0.20–0.40), although heritability
However, it is not possible to measure milk production on of resilience to endoparasites is lower (about 0.10).
the males in the population and they must be selected However, there is limited evidence for the heritability
either on breeding values derived from milk records from of disease resistance in tropical sheep and goats.
their female progeny or from their female relatives (e.g. It appears that resistance to endoparasites in resistant
dam or grand-dam). The breeding value of a particular breeds like the Red Maasai may be very lowly
trait for an animal is a description of the value of that heritable (Baker et al. 2003). Similarly, resistance
animal’s genes to its progeny. The genes an animal to endoparasites in goats in the tropics has been
carries are not known so we never know what the true reported to be very lowly heritable (e.g. Woolaston
breeding value is but it can be estimated from heritability et al. 1992), but some recent studies have been
estimates, the records of the individual (i.e the phenotype) more encouraging and suggest moderate estimates
and, if available, records of the individual’s relatives (Baker et al. 2001).
(Falconer 1989, Kinghorn 1995).
Some traits are expensive, impractical or impossible
Heritability estimates are low for fitness traits such as to measure and this includes some of the production
reproductive rate and mortality rates (0.01–0.10), traits (e.g. lifetime productivity, feed intake of grazing
moderate for growth and milk production (0.2–0.3) animals, carcass quality, behaviour) and many of the
and high for carcass quality traits (0.4–0.5). In theory, disease resistant and adaptability traits (e.g. metabolic
genetic parameters such as heritabilities and genetic efficiency, water tolerance, heat tolerance). In some
correlations are specific to a population and a given cases indirect measures have been developed but
environment. In practice, estimates of these parameters in others measurable traits do not exist at present.
for the production traits (e.g. reproduction, growth) However, where breeds or genotypes have been
have been found to be relatively robust across breeds demonstrated to have the required attributes such as
and different environments and it is common to assume disease resistance or adaptability, then these genetic

83
 qualities can be harnessed by using those breeds or by bucks) or semen. This structure works well as long
crossbreeding with them without any need to resort to as the nucleus breeding flocks are achieving genetic
within-breed selection. It is also important to remember improvement. This genetic improvement then flows
that the rate of genetic progress per generation in a through to the commercial sector. If, however, the
breeding flock is proportional to the selection intensity nucleus flocks are not making any genetic improvement
(which is a constant for a given breeding structure), the then no improvement will flow through to the commercial
degree of variability (i.e. the phenotypic variance) and flocks. Historically, the registered stud industries in many
the heritability (Falconer 1989). Some of the traits which developed countries put a lot of emphasis on traits not
are lowly heritable, such as reproduction rate, are also always closely related to productivity or profitability such
extremely variable and the expected rate of genetic as colour, type and body shape. In Australia and New
progress of about 2% of the mean per year is similar Zealand open and closed group breeding schemes
to what is expected from traits such as growth or milk were established originally as a way of breeding
production which have moderate heritabilities but are livestock with emphasis on productivity and provided
less variable. FEC, which is commonly used as a competition with the more traditional stud industry for
Appropriate breeds and breeding schemes for sheep and goats in the tropics

predictor of resistance to endoparasites, is highly provision of breeding stock. Today the registered stud
variable and usually has an over-dispersed skewed industry displays a very different attitude, with many
distribution. Even when transformations have been breed societies encouraging, or making mandatory,
applied to FEC to normalise the variance (e.g. the recording of economically important traits (Hammond
logarithms or square root), it still tends to be a fairly et al. 1992). Many tropical developing countries
variable trait with a moderate heritability at least in do not have breed societies and their existence is not
susceptible breeds. It must also be remembered that essential to achieve genetic improvement. However,
while selecting for several different traits may be it is most unlikely in most tropical developing countries
justified, the more traits that are included as selection that performance recording will be logistically feasible
criteria the less genetic progress that will be made in large numbers of smallholder or pastoralist flocks.
for each one of them. For this reason, some form of open or closed nucleus
breeding structure has been widely advocated so that
Industry structure and dissemination the performance recording effort can be concentrated
of genetically improved animals in one large nucleus flock or several reasonably large
ones (Ponzoni 1992). Often the nucleus flocks have
The developed world contains well documented been established on government research stations and
breeding structures where genetic improvement takes while this may have been successful initially when external
place in a small proportion of the total industry (e.g. funding was available, when this ceased these flocks
nucleus breeding flocks or the registered stud industry) were often disbanded (Madalena et al. 2002). There
and then genetic improvement is passed on to the are also questions about whether the management
commercial industry through sale of males (rams or systems that are adopted on well-funded government
84
research stations are relevant to the environments under
which the improved genotypes are expected to perform
in low-cost, low-input smallholder systems.
Once nucleus breeding has been successfully
implemented there is usually a need to establish a
multiplication tier of farmers to ensure that reasonably
large numbers of rams or bucks are available for the
commercial industry. Jaitner et al. (2001) have discussed
some of the constraints to doing this in relation to nucleus
breeding schemes for Djallonke sheep and West
African Dwarf goats which have been initiated by the
International Trypanotolerance Centre in The Gambia.
They highlighted, in particular, the constraint of individual
farmers’ small flock sizes (2–3 breeding females) and
suggested that a possible solution was to establish
village flocks as multipliers. This resulted in a combined
flock size of about 30–50 ewes or does which would
then be mated to improved rams or bucks from the
nucleus once all the breeding males in the villages
had been sold or castrated.
Recently, plant breeders have been carrying out breeding
Choice of buck and timing of mating can be controlled
programs in some tropical countries in collaboration by keeping males and females separate for most of the
with smallholder farmers (e.g. Eyzaguirre and Iwanaga year. (G.M. Hood)
1995, Bellon and Reeves 2002). For example, farmers
evaluate different crop varieties and give their views on
what they consider are the important crop characteristics. develop farmer-assisted breeding programs, there is
FAO and ILRI are developing and testing ‘breed survey scope for some innovative research and development
guidelines’ which, among other things, seek farmers’ on this topic.This could take place in smallholder
views on important livestock characteristics and their flocks, use modern participatory methods to gain
perceptions of the value of different breeds and strains insights into how smallholders make decisions about
of livestock (Rege and Rowlands, pers. comm.). Although livestock and set breeding objectives, and use DNA
it may be more difficult with livestock than plants to technology to assist with identification of parentage.

85
 Conclusions breeds with particular attention to their adaptation
to stressful tropical environments. Adaptation in the
■ The experimental design used to evaluate sheep tropics includes not only disease resistance but also
and goat breeds for resistance to endoparasites heat resistance, tolerance of water shortages and
needs to be improved. In particular, attention needs the ability to cope with poor quality and quantity
to be paid to the number of sire families evaluated of feed.
per breed with a minimum of 15 required and
■ Prior to initiating any livestock improvement
a minimum of five offspring per sire family. The
programme in the tropics it is important to have a
15 sires should also be as unrelated as possible.
good understanding of the production systems and
At least two breeds must be compared in each
the relative importance of the ecological, biological
experiment.
and socio-economic constraints to production in
■ Despite the poor experimental design used in many these systems. Genetic improvement programmes
published studies there is now good evidence from usually should only be attempted once the nutritional,
a number of independent studies that some tropical health, management and socio-economic constraints
Appropriate breeds and breeding schemes for sheep and goats in the tropics

sheep breeds are resistant and/or resilient to have been resolved.

endoparasites (predominantly Haemonchus contortus).
■ Crossbreeding programmes with non-adapted
These include the East African Red Maasai, the
imported breeds should be discouraged for low
Florida Native and Gulf Native in the USA and
input smallholder systems in the tropics. However,
the Barbados Blackbelly and the St Croix from the
crossbreeding among the indigenous tropically
Caribbean. The Indonesian Thin Tail sheep have
adapted may be an option in some farming systems.
been shown to be resistant to the liver fluke
Fasciola gigantica. ■ Within breed genetic improvement programmes is
a feasible option for many tropically adapted breeds
■ There is much less evidence for breeds of goats
of sheep and goats.
that are resistant to endoparasites but the Small
East African goat in Kenya and the Alpine goat
in France have been shown to be resistant breeds.
■ There is strong evidence that breeds of sheep and
goats that are indigenous to the tropics have much
more to offer for small-holder farmers than is often
appreciated. There is an urgent need for more
comprehensive breed evaluation studies that assess
the total biological and economic productivity of these

86
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6. Options to overcome worm infection in small
ruminants for producers in Nepal
R.K. Bain, B.R. Joshi, D. Gauchan and G.D. Gray

Introduction
The kingdom of Nepal is a landlocked country lying inhabited, or are uninhabited, with most land above
between India and China, on the southern slopes 5500 m being permanently snowbound.
of the Himalayas. The country has a land area of
The climate and therefore the natural environment
147,180 sq km. It is 800 km from east to west and
of the country are influenced by two factors. First, Nepal
varies from 144 to 240 km north to south, between
is in sub-tropical latitudes so that temperatures at low
longitudes 80–88°E and latitudes 26–31°N.
altitudes are warm to hot. Superimposed upon, and
The three main physical regions of the country are modifying, this potentially subtropical climate are the
based broadly on altitude. To the south of the country effects of altitude and aspect, which result in markedly
is the terai which is fertile, flat, low-lying land between diverse microclimatic temperature and rainfall conditions.
50–300 m and 25–32 km wide. Rising from the terai Hence the natural environment can show great variation
plains, at an altitude of 300–2500 m, and following an within a particular location.
east/west alignment, are two ranges of hills collectively
The climate of the terai is subtropical, with the natural
referred to as the mid-hills. Lower elevations of this region
seasons being determined by the monsoon rains which
are known as the Siwalik (or Churia) Hills and higher
affect the entire Indian subcontinent. In the low to mid-
elevations as the Mahabharat Lekh Range. Between
hills (300–2500 m), the climate is classified as warm
the Mahabharat Lekh and the high Himalayas, covering
temperate and above this, between 2500 and 4500 m,
elevations from 2500–5000 m, are another series of
cool-temperate. The high hills (2500–5500 m), comprise
mountains commonly referred to as the high-hills. The
an alpine zone, while above 5500 m, the temperature
high-hills ring a transitional zone and generally align
is almost always below freezing point.
north/south as a result of the rivers draining through them
from the high Himalayas. To the north of these high-hills Rainfall varies from as little as 500 mm per annum, in the
are the Himalayas proper at 5000–8800 m, aligned rain shadow areas to the north of the high Himalayas,
east/west and including the highest mountains in to over 5000 mm in areas to the south of some of
the world. These last two zones are either sparsely the major Himalayan massifs. For most of the country,

97
 average rainfall lies between 900 and 1900 mm per Reducing poverty and commercialising subsistence
annum, becoming progressively drier from east to west. agriculture are key government goals. The Ninth Plan
The greater part of this rain falls during the monsoon, which started in 1997 emphasised poverty alleviation
between the middle of June and the end of September. and aimed to reduce the proportion of those living below
In general, there are four major and distinct seasons the poverty line from 42% to 32% by 2002–03. This
in Nepal: winter (December–February); spring was to be done largely through growth of the agricultural
(March–May); summer (June–August); and autumn sector. The Agricultural Perspective Plan (APP 1995)
(September–November). placed increased emphasis on livestock development
to generate national economic growth and improve the
livelihood of the rural poor in the hills and mountains.
Economy The contribution of livestock is projected to increase,
Annual per capita GDP in Nepal is about USD 220. from the present level of 31%, to 45% by the end
With a human development index of 0.332, Nepal of the plan period (2015). Highest growth has been
ranks 151st out of 174 countries (the average in South estimated for the hill and mountain regions of the
Asia is 0.444) (IFAD 1998). Life expectancy at birth country. Within the livestock sector, the contribution of
Options to overcome worm infection for small ruminant producers in Nepal

is 54 years, infant mortality is estimated at 98 per small ruminants is 12% but this needs to be substantially
thousand and only 31% of the adult population (only increased in future to achieve the planned levels of
13% of the women) are literate. The daily calorie growth and improvements in rural poor livelihoods.
intake is estimated at 1957 per capita.
With the present population growth rate of 2.3% Livelihoods analysis and poverty focus
per annum and a growth rate of less than 3% in the
Using a livelihoods analysis approach, a range of
agricultural sector, Nepal faces an increasingly serious
indicators pertaining to the five classes of capital, as
risk of food deficit and poverty. Marginal farmers, small
defined by Carney (1998), were considered. On the
farmers and the landless account for 89–96% of those
basis of these indicators, it was apparent that poverty
living below the poverty line in rural areas. Just over
increases from the plains to the mountains. There is also
half the population live in the hills and mountains and
a trend for the more remote districts in the west of Nepal
60% of this group live below the poverty line (APP,
to be poorer than their more accessible counterparts
1995) compared with 42% in the terai. Holdings of less
to the east.
than 1 ha account for 82% of the total in the mountains
and 77% in the hills, compared with only 59% in the Capital access
terai (CBS 1998). Land holdings tend to be smaller
Table 6.1 provides a summary of some of the indicators
in the hills (0.7 ha/household) and mountains (0.8 ha/
examined and the proportion of districts in each region
household) compared with the terai (1.3 ha/household).
that are in the lowest third of the country’s ranking. It is

98
evident from Table 6.1 that, by most measures, the hill disasters which, in the past, have brought famine
and mountain regions are ranked lower than the terai. to remote districts. Landslides are not unusual, while
In particular, access to natural resources is a constraint hailstorms, earthquakes, droughts and floods are all
in the hill districts, while access to financial, social and reported in the literature as being past causes of distress.
physical capital, all highlight the problems of remoteness Rinderpest has been present in the past and peste des
in the mountain districts. petites ruminantes is a threat to the sheep and goat
livestock system that has the potential to seriously
Vulnerability context
threaten livelihoods.
Population growth in Nepal is about 2.3% per annum,
which is limiting access to natural resources in the hills.
The population of the hill districts rose by 45.5% Role of small ruminants
between the census of 1981 and that of 1991, while Livestock contribute 31% of Nepal’s GDP and small
the mountain districts’ population rose by only 7.8%. ruminants 12% (LMP 1993; APP 1995). Small ruminant
In part, population growth in the mountain districts is production is an important component of mixed farming
reduced by outward migration, although this appears systems and an important source of cash generation
to be a destabilising influence on the farming system and livelihood for resource poor farming communities
and may further erode aspects of social capital. (including women and marginal farmers) who are unable
There is a trend towards improved access and to invest in large ruminants. These animals are an
communication as roads and telecommunications important source of liquid assets for poor farm families
permeate the more remote districts. Farmers in the hills and women during famine, illness and emergencies.
and mountains are vulnerable to occasional natural Goat meat has wide acceptance in all the communities

Table 6.1 Poverty indicators used in the study

Type of capital Terai Hills Mountain Indicator

Human 8.6 million 8.4 million 1.4 million Population

Natural1 0 62 6 Natural resource endowment index
Financial1 5 39 50 Agricultural credit uptake
Physical1 15 33 56 Socio-economic infrastructural development index
Social1 40 23 50 Women’s empowerment index
1Percentage of districts in each region that fall in the lowest third of national ranking for each index.
Source: Districts of Nepal, Indicators of Development (ICIMOD 1997)

99
 Small ruminants raised by poorer farmers do not attract
the attention of the mainstream scientific establishment
and little effort has been made to improve their economic
prospects. Cash resources are limited and uptake of
credit low. Together with poor access to technology
and information, these constraints limit farmers’ ability
to use capital intensive techniques.

There is increasing conflict over lands used for grazing

Sedentary goat production
and forestry which can be reduced by confining goats. in the hill districts
(G.D. Gray)
Farming systems

and ethnic groups in Nepal. The demand for both Most farms in the hill districts are small-holder mixed
goat meat and live animals in rural and urban areas enterprises. Cropping areas are mainly terraced,
Options to overcome worm infection for small ruminant producers in Nepal

is increasing for consumption and religious sacrifices. producing rice, wheat, barley, maize, potatoes and
The price of goat meat has more than doubled in vegetables. Both rain-fed and irrigated systems are
the past five years compared with that of poultry and found and agro-forestry is practised. Livestock consist of
buffalo meat, indicating its importance and unfulfilled cattle, buffalo, goats and poultry. Forests are used as
demand for it. Women contribute significantly to a forage resource for grazing and browsing livestock.
livestock raising, providing 70% of the work effort Livestock contribute manure and traction to the crop
and are reported to be more knowledgeable than system and benefit from by-products and weeds from
men about treating sick animals (APP 1995). the cropping areas.

Mountain communities prefer to raise sheep for meat, Livestock management

wool and manure production. Sheep wool production Small ruminants, particularly Khari goats, are managed
also provides income and employment opportunities for in sedentary systems in the hill districts. Goat management
rural women. Woollen products (hand-made carpets, practices are influenced by location, availability of
blankets, Pashmina) produced from sheep and goat pasture and communal grazing, availability of family
wool are major sources of rural income and livelihoods. labour, cropping pattern of the area and market
Hand-made carpets and Pashmina shawls are the major prospects. Animals are kept in one area throughout the
export products of Nepal. year and are penned at the homestead at night. Night
pens are normally small sheds made of local materials,
which may or may not be raised constructions with

100
slatted floors. They may be semi-stall-fed or stall-fed Sick animals are treated as and when is necessary,
(Ghimire 1992). However, grazing on waste or fallow first by traditional methods and then by veterinary ones
land and browsing in bush or forest areas close to the if the animal does not recover. Many ethnoveterinary
village are more common. Because of limited availability practices are used, for example, leaves of Cannabis
of fodder and pastures in grazing land, in many places indica for the treatment of scour and garlic bulbs for
the animals are routinely supplemented at the stall with plant poisoning. However, the effectiveness of these
grasses, straw or fodder tree leaves. Food grains and is uncertain.
salts may also be provided. Animals are watered during
Helminth problems
the day on the way to grazing.
Parasitic diseases (including gastrointestinal nematodes,
With present management techniques, productivity is
liver fluke and external parasites) of small ruminants
low, there is little selection or breeding control and some
are regarded as the most important cause of reduced
relatively unproductive animals may be maintained and
productivity among goats in sedentary management
compete for scarce feed resources. Throughout the year,
systems in Nepal. Parasitic diseases were ranked first
goats must compete with cattle and buffalo and poor
by farmers and this view has been further supported by
pasture quality forces animals to use forest resources.
studies showing superior response by animals treated
Continuous grazing of the same limited grazing areas
with anthelmintics. Infection is mostly confined to the
may contribute to the build-up of heavy parasite burdens
wet summer months, with low levels of infection during
and contribute to low productivity.
the winter and dry summer months. The main nematode
Animal health issues in small ruminants genera found are Haemonchus, Trichostrongylus and
Oesophagostomum, with Cooperia, Strongyloides and
Diseases and parasites are regarded as major
Bunostomum being found less often (Joshi 1997, 1999).
constraints to production in the sedentary production
system. In fact, farmers ranked disease as the first Trichostrongylus and Oesophagostomum may be the
constraint to increased productivity of sedentary goats. cause of the goat diarrhoea reported by farmers while
Various diseases (reported on a symptomatic basis) have Haemonchus on its own (or in combination with Fasciola)
been reported in goats and sheep under sedentary may be a significant cause of mortality or reduced
management. Among them, the prominent causes of productivity on these farms.
losses are diarrhoea, fever, respiratory problems, skin
The effect of gastrointestinal nematodes on animal
infections, worm and fluke infections, foot and mouth
production was evident in studies in which the growth rate
disease, contagious ecthyma and coenuriasis. In addition
of the animals given regular anthelmintic treatment was
to the common problems, peste des petits ruminants and
higher relative to untreated animals reared alongside
setariasis have also been reported, in some parts of the
(Joshi 1998). The daily weight gain of anthelmintic-
country, during the past few years.

101
 treated kids was up to 2.5 times that of untreated kids
under sedentary conditions. These responses show
that controlling parasites can greatly improve goat
productivity in this system.
Options for helminth control
The following options, either alone or in combination,
could help to reduce the effects of helminthiasis in
sedentary flocks. These options might form a suitable
list from which farmers could choose most-favoured
options for further study, as part of participatory on-
farm adaptive research. They are:
■ controlling grazing to avoid the most heavily
contaminated areas
Options to overcome worm infection for small ruminant producers in Nepal

■ managing grazing to minimise build up

of infection in grazing areas
■ managing manure to prevent spread of eggs
Most farms in the hill districts are small-holder mixed
and larvae from housed animals
enterprises. (ACIAR)
■ increasing stall feeding to reduce pasture intake
during risk periods
■ treating kids strategically with anthelmintics to
■ avoiding grazing completely during the riskier
suppress build-up of infection during risk periods
wet months
■ using supportive therapy for sick goats including
■ using cut and carry forage grasses and weeds
symptomatic treatment to permit survival and
to boost nutrition and enhance resilience
recovery, for example, protein and energy
■ using anti-parasitic tree forages such as mulberry supplementation and anti-scouring agents
to reduce parasite burden
■ managing breeding to reduce the number of
■ using nutritional supplementation purchased as susceptible animals present during the risk periods.
by-products such as rice polish and mustard cake
Based on currently available technology options a
■ using non-conventional feeds for goats such possible advisory note for people in sedentary systems
as poultry manure and brewers grain appears in the Appendix to this chapter.

102
Sedentary system case study — Pyughar Village
Goat production is an important source of livelihood Constraints to goat production
for the farming community in Pyughar village (Deurali
There are several critical constraints to smallholder goat
VDC) of Tanahu district, in the western hill region of
production in the village. Farmer-perceived constraints
Nepal. It is a small village (55 households) located
were listed after group discussion with 14 farmers and
at an altitude of 400 m, on the bank of the Seti river
then pair-wise ranked. In order of importance, these
and a one-hour walk from the Mugling–Narayangarh
were: disease, lack of knowledge about goat raising,
highway. The village is predominantly inhabited by
capital constraints and feed scarcity, and family labour
people of the Gurung community with a few households
constraints. Labour is a constraint in small families in
of other ethnic groups such as Magar, Bahun, Chettri
which there is a shortage of adults to take care of
and occupational caste (Damai). Cereal food crops
the animals.
(rice, maize, wheat), goats, off-farm activities and
vegetable production are the main sources of livelihood. Symptoms and seasonality of disease
After cereal food crops, goat raising is the next most Diarrhoea was the most important disease symptom
important component of the mixed farming system. reported by the goat farmers. Other important symptoms
Most farmers are smallholders (<1 ha) with small mentioned were: watering from the nose, occurrence
marginal (upland) and low producing, cultivated of fever and stomach swelling. The severity of disease
lands. Since the majority of the farm households (>60%) is greatest in young animals during the rainy season
have inadequate food production from their limited (May–September).
marginal farms, most of them suffer from food insecurity
during some parts of the year (mostly during the pre- Disease management
harvest period). Goat raising plays a critical role in Goatkeepers use both traditional and chemical methods
meeting the food security and livelihood needs of to control disease when animals develop diarrhoea.
these households. Some use cooked lemon extracts (chook), cannabis or
Goats are grazed close to the village, in communal garlic to control the initial stages of the disease symptoms.
grazing lands and forests, during the day and kept in Farmers resort to the use of chemicals/anthelmintics
sheds close to the house overnight. Little supplementary only when traditional methods do not work well. Drugs
feeding is provided to animals in the sheds. The number and associated information are normally obtained from
of animals kept by each household ranges from 1 to 18 agroveterinary suppliers at Bharatpur (Chitwan district).
with an average of 6–7 animals per household. Goats Technical information and chemicals are rarely obtained
are of the indigenous hill breed (Khari) and are small. from the local government livestock extension office.
Farmers rarely receive relevant information from radio
or other communication methods.

103
 Transhumance sheep and goat The most common ailments reported are ‘six-month
disease’ (a disease of unknown etiology), diarrhoea,
production in the mountain districts pneumonia, mange, contagious ecthyma and abortion.
Farming system In addition, land leeches and nasal leeches are also
reported as a serious nuisance to the animals. The main
Agro-pastoralism is the dominant form of farming in the season for six-month disease is spring (April–May) and
mountain districts. Transhumance livestock production autumn (September–October), while diarrhoea is most
is integrated with limited cropping of barley, buckwheat common during the monsoon, and pneumonia and
and potatoes. Livestock contribute significantly to farmers’
mange during winter. Most of the ailments are treated
livelihoods and provide the soil fertility necessary for
with available herbs and veterinary medicines are
continued cropping.
only used when the flocks are in accessible locations.
Livestock management The commonly used herbs are garlic, satuwa and kutki.
Most of the sheep and goats in mountain districts are Helminth problems
raised under the transhumance system of management.
Parasitic diseases (including gastrointestinal nematodes,
Animals are moved to different altitudes and climatic
Options to overcome worm infection for small ruminant producers in Nepal

liver fluke and external parasites) of small ruminants are

conditions throughout the year and are never penned
or fed cut forage. This migratory movement is determined regarded as an important cause of reduced productivity
by the availability of fodder, the farming system and of sheep and goats under transhumance management
the climatic conditions. In the migratory flocks sheep in Nepal. Parasitic diseases are ranked second in
and goats are raised together (sheep comprising the importance after six-month disease and this view is
higher proportion). Baruwal sheep and Sinhal goats, further supported by the superior response of animals
well known for their flocking tendency and hardiness, treated with anthelmintics in experimental studies (daily
are the principal breeds used in this system. weight gains of treated kids were about double those
of untreated kids) (Joshi and Joshi 1999, Joshi 1998).
During early summer (May to early July) flocks migrate up
to alpine pastures, grazing and browsing in the forests. The main nematode genera found are Haemonchus,
From late July to early September animals feed on the Ostertagia, Teladorsagia, and Trichostrongylus and
alpine meadows and gain sufficient body weight before to a lesser extent Oesophagostomum, Cooperia,
descending through the forests again in late September. Strongyloides and Bunostomum. Studies indicate that
From October through to April flocks graze in the fields Ostertagia and Teladorsagia are the main worm genera
and forests adjacent to the lower altitude villages. in the transhumance animals, although Haemonchus
Animal health issues in small ruminants burdens increase when sheep and goats are in the low
pastures in the winter (Joshi 1999).
Shepherds of the transhumance flocks report disease
and predation as important causes of animal loss.

104
Transhumance system case study — Ghandruk village
Ghandruk is a high mountain village (altitude 2000 m) Symptoms and seasonality of disease
located in the north-western part of Kaski district on
Chhamase (‘six-month’) disease was perceived to be
a trekking route to the Annapurna Himalayan range.
the most serious disease of sheep by the owners and
The village is predominantly inhabited by people of
shepherds. This disease kills young animals four to six
the Gurung community. Agriculture, tourism and off-
months old causing significant economic losses to their
farm activities are the main sources of livelihood for
owners. Fever and diarrhoea are the common symptoms
the local people.
of this disease, which occurs during migratory movement
Transhumance is the production system used for sheep of the flocks (April–May and October). The other
and goat flocks in this mountain village. Farmers normally important disease reported by shepherds, which
keep mixed flocks of sheep and goats (sheep comprising appears in some years, was blindness disease in sheep
the higher proportion). Indigenous sheep (Baruwal) (probably a tapeworm cyst). Goats were reported to
and goats (Sinhal) are raised in high mountain alpine be relatively free from disease compared with sheep.
pastures during the summer rainy season and grazed However, sometimes diarrhoea from worm infection
in the crop fields and forests/bush in the lower hills kills goats. Diarrhoea is severe in goats during the
during winter. The number of animals per flock ranges rainy season (June–September).
from 250 to 500. Flocks are either owned by an
Disease management
individual or two to four owners. There is a declining
trend in migratory sheep production in the village, Herders normally use herbal plants and also antibiotics
with only five flocks currently in the community where (if available) to control Chhamase in sheep. For goat
formerly there had been 10. diarrhoea they use cooked lemon extracts (chook),
garlic and other herbal remedies to control the initial
Constraints to sheep and goat production
stage of the disease. They obtain drugs and the
Semi-structured interviews and discussions with herders information from agroveterinary suppliers in Pokhara
and owners revealed that the important constraints to and from the Agricultural Research Station at Lumle.
migratory small ruminant production were: (i) diseases;
(ii) predation from leopards and bears; and (iii) land
leech nuisance to animals. An allergic reaction in sheep
feeding on pastures containing a hairy caterpillar (which
is a serious pest of Alnus nepalensis) was also reported
as serious by one of the sheep owners.

105
 in the mountain regions. The poverty focus of activities
would be enhanced by paying greatest attention to
the more remote areas in the west of the country.
The participatory exercises described here with farmers
in the hill region highlighted that farmers recognise
their lack of knowledge as a constraint to production.
If farmers’ demands for better knowledge were met
and they were trained in simple skills associated with
parasite control, there is a real chance that sustainable
control practices might be adopted.
Allied to the above, the establishment and use of
farmer research groups to undertake participatory
Discussion and observation with farmers in their testing of most-favoured options, chosen by farmers
own surroundings builds trust and yields better data. from the list of control options, might result in useful
practical adaptation of these strategies. Such an
Options to overcome worm infection for small ruminant producers in Nepal

(G.D. Gray)
exercise might provide valuable information on the
Options for helminth control process which could be extrapolated to the other
countries in the project.
Few options for improving helminth control can be
Further data are needed before valid control options
suggested for the transhumance system and none that
for the migratory system in the mountains can be
could be readily or immediately implemented. Gaps
implemented. The logistical problems in undertaking
in the understanding of the epidemiology of parasite
this work should not be underestimated. However, the
species in this management system require further study.
While such studies have the potential to contribute to the
productivity of the system and the livelihoods of the
Table 6.2 The significance and growth of
shepherds and owners, there are many logistical
livestock production per region
problems to undertaking such work.
Livestock Livestock Growth
Region GDP Proportion rate (91/92–94/95)
Conclusions
Terai 38% 2.8
Because poverty and small ruminant production are Hills 53% 2.9
clearly linked, the focus for any project activities should be Mountain 9% 3.0
the sedentary goat production system in the hill regions
Source: Agriculture Perspective Plan (1995)
and the migratory sheep and goat production system

106
 Table 6.3 The importance of ruminant livestock in different regions
Terai Hills Mountains

Livestock cash income (% of total cash income) 9.7% 19.7% 21.2%

Labour utilisation for livestock (man days) 64 73 51
Goat numbers (000s) 1,828 3,396 855
Sheep numbers (000s) 122 386 361
Percentage of households keeping goats 46.8 54.2 55.5
Percentage of households keeping sheep 1.8 4.2 6.5
Data from: Livestock Master Plan (1993), Statistical Information on Nepalese Agriculture 1997/98 and Agriculture Perspective Plan (1995)

benefits from a greater understanding of the diseases Central Bureau of Statistics, National Planning Commission
present in this vulnerable and marginalised system would Secretariat 1998. Statistical year book of Nepal.
help increase its potential to meet the livelihood Thapathali, Kathmandu, CBS.
requirements of the region. Federation of Nepal Chambers of Commerce and
Industry 1999. Nepal and the world: a statistical
profile. Kathmandu, Nepal, FNCCI.
References
Ghimire, S.C. 1992. The role of small ruminants.
Much of the relevant literature on livestock and small In: Abington JB. ed. Sustainable livestock production
ruminant production in Nepal is published informally in the mountain agro-ecosystems of Nepal. Animal
in reports and other grey literature. Those used in the Production and Health Paper 105, Rome, FAO.
preparation of this chapter are listed here.
Gauchan, D., Yokoyama, S. 1999. Farming systems
Agricultural Statistic Division, Ministry of Agriculture research in Nepal: current status and future agenda.
1997/98. Statistical information on Nepalese National Research Institute of Agricultural Economics,
agriculture. Singha Darbar, Kathmandu, ASD. Ministry of Agriculture, Forestry and Fisheries,
Agricultural Perspective Plan (APP) 1995. Prepared for Tokyo, Japan.
His Majesty's Government of Nepal by Agricultural International Center for Integrated Mountain Development
Project Service and John Mellor Associates, Inc. 1997. Districts of Nepal, indicators of development.
Carney, D. 1998. Sustainable rural livelihoods. Kathmandu, Nepal, ICIMOD.
What contribution can we make? London, DFID.

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 International Fund for Agricultural Development 1998a. Joshi, B.R. and Joshi, H.D. 1999. Responses of migratory
Managing poverty alleviation programmes in Nepal: sheep and goats to single anthelmintic treatment during
lessons learned by IFAD. Workshop Report, Rome, early winter month in Lamjung district of West Nepal.
Italy, IFAD. Proceedings of the 2nd National Workshop on
Livestock and Fisheries Research held at Lumle,
International Fund for Agricultural Development 1998b.
Pokhara, Nepal, June 1999. pp. 99–106.
Summary of country portfolio report (Annex III).
Managing poverty alleviation programs in Nepal: Livestock Master Plan (LMP) 1993.
lessons learned by IFAD. Workshop Report, Rome,
Ministry of Agriculture, His Majesty’s Government of
Italy, IFAD.
Nepal 1993. Livestock master plan. Kathmandu,
Jazairy, I., Alanir, M., Panuccio, T. 1992. Rural Nepal, MOA.
development through poverty alleviation. The state
Ministry of Finance, His Majesty's Government of Nepal
of world poverty: an inquiry into its causes and
1998. Economic survey. Kathmandu, Nepal, MOF.
consequences. Rome, Italy, IFAD.
Nepal Rastra Bank 1988. Multi-purpose household
Joshi, B.R. 1997. Gastrointestinal nematode fauna of sheep
budget survey: a study on income distribution,
and goats in the hills of Nepal. Veterinary Review,
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employment and consumption in Nepal. Kathmandu,

12, 30–32.
Nepal, NRB.
Joshi, B.R. 1998. Gastrointestinal nematode infection
Rasali, D.P., Joshi, B.R. and Paudel, K.C. 1997.
of small ruminants and possible control strategies in
Livestock systems analysis through a Samuhik
the hills and mountains of Nepal. Veterinary Review
Bhraman in the western hills of Nepal. LARC
13, 1–5.
Working Paper No. 97/34. Kaski, Nepal,
Joshi, B.R. 1999. Infection and effects of gastrointestinal Lumle Agricultural Research Center.
nematodes in Sinhal and Khari goats raised under the
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Veterinary Review, 14, 18–22.

108
Appendix efficiency of stomach and liver function. In addition,
Haemonchus is a blood feeder and leads to blood
Source material for an advisory note loss and anaemia.
for sedentary system goat-keepers Interaction with management
in Nepal Under current management, animals tend to revisit the
same grazing areas regularly during the wet season and
Internal parasites cause death and reduced production
it is presumed that high levels of infectivity build up on
of meat, milk, fibre and manure from sheep and goats
the pasture of these areas. In addition, since pasture is
throughout Nepal. In the hill regions, problems are
at its most abundant during this time, supplementation
caused by nematode worms in the stomach and
with cut fodder is reduced, encouraging animals to have
intestines and flukes in the liver. Options for better
higher intake of infected herbage and at the same time
control include grazing control and management,
reducing the total quality of feed intake.
stall-feeding and use of anthelmintics.

Grazing control and managment

The problem
Grazing control
When does the problem occur?
■ to avoid the most heavily contaminated areas
While animals may be continuously infected and
experience production losses all year round, clinically Grazing management
apparent signs are mainly found during the wet summer
■ to minimise build up of infection in grazing areas
months of the monsoon period (July to September).
Manure management
What are the causes?
■ to prevent spread of eggs and larvae from
Animals acquire burdens of Haemonchus, Trichostrongylus
housed animals
and Oesophagostomum causing a highly pathogenic
multi-species parasitic gastroenteritis syndrome.
In addition, animals are frequently infected with Stall feeding
Fasciola which increases the severity of the condition. Increased stall feeding
How the damage occurs ■ to reduce pasture intake during risk periods
Trichostrongylus and Oesophagostomum cause a profuse Zero grazing during wet months
diarrhoea, with a consequent failure to efficiently absorb
nutrients in the intestine. Haemonchus and Fasciola cause ■ to avoid grazing completely during risk periods
a protein loss in the stomach and liver and reduced

109
 Table 6.4 Use the right drug for the right worms
Anthelmintic Group Chemical Roundworms Flukes Tapeworms

Group 1 Albendazole YES YES YES

Oxfendazole YES YES
Fenbendazole YES YES
Group 2 Levamisole YES
Tetramisole YES
Group 3 Ivermectin YES
Others Rafoxanide Haemonchus only YES
Oxyclosanide YES
Closantel Haemonchus only YES
Triclabendazole YES
Options to overcome worm infection for small ruminant producers in Nepal

Cut and carry forage grasses and weeds Use of anthelmintics

■ to boost nutrition and enhance resilience Improved knowledge and use of anthelmintics
Anti-parasitic tree forages ■ to permit effective treatment and prevent the
■ use of forages such as mulberry to reduce establishment of anthelmintic resistance
parasite burden Strategic treatment of kids
Purchased by-products ■ preventative use of anthelmintics to suppress
■ nutritional supplementation with rice polish, build up of infection during risk periods
mustard cake, Supportive therapy for sick goats
Use of non-conventional feeds ■ symptomatic treatment to permit survival and
■ brewers grain, poultry manure etc. recovery e.g. protein and energy supplementation
and anti-scouring agents

110
Breeding management ■ Use drugs before expiry

Better breeding management ■ Most drugs work best if given when the animal
has an empty stomach
■ to reduce the number of susceptible animals
present during risk periods ■ If giving a drug by mouth, it should be given
as far back in the mouth as possible
Best practice for drug use ■ Drug bottle contents should be well mixed
■ Use the correct drug before use

■ Make sure you use the right dose of drug — ■ Store drugs away from direct sunlight and
don’t underestimate an animal’s weight children

■ Don’t use anthelmintics too frequently

or animals may develop resistance

111
7. The impact of parasitism on the development of small
ruminant populations in Southeast Asia
G.M. Hood

Introduction
For smallholders to benefit from rising demand for Parasitism as a constraint to the development by
livestock products, they need to increase herd and flock smallholders of a medium-sized enterprise based on
sizes so that livestock form a significant part of their meat goats, and demographic models will be used
farming income. With the notable exception of West in this chapter to assess the impact of mortality, reduced
Java — where sheep form a large component of the growth rates and delayed reproduction on both annual
farming mix — small ruminant populations in Southeast productivity and herd size. The set of models considered
Asia are small (FAO 2002). At the household level, this here includes a stochastic version that uses individual
is reflected as small herd sizes. Figure 7.1, for example, animals as the unit of study. It is therefore well suited
shows the distribution of goat holdings in the municipality to modelling smallholder systems in which the number
of Muñoz in the Central Luzon area of the Philippines. of animals is small and the fate of individuals important.
Most households have fewer than 10 goats, and the The observed mortality rate in tropical goats is one
average holding in 2001 was just over three per of the chief constraints to the growth of herd size, but
household. Throughout much of Southeast Asia, herd opportunistic harvesting also prevents smallholders
sizes are small despite a strong market, rising prices from developing medium-scale enterprises.
for goat meat and recent demonstrations that raising
goats for meat is profitable (e.g. Chapter 3).
Model details
Parasitism is one of many constraints that limits the
creation and development of small ruminant enterprises. We use the Leslie matrix (Leslie 1945) as the basis for
Parasitologists often report the effects of parasitism on model development because of its close links to life tables
physiological parameters, growth rates, reproduction and the availability of a large body of analytical theory
and mortality, but it is relatively rare to see these effects (Caswell 2001). The model we consider, however, is
translated to farming systems and the decisions made an extension of that formalism which includes a group
by smallholders. of classes to represent the stages of the breeding cycle,
as illustrated in Figure 7.2.
113
 Figure 7.1 Distribution of herd sizes among 1015 goat owners in Muñoz, Nueva Ecija, The Philippines
in 2001. Source: Census by city veterinarian, Dr Jerry Rigoz.

300

250 Mean = 3.35

Number of households

200

150
The impact of parasitism on the development of small ruminant populations in Southeast Asia

100

50

0
1 2 3 4 5 6 7-10 11–20 21–50 51–80

Number of goats

Figure 7.2 Lifecycle diagram showing stages of the goat’s breeding cycle

Juv 1 Dry Preg 1 Preg 5 Lact 1 Lact x

114
Full details of the model are included in the help file that Where A is a square population projection matrix, and
accompanies the GLORIA software package (available Nt is a column vector in which each element represents
at www.worminfo.org/goatflock). In brief, ‘Juv 1’ the number of animals in each class at time t. For this
represents female kids that have just attained the age class of model, an array of analytical tools (Caswell
of one month. Juveniles pass through several age classes 2001) can be employed to understand the relationship
(represented by the dotted arrow) until they are of of demographic rates to the productivity of the
reproductive age (Dry), whereupon they can fall population. In particular, the dominant eigenvalue, λ1,
pregnant (Preg 1), or stay dry. Newly conceived females of the projection matrix, A, gives the population growth
go through five months of pregnancy (dotted arrow) rate. We will use the annualised population growth
before kidding. They then spend one or more months rate as an index of the potential rate of harvest for
with kids at foot (Lact 1 to Lact x) before they can either each scenario.
conceive or return to the dry state after weaning of kids.
A more realistic version of the model treats the survival
Survival of male kids is modelled as a simple chain of
parameters in the model as probabilities and the
age classes; the survival of adult males is not considered
reproductive parameters as the means of specified
at all in the model. The availability of bucks for mating
distributions. Although this stochastic version of the
enters by proxy as a conception probability.
model has intractable mathematics, it can easily be
Each of the arrows in the life-cycle diagram represents simulated to estimate quantities like the population
a parameter, or set of related parameters, which must growth rate. The particular advantage of the stochastic
be estimated. Unfortunately, a complete set of survival model is that it allows us to consider the fate of a small
and reproduction parameters is rare in field studies or herd of one or more females and to understand the
surveys of smallholder populations. We therefore use risks that smallholders face due to parasitism-related
an amalgam of published estimates and best guesses mortality and other causes.
to parameterise the model. Specific suites of parameter
estimates are available as scenarios in the (‘GLORIA’)
software package. Analysis
The simplest version of the model treats the parameters We first consider model behaviour using a default set
as deterministic rates. Under these conditions, the of key parameters. (Many other parameters are used
life-cycle diagram can be mapped to a population in the model, but this is a key set likely to be affected
projection matrix, which allows the dynamics of the by parasitism.) These have been estimated from field
model to be written: surveys in the Philippines, where goats are principally
raised by tethering on crop residues and roadsides.
Nt +1 = ANt Under these conditions, mortality from parasitism and
other causes is high (Table 7.1).

115
 while in Figure 7.3b, the population has grown from
Table 7.1 Default parameter set
four to nine goats in the same period and four kids
Parameter Value Explanation have been produced for sale.
Pre-weaning 40% Total mortality up to A second set of parameters illustrates the population
mortality the age of weaning growth rates achievable when parasites are controlled
Post-weaning 20% Total mortality after and mortality is low (Table 7.2). These parameters have
mortality weaning but before been estimated using data collected in the Philippines
attaining breeding age (see Chapter 3) where, among other feeding and
Adult mortality 35% Annual mortality of management options, wet season housing has been
breeding females provided, and haemonchosis has been controlled by
The impact of parasitism on the development of small ruminant populations in Southeast Asia

Age at sale 9 Age at which surplus regular anthelmintic treatment. The principal change
stock is sold here is the reduction of mortality to rates similar to
Breeding age 10 Age at which female those found in temperate climates, together with a
kids are first mated slight increase in the conception rate to reflect higher
Conception rate 50% Monthly probability that body weight and better condition score.
eligible females conceive Analysis using the ‘Housed’ parameter set yields
Weaning age 3 Age in months at which a population growth rate of 79% per annum for
kids are weaned the deterministic model and 78% for the stochastic
Twinning rate 30% Percentage of litters version (mean of 1000 runs), with almost two surplus
that yield twins kids produced per breeding female. There is also a
profound decrease in the variability of the outcome.
The GLORIA software package provides tools for
Given these parameters, analysis of the deterministic investigating this variation in detail, but a simple
model yields a population growth rate of only 3% per indication of the magnitude of the change can be
annum, making it difficult to produce surplus stock for obtained by comparing the coefficient of variation
sale and increase herd sizes. An additional difficulty (CV = standard deviation divided by the mean) in the
is illustrated in Figure 7.3, which shows two runs size of various age classes at the end of a 36-month
of the stochastic version of the model. Here, even simulation. For the default parameter set, we obtain
though the stochastic growth rate (mean growth rate a CV in the final size of the breeding herd of 66%,
in 1000 simulations = 3%) is similar to the deterministic while for the ‘Housed’ scenario we obtain a CV of
version, individual runs of the model are quite different. 21% for the breeding herd. A similar decline in
In Figure 7.3a, for example, the population has barely variation is observed in all age classes.
survived, producing only one kid for sale in three years;

116
Figure 7.3 Two runs of the stochastic version of the model starting from a herd size of two adult and two
juvenile females and running for three years (36 months). Lines show size of the female part
of the herd and vertical bars show sales of surplus animals (usually kids).

(a) 10 10(b) 10

8 8 8
Number of females

Number of females

Number of females
6 6 6

4 4 4

2 2 2

0 0 0

0 12 24 36 36 0 0 12 12 24 24 36 36
Month Month Month

Table 7.2 ‘Housed’ parameter set

Parameter Value

Pre-weaning mortality 5%
Post-weaning mortality 5%
Adult mortality 5%
Age at sale 8
Breeding age 10
Conception rate 70%
Weaning age 3
Twinning rate 45%
Forage crops can provide a regular source of feed that
allows more intensive production and reduces the labour
required for feeding and herding. (G.M. Hood)

117
 The unpredictability of the farming system with the
default high mortality rates may help to explain the
lack of development of small ruminant enterprises
in Southeast Asia. Most goats in the region are kept
as an easily liquidated asset for the purchase of
medicines, payment of school fees and other needs.
The demand for cash must often arise at times when
surplus male kids are not available, so that owners
are forced to sell breeding females. The combination
of low inherent productivity and urgent cash requirements
The impact of parasitism on the development of small ruminant populations in Southeast Asia

could, therefore, enforce a low ceiling on herd size.

So, it is pertinent to consider the possible trajectories
that a smallholder might follow in attempting to build
a larger herd from a small initial holding.

Moving from a small to a

medium-scale enterprise Selling more young goats at better prices will allow
Consider the case in which parasitism and other major youngsters to spend more time at school. (G.M. Hood)
sources of mortality have been controlled, but in which
there is an urgent need for cash on an annual basis exceeded). Each of the panels of the figure shows
that must be satisfied by selling goats — to pay school the result of simulations under a different set of financial
fees, for example. Using the model, scenarios will be circumstances. Figure 7.4a assumes that no urgent cash
considered with and without this cash requirement, and requirement exists, so that surplus kids and adults are
the rates at which a goat enterprise can develop will simply sold as they become available. Under these
be contrasted. The endpoint will be a herd size of about conditions, mean herd size grows quite rapidly to reach
12 breeding females, starting from an initial herd of a steady state capacity at about four years. In each of
four animals two adult females (one of which is pregnant) the 100 trajectories, the herd never died out.
and a six-month and eight-month-old female kid. In Figure 7.4b a ‘cash requirement’ has been imposed,
Figure 7.4 shows the mean of 100 trajectories using forcing the owner to sell three goats in August every
the ‘Housed’ parameter set, but with the imposition year. The rule imposed here is that surplus stock are
of a ceiling of 12 adult breeders (that is, breeders sold first to meet the cash requirement, but breeders
are culled to reduce herd size when the ceiling is are also culled if necessary. Under these conditions,

118
 Figure 7.4 Mean of 100 trajectories using the ‘Housed’ parameter set but with a ceiling of 12 imposed
on the breeding population: (a) no cash requirement, (b) a requirement that three animals
must be sold every 12 months to meet urgent cash needs, and (c) the cash requirement is
spread over 3 months. Error bars show the standard deviation of herd size

(a) No cash requirement (b) With cash requirement (c) Deferred payment

30 30 30

25 25 25

20 20 20
Number of females

Number of females

Number of females
15 15 15

10 10 10

5 5 5

0 0 0

0 12 24 36 48 60 72 84 0 12 24 36 48 60 72 84 0 12 24 36 48 60 72 84
Month Month Month

mean herd size grows relatively slowly and the final Figure 7.4c shows the result of simulations in which the
herd size is lower than that attainable without the cash cash requirement is spread over three months, as would
requirement. The error bars of the figure show that the occur if an interest-free loan were obtained. In this case,
variation between trajectories when the cash requirement mean herd size grows somewhat faster than in Figure
is imposed is extreme compared to the relatively 7.4b to a slightly higher plateau. More importantly,
predictable dynamics of the first scenario. The variation herd size reached zero in only 8 of 100 simulations.
is partly driven by the extinction of some herds — in 18
of 100 simulations, the herd died out before six years
had elapsed.

119
 Conclusion References
The differences between the scenarios of Figure 7.4 Calara, A. and Lapar, L. 2001. Final report. Policy options
should not be surprising to development workers. The for market-oriented livestock production by smallholder
transition from bare subsistence to earning a modest producers in The Philippines, Los Baños, Philippines, IRRI.
income from any agricultural enterprise is difficult. Caswell, H. 2001. Matrix population models: construction,
Smallholders must cope with unpredictable changes analysis, and interpretation. 2nd edition, Sunderland,
in the weather and economic circumstances, which Massachusetts, Sinauer Associates.
will drive managerial decisions, so that an optimum
FAO 2002. FAOSTAT on-line statistical service, Rome, FAO.
path for development of the enterprise cannot be
followed. For small ruminants in the tropics, nutrition Leslie, P.H. 1945. On the use of matrices in certain
The impact of parasitism on the development of small ruminant populations in Southeast Asia

and the control of parasitism are key technological population mathematics. Biometrika, 33, 183–212.
innovations that sustain viability, but appropriate
markets and economic structures must be also in
place to help smallholders succeed. As Figure 4c
suggests, obtaining credit at a reasonable rate of
interest, rather than the punitive rates prevalent under
village conditions (e.g. Calara and Lapar 2001),
may allow farmers to make better decisions.

120
8. Worm control for small ruminants in the Philippines
G.D. Gray, C.A.T. Yee and E.C. Villar

Introduction
The consensus which emerges from the literature limit small ruminant production. Parawan concludes
published in the Philippines in the last 20 years is that his discussion on the integration of livestock with tree
there is a need to increase production of small ruminants crops with:
in the country and that helminth parasites are a ‘major
The most important aspect of health and diseases
constraint on production’. The greatest opportunity
on grazing livestock under tree crops is the
appeared to be the integration of sheep and possibly
problem of internal parasites. The problem is
goats in plantation crops, especially coconuts but, at
aggravated by the shading effect which favours
present, ‘backyard’ production is by far the dominant
parasite egg survival and persistency
production system. A comprehensive review (Dar and
Faylon 1996) identified the range of constraints on the Typical of published observations is that of Villanueva
substantial goat (2.63m head in 1996) and emerging and Soriano (1988) who concluded a report of a study
sheep (30,000 head in 1996) industries and do not of feeding water hyacinth meal to young sheep:
restrict these to animal health. That paper describes There was however an observed stunted growth
the medium term Philippine livestock R&D priorities in the experimental animals but this disturbance
1995–2000 which included the aim of controlling was due to external and internal parasites;
and eradicating economically important diseases of
swine, poultry and ruminants: The key phrase in this or Bautista and Vaughan (1983), in explaining the
objective is ‘economically important’ and Ducusin and lack of progress in their goat breeding program
Faylon (1996a) [later published in the Philippines in Bagalupa, Mindanao,
(Ducusin and Faylon, 1996b)] tackle the question of the high kid mortalities appear to have been due
importance of gastrointestinal helminths in Philippine to pneumonia caused by a combination of
sheep and goats and list the parasites present. Further, inadequate shelter, poor nutrition and helminth
they agree with Manuel (1983a) and Parawan (1988) parasitism,
and many anecdotal reports, that nematode parasites

121
 or Cruz et al. (1997) on the development of improved research efforts, of how to achieve these objectives
goats in Central Luzon, and to prevent parasitism from denying farmers their
economic returns.
“Parasitism is one of the causes of high
mortality not only at the university goat project
but especially under farm conditions. A broad Host-parasite relationships
spectrum dewormer is being used during [the]
rainy season and once every three months and worm control options
during [the] dry season”.
Descriptions of parasites of small ruminants
The two main strategies that emerge from the literature
for increasing small ruminant production are: in the Philippines
■ The development of new industries integrated A slaughter study of 40 goats from sale stands in
with tree crops including coconut, mango, oil palm, Manila and Quezon City (Manuel and Madriaga,
pepper, calamansi, coffee and rubber (Villar 1984, 1966) found four nematode species: Trichostrongylus
1995; Tacio 1998; Alvarez et al. 1985; Subsuban sp., Haemonchus contortus, Oesophagostomum
et al. 1995; Faylon et al. 1989; Castillo 1994). columbianum and Trichuris ovis. This was also the
first Philippine description of Eurytrema pancreaticum,
■ Increased efficiency of existing extensive and the pancreatic fluke.
intensive production systems (Villar 1984;
The parasites (helminths and protozoa) of goats from
The control of helminths in small ruminants in the Philippines

Faylon and Villar 1988).

a large number of provinces in the Philippines have
A national survey documented by Faylon and Villar been subjected to an extensive study (Tongson et al.,
(1988) characterised the current stock of sheep in the 1981). 1230 faecal samples were examined and
Philippines and determined the existing components of 39 goats necropsied. From the faecal examinations
sheep production systems. Management, husbandry and the four outstanding genera were Trichostrongylus,
herd health practices were identified with the aim of Haemonchus, Oesophagostomum and Strongyloides
formulating a national framework for sheep research and found in 1117, 1073, 1047 and 524 of the samples
development. Among their many findings, deworming respectively. The actual counts are not presented.
and vaccination were the most commonly employed herd This was the first report of Strongyloides papillosus
health practices. A very general account of ruminant in the Philippines.
development in developing countries was written from
an international perspective by Madamba (1989). In a comprehensive account of the worldwide distribution
of paramphistomes Eduardo (1988) lists Cotylophoron
No matter what national or international objectives are cotylophorum as a rumen fluke of sheep and goats in
identified, the challenge remains, despite substantial the Philippines, Carmyerius synethes and Fischoederius

122
cobboldi as rumen flukes of goats and the pancreatic
fluke Eurytrema pancreaticum in goats. Tongson and Trovela
(1980) found no correlation between faecal egg counts
and worm burdens in ‘grade Spanish Merino’ sheep of
various ages infected with Haemonchus contortus,
Oesophagostomum, Trichostrongylus and Cooperia.
Likewise there was no correlation between worm size
and worm burden but there was a significant correlation
between adult female numbers and faecal egg count.
The ages of the sheep at slaughter were 3, 6, 12, 18
and 24 months with four animals killed at each age.
In assessing the value of the lack of correlation the small
number of animals in each class needs to be noted.
Although not conclusive, this paper reinforces the warning
Tethering exposes animals to extremes of weather.
that egg counts alone are not necessarily an indication
(G.D. Gray)
of worm burden, although they are a direct measurement
of pasture contamination.
Faeces from 60 sheep of varying ages were examined Worm control programs
and larvae cultured (Matibag et al., 1991). Trichostrongylus One study strongly supports the concept of rapid
and Haemonchus dominated the cultures, ‘strongyles’ rotational grazing systems in the Philippines (Barger
dominated the egg counts with Strongyloides and 1996). [An interesting early reference to rapid rotational
five other nematode genera present. grazing systems in tropical conditions may be found in
Pajares (1986) described and elegantly photographed Spindler (1936) and Thomson and Carr (1957) who
Haemonchus eggs and larvae as they develop from said that, in the tropics, small ruminants should be kept
laying to hatching and moulting to infective larvae. off pasture for 21–28 days.] Worm eggs from a native
goat infected with several nematode species were
From the studies it can be summarised that using faecal
maintained either under direct sunlight or in shade for
samples alone for parasite identification is imprecise
several weeks, and at weekly intervals the viability of the
especially if only eggs are used for identification and
eggs and larvae developing from them were estimated.
are not allowed to develop to later free-living larval
Although the study was undertaken in Petri dishes and a
stages which can be more readily identified. Slaughter
direct comparison with pasture conditions cannot be
studies which permit identification of adult worms and
made, the viability of deposited eggs to be recovered
parasitic larval forms are always preferable but not
always practical. as larvae after 4 weeks was nil in the sunlight exposed

123
 samples and very low in the shaded samples
(Tongson and Dimaculangan, 1983). The humidity
of the samples was maintained at >85% throughout.
The recommendation from this study was that pastures
should be rested for at least 4 weeks after grazing
by infected goats and that this should be tested under
field conditions.
Alvarez et al. (1991) showed that goats supplemented
with ipil-ipil, but grazing in a rotational system rather
than continuously, have a ‘slight advantage’ in terms of
liveweight gain. This could be the result of diet quality,
parasites or a combination of these.
Feed supplementation (eg with urea molasses blocks)
A worm control program (Anon, 1981) for cattle increases growth and reduces the impact of parasites.
describes the principles of strategic, tactical and (G.D. Gray)
offensive drenching for Philippine conditions. Drenching
2–3 weeks after the first heavy rains is suggested as
a good strategy along with a mid-summer drench 6. Keep animals well nourished, supply vitamin
and one after soaking regular rains. It is not said if and mineral supplements.
The control of helminths in small ruminants in the Philippines

these strategies should also apply to small ruminants. There is no evidence in this paper or later of these
Manuel (1983b) provided the following worm control programs being tested experimentally against any other.
program for ruminants: In an overview of livestock parasites in the Philippines,
1. Calves should be treated against large ascarid Manuel (1980) stated that “sheep and goats in this
and threadworms at the age of 1 month country are equally affected [by liver fluke, as buffaloes]
but the condition is not considered a serious problem”:
2. Lambs and kids should be treated against
the prevalence is the same but level of morbidity and
Strongyloides at the age of 1 month.
mortality is less.
3. Calves, kids and lambs should be treated against
Several recent studies may reflect a change in approach
other gastrointestinal helminths at the age of 3 months.
to worm control as they describe seasonal variation on
4. Drench all animals (young and old) at least once a nematode infections in sheep and goats. Rosillo (1995)
year preferably 1 month after the onset of heavy rain. found that H. contortus and S. papillosus were present
in ewes all year round when ewes were sampled
5. Pasture rotation should be practised.
regularly. Gemino (undated), Pangilinan (1998) Arrieta

124
(1998), Dilla (1998) and Gorospe (undated) examined basis of egg morphology. Overall, there were no major
faeces of goats of different age classes on a research differences between wet and dry seasons, between
farm in Neuva Ecija for a six month period from the climate type and between worm genera in the two
dry to the rainy season. The dominant parasites were samples collected — one in the wet and one in the dry.
Haemonchus and Trichostrongylus with a distinct seasonal
The experiments which led to the herd health program
increase. Although limited in nature this trend towards
involved sampling of does 1–2 weeks, 1 month, 3 months
longer term studies is encouraging. As part of these
and 6 months after treatment with a dewormer which
studies counts of parasitic and non-parasitic larva
was given to three different groups of does at monthly,
on pasture were also undertaken (Anon, 1998).
3-monthly or 6-monthly intervals in each of the
A more detailed study of the seasonal pattern of helminth three regions.
infection of goats in La Union was reported by Barcelo
The results show albendazole used in Masbate
and Camalig (1997). Although not a full report, the
was very poorly effective (measured by change in
study extended over two complete years and, with the
prevalence). Tetramisole in all regions was poorly
exception of April in the first year when Trichostrongylus
effective. Confirmation of our interpretation of the
made up more than 50% of the larvae which emerged
experimental protocol with the study author is required.
from culture, the dominant species was Haemonchus
Goats drenched monthly gained most weight over a
which for all other months comprised more than 90% of
6-month period. This is possibly the first circumstantial
the cultured larvae. This was reflected in the numbers
evidence of anthelmintic resistance in the Philippines and
of infective larvae in soil and herbage although only
could become a focus for a future survey of resistance.
Haemonchus and Trichuris larvae were recovered
(time of sampling not given).
Marbella (1991) undertook some epidemiological Impact of helminths on production
studies which led to the establishment of a goat herd Kingscote (1968) estimated the impact of parasites in
health program in the Bicol region of southern Luzon. general on Philippine sheep and goats as 10% of the
The unit of measurement of a range of gastrointestinal value of production and included ‘unthriftiness, death
parasites and Dictyocaulus was ‘prevalent’; simple and predisposition to other diseases’ as the sources
flotation and sedimentation techniques being used to of that loss. Justification for this figure is not provided
detect the presence and absence of nematode eggs and because none was available: economic estimates of the
larvae, and trematode eggs. Twelve farms with at least wide and long-term effects of helminth infections are
10 does were used across the region, representing difficult to obtain experimentally, especially under field
three major climatic types. Four commercial dewormers conditions. However, comparison between parasitised
(three BZs and tetramisole) were also tested for efficacy. and non-parasitised goats in two barangays in southern
Identification of nematode genera was made on the Luzon (Que et al., 1995) showed that they differed

125
 in growth by several kilos over a period of 8 months Anthelmintic plants and
representing a good return on investment from a single
dose of anthelmintic. Such studies are often difficult to biological control
interpret (see Chapter 1) when the experimental and
control (treated) animals are, as in this case, grazed Medicinal plants as anthelmintics
separately on different farms. Nevertheless the result
Medicinal plants have attracted attention from various
does point to a substantial impact of helminths on
groups in the Philippines whose interests have been on,
growing goats. A series of papers by Howlader et al.
but not restricted to, their anthelmintic effects. Loculan
(1997a, 1997b, 1997c) describes the pathological,
and Mateo (1986) surveyed 22 barangays in Lipa
parasitological and production changes in young
City and identified the plants being used as medicines
goats of different ages infected artificially with varying
and their intended effect. The plants with purported
doses of H. contortus. Kids born of infected mothers
anthelmintic effect for ruminants are shown in Table
had their growth affected by infection (about 70g/day
over 5 weeks after birth compared with around 20g/day 8.1. Other publications by Mateo (1986 and 1996)
for the kids of uninfected dams) but this impact was not contain similar information.
dependent on infective dose. Growing goats gained less A more comprehensive list of anthelmintics for large
weight than uninfected counterparts: about 4g/day animals (it is not stated which are for ruminants) was
in infected kids compared with about 19g/day in published by Mateo (1987) and is summarised in
uninfected kids. Once again, the effect was not Table 8.2.
The control of helminths in small ruminants in the Philippines

dependent of the level of infection given to the

Claud and Mateo (1988) conducted interviews in
experimentally infected animals. In the same growing
Batangas province and found that in 100 responses
goats there was no effect of infection on circulating
leukocyte numbers and a moderate effect on erythrocyte from 18 barangays, 89% of respondents were using
numbers. Related studies (Howlader et al., 1996a, herbal medicine and ‘obtained satisfactory results’.
1996b) showed similar effects on growth and blood Nineteen medicinal plants were identified. These were
parameters as the result of Haemonchus infection. prepared in a variety of ways and some were used to
It is difficult to relate these results to field conditions treat parasitism. Fernandez (1991) screened some local
but once again they point to a significant impact plants for their efficacy against Haemonchus contortus
on the performance of young and old goats. and found that eight were effective. Further studies on
two of these have been published in abstract form: a
‘crude extract’ of Mimosa pudica was 93.6% effective
against Haemonchus larvae in vitro and was ‘as good
as a commercial dewormer’ in vivo in a dose response
trial in terms of worm egg count reduction and reduction

126
Table 8.1 Plants with anthelmintic effect for ruminants
Method of
Common Scientific Parts Preparation and Approximate Specific Animals
Name Name Used Administration Dosage Ailments Treated

Niyog Cocos nucifera Oil/milk Mixed with feeds 350ml, Dewormer Cattle
2 x day for 2 days
Makabuhay Tinosphora Vines and Fresh plant, 1–2 ft of vine, Dewormer Cattle,
rumphii body of plants force fed 2x day for 4 days carabao
Source: Loculan and Mateo, 1986

Table 8.2 Medicinal plants with anthelmintic effect

Common Ailment Medicinal Plants Direction for Use

Specific for tapeworms Pakwan (Citrullus vulgaris) Seeds fed ad lib

Common intestinal Atis (Anona squamosa) Raw leaves fed ad lib
worms for large animals Makabuhay (Tinosphora rumphii) One basket of fresh leaves orally
Kamonsil or Kamanchili (Pithecocobium duice) (sic) Raw leaves fed ad lib
Kakawate (Gliricidia sepium) Raw seeds fed ad lib
Aludig (Streblus asper) Boiled stem juice given as drench
once a day
Langka (Artocarpus heterophilus) (sic) Decoction of leaves given orally
Repeated after 1 week
Specific for liver fluke Bunga (Areca catechu) One whole nut in seven parts water
per 50 kg body weight
Source: (Mateo, 1987)

127
 in worm number post mortem (Faelnar, 1997). Nutritional supplementation
Tinosphora rumphii ‘stem crude extract’ was 85.6%
effective in vitro and at a non-toxic dose level in vivo There have been few published studies which either
half of the experimental animals had their ‘worm burdens directly or indirectly implicate nutritional status as having
significantly reduced’ (Fernandez, 1995). an impact on parasite levels in either sheep or goats
under grazing conditions. Supplementation with
Salazar et al. (1986) report (in abstract form) 72 plant concentrates fed as a replacement for ‘grasses’ in
species used for livestock and poultry health but give no confined goats resulted in decreased FEC in 1-year-
details of which plants were used for internal parasites. old native and Anglo-Nubian goats over a 6-month
Jovellanos (1997) dramatically demonstrated the efficacy period while harbouring a nematode infection dominated
of two out of three plant extracts in the treatment of by Haemonchus and Trichostrongylus (Barcelo and
Camalig 1998).
gastrointestinal nematodes in cattle. The plant products
were atis (custard apple: Anona squamosa), papaya Sevilla (1990a) reviewed approaches to feeding small
(Carica papaya) and pineapple (Ananas comosus). The ruminants and mentioned a range of supplementation
studies were conducted at Santa Barbara, Pangasinan. strategies appropriate for high-fibre diets in the tropics.
Forty cattle were selected with FECs over 400 epg. Sevilla rejects what he describes as ‘traditional feeding
Albendazole was used as a control in one group of standards’ as a suitable approach to feeding small
10 cattle and the remainder were divided into three ruminants in the tropics where there are limited options
groups of 10 given a single treatment with dried for feed resources which can be highly variable. Studies
The control of helminths in small ruminants in the Philippines

powdered leaves of the three plants with molasses as such as that of Magay and Perez (1984) may fall into
a ‘lick’. Cooperia and Haemonchus were the dominant the ‘traditional’ category as they fed young native goats
species. The efficacies of the treatments were: albendazole highly prepared diets, based on leguminous leaves and
starch grains. Such feeds are not always available
100%, Ananas 98.46%, Anona 95.53% and Carica
and the prescriptive recommendations from that study
‘no effect’. Efficacy was based on FEC. The cost of
may apply only in certain circumstances and, we would
treatment with the plant extract was estimated to be the
argue, circumstances that are rarely found in real
cost of molasses alone at P 9.5 per animal compared
farming situations.
with P 37.33 per animal for albendazole treatment.
Cost of collection and preparation of the extracts were Boloron and Magadan (1982) made detailed
not reported. recommendations for the improved nutrition of cattle
and dairy goats using pasture and concentrates under
backyard conditions. Castillo (1982) discussed fibrous
agricultural residues and noted that winged bean residues
had lower digestibility in goats (49%) than in cattle and
carabao (63%).

128
High protein supplements such as Azolla (Sevilla et
al., 1987) have been investigated and have been
extensively reviewed (Sevilla, 1990b). In the case of
Azolla the growth of animals with its leaf as a dietary
component grew less well than those with comparable
amounts of ipil-ipil (Leucaena) leaf.
A large number of supplementation trials have been
undertaken using cassava leaves (Manihot esculenta)
(Baquirquir and Coruña, 1989), ipil ipil (Leucaena
leucocephala) (Faylon and Momongan, 1985; Aliling,
1980; Abilay et al., 1981; Patricio et al., 1990;
Rasjid and Perez, 1982) and kakawate (Gliricidia
sepium) (Siasico et al., 1990; Siasico and Coruña, Goat kids in the feed trough can defecate on feed,
1990). If stated, all these trials cited were conducted increasing chances of parasitism. Goats from Balungao,
in pens. In some cases the animals were dewormed Philippines. (G.M. Hood)
before the start of the trial but in most cases no mention
is made of parasites or treatment for parasite control.
castrated goats grazing at 20 head/ha. The supplement
It is possible therefore that the effect of parasites may
was molasses/urea at two ratios, 20:1 and 10:1.
have influenced the outcome of these studies. Both supplemented groups gained more weight than
Other supplements that have been tried include biogas the control group but the conclusion, similar to studies
sludge (Cruz, 1981), urea-molasses (Gerona et al., with sheep under coconuts (Faylon et al., 1991), was
1984), urea-supplemented wheat straw (Ordoveza and that goats need additional supplementation if pastures
Johnson, 1983), rice straw with urea-molasses (Lapuz, are not to be degraded at these stocking rates.
1982; Trung et al., 1990), dried poultry manure (Bazar Alvarez et al. (1991) showed that goats which were
and Intong, 1991), water hyacinth meal (Villanueva and supplemented with ipil-ipil but grazing in a rotational
Soriano, 1988) and vegetable waste (Anon, 1982). system in Pampanga, Luzon, have a ‘slight advantage’
Lanting and Sevilla (1998) found that inclusion of the over goats given the same level of supplement but
tanniniferous legume Flemingia improved growth and grazed continuously. Pastures were also in better
intake of sheep fed a Stylosanthes based diet. They condition under the rotational system.
did not investigate the impact on parasites. A general pattern that may be emerging is that for
There have been some grazing trials using agronomic reasons it is essential to supplement sheep
supplementation. Gerona et al. (1984) compared and goats if they are to graze continuously in coconut
the production of supplemented and non-supplemented plantations at the stocking levels used in these studies.

129
 One future research application may be to investigate Production differences between
the timing and nature of nutrient supplementation to
optimise animal production, pasture conservation and and within breeds
parasite control.
Matias et al. (1997) list seven exotic and three local
breeds of goats and 10 exotic and three local breeds
Genetic variation in production of sheep (Table 8.3). The numbers of each breed have
not been accurately estimated.
and resistance to disease
A number of studies have sought to compare native
There are no published studies on genetic differences goats with varying levels of cross with Anglo-Nubians.
in resistance to helminths between sheep and goats, These are summarised in Table 8.4.
within breeds of sheep and goats and only one account
There are several notable features. In none of the studies
of breed differences among goats but none for sheep.
are sires identified or accounted for in the analysis of
However it is likely that parasites have been present in
differences between ‘breeds’ and no attempt is made
all the studies described in this section and that they have
to account for heterosis in evaluation of the crosses.
contributed to some extent to the observed difference
One intensively analysed study was by Karnuah et al.
sin production. The extent of their effect is not known.
(1992) on 76 does of five genotypes which varied
in their proportions of the two breeds, from 100%
Genetic differences between Anglo-Nubian to 50% Anglo Nubian and 50% Native.
sheep and goats
The control of helminths in small ruminants in the Philippines

They concluded that crossbred animals were more

productive across a range of parameters.
Interpretations of comparisons of any trait: disease,
production and anatomical, between sheep and goat Aurelio et al. (1987) and Bautista and Vaughan (1983)
are notoriously difficult unless they are constrained to studied crosses of Anglo-Nubian and Native (473 does)
known diets and behaviours. Palo et al. (1995) elegantly and Anglo-Nubian and Saanen crosses with Natives
demonstrated the comparative feed selectivity of sheep (number unknown) with mixed results which were heavily
and goats using oesophageal fistulae. Goats were influenced by weather.
shown to be more selective and eat the forages of A substantial comparative study of milk production
higher nutritive value. This may be important for intake and kidding performance at two farms in Mindanao
of parasitic larvae that tend to be consumed from the could not distinguish breed effects from management
low parts of more erect species rather than on the leaves effects (Amonruji and Rigor, 1988) although on reading
of trailing or erect broadleaf plants. the methodology a comparison between Anglo-Nubian
Bato and Sevilla (1988) used oesophageal fistulae and Anglo-Nubian crosses should have been possible
to investigate diet selection of goats on improved and in at least one location. The data to support their
unimproved pastures. conclusion that ‘there were no differences in milk
production on the basis of ... breed’ are not presented.
130
 Table 8.3 Exotic and local breeds of goats and sheep in the Philippines
Goats Sheep

Exotic Local Exotic Local

1. Anglo-Nubian 1. Cebu 1. Barbados Black Belly 1. Bukidnon

2. French Alpine 2. Dadiangas 2. Polled Dorset 2. Leyte
3. Toggenburg 3. Muñoz 3. Border Leicester 3. Bicol
4. Jumna Pari 4. Katahdin
5. Boer 5. Rambouillet
6. La Mancha 6. Merino
7. Saanen 7. St. Croix
8. Suffolk
9. Wiltshire Horn
10. Southdown
Source: Matias et al., 1997

Castillo (1983) and Villar et al. (1984) were able to that Native goats raised in villages are a different
analyse data from the Philippine Rural Life Centre from size and shape to Anglo-Nubian goats raised on
1979 to 1981 and 1980 to 1982 respectively in which research stations.
four breeds were represented. No breed or cross
The Dadiangas goat breed (a hybrid of Native and
emerged with a clear productive advantage. Parawan
several introduced breeds) found mostly in Mindanao
et al. (1987) was able to study under village conditions
has been advocated as a good ‘prospect’ (Anon, 1990,
the performance of Native and Anglo-Nubian crosses in
1992; Villar, 1995). No comparative trials of their
a rainfed coconut system in Mindanao. The conclusion
productivity have been published.
was that Native goats performed better when 3–5 were
present in the production ‘module’ but not as well at Future use of blood packed cell volume as a measure
lower numbers. It would be interesting to re-analyse that of anaemia resulting from Haemonchus infection, the
data on a ‘weight of kid weaned per doe joined’ basis. baseline haematological study by Ducusin et al. (1995)
in sheep grazing in coconut plantations may be useful.
Kharel and Lambio (1990) published an exhaustive
study on morphological differences which showed

131
 Table 8.4 Studies which draw conclusions on production differences among ‘Native’,‘Anglo-Nubian’
and ‘Grades’ Native and Anglo-Nubian
No. of No.
Animals Sires Type of
Author per per Traits Statistical
(Date) Genotypes Compareda Breed Breed Measured Analysis Notes

Amonruji 100% Anglo-Nubian Varied No Mean age at first Descriptive analysis,

and Rigor 87.5% Anglo-Nubian with infor- breeding and first simple correlation
(1988) 50% Anglo-Nubian nature mation kidding, milk production coefficients, pooled
of obser- given per day, lactation correlations,
vation length and kidding ANOVA-CRD,
interval and service pd. split-plot analysis,
t-test, multiple
regression analysis
Aurelio and 100 % Anglo-Nubian 282 No Birthweights, weaning T-test, ANOVA-CRD,
Natural 75% Anglo-Nubian 127 infor- weights, litter size, multiple linear
(1988) 50% Anglo-Nubian 64 mation kidding intervals, correlation analysis,
given occurrence of multiple linear
simple births regression analysis
The control of helminths in small ruminants in the Philippines

Maglunsod 100% Anglo-Nubian 230 kids 5 AN Birthweight, subsequent General linear Kids were
and Natural 75% Anglo-Nubian (total) (for all body weights, heritability model – CRD, produced
(1988) 50% Anglo-Nubian kids) of birthweights, correlation paternal half-sib from mating
coefficient b/w correlation, of pure Anglo-
birthweight and product moment Nubian buck x
subsequent 6-, 8- and correlation Native and 50%
12-month body weights Anglo-Nubian
does.
Bautista and 100% Anglo-Nubian Kids No No Growth rates, No information The proportion of
Vaughan Anglo-Nubian x Native Kids infor- infor- inter-kidding intervals given each breed is not
(1983) Anglo-Nubian Native mation mation indicated in the
Goatlings given given publication
Anglo-Nubian x Native Does
Anglo-Nubian x Saanen x
Native Goatlings
continued over

132
Table 8.4 continued
No. of No.
Animals Sires Type of
Author per per Traits Statistical
(Date) Genotypes Compareda Breed Breed Measured Analysis Notes

Parawan 50% Anglo-Nubian No No Kidding interval, No information

et al. 25% Anglo-Nubian infor- infor- occurrence of multiple given
(1987) 100% Native mation mation births, age at first
given given breeding, weight of
females at 6 months, ADG
values, kidding per year,
number of kids per year
Villar et al. 100% Anglo-Nubian 4 No Age at first breeding, ANOVA-CRD,
(1984) 50% Anglo-Nubian 4 infor- kidding interval, number Duncan’s Multiple
100% Native 4 mation of days open, kidding Range Test,
(4 repl- given rate, kidding percent, descriptive analysis
icates per post-partum oestrus,
treatment birthweight, incidence
group) of twinning, litter size
Karnuah 100% Anglo-Nubian 31–76 No Oestrus manifestation, General Linear
et al. 93.75% Anglo-Nubian (varied infor- age and weight at first Model (GLM) of the
(1992) 87.5% Anglo-Nubian w/ the mation oestrus, age and weight canned package
75% Anglo-Nubian nature given at first breeding, Statistical
50% Anglo-Nubian of obser-- conception rate, gestation Analysis System
vation period, kidding interval, (SAS), Least
incidence of multiple birth Squares Analysis
and post-partum oestrus
Reyes and 100% Anglo-Nubian 10 No Oestrus cycle length, No information
Abilay 100% Native 6 infor- oestrus duration, services given
(1981) mation per conception, gestation
given period, kidding rate, birth
and weaning weight,
growth rates, daily milk
yield, mortality rate at birth
Yokota 100% Anglo-Nubian 66 8* Birthweight, growth rates No information *8 bucks were
et al. 75% Anglo-Nubian (total) given kept on the farm
(1991) but their use to
generate the
experimental
animals is not
stated
a The proportion of ‘exotic’ breed is indicated. Unless another breed is given then remaining proportion is ‘native’.

133
 Arboleda (1986, 1987) discusses the animal genetic alkaline phosphatase in a population of 288 adult
resources available for livestock production in the female indigenous goats from eight provinces (they
Philippines. Although not entirely complimentary about were monomorphic for albumin, esterase and L2
the livestock of smallholders, describing them as macroglubulin) to construct a dendrogram based on
‘nondescript mongrels with low performance potential’, genetic distance among the samples. Only the sample
Arboleda makes some telling points about the priorities from Ilocos Norte differed genetically from the others
of smallholders. He argues that smallholders have been which could not be distinguished from each other.
using smaller carabao for breeding while using their Up to 20 polymorphic enzymes have been required
larger animals for draught power, leading to a continual to produce accurate dendrograms in other published
decrease in the size of the local animals. This raises the studies. No studies of genetic distance have been
possibility that some similar effects may exist for sheep conducted in sheep and no studies on sheep or goats
and goat populations with larger males and females have been reported using DNA polymorphisms. [Genetic
being sold off for slaughter. Although enthusiastic about polymorphism among goat and buffalo population in
the upgrading of local stocks he has a cautionary South and Southeast Asia has been the subject of two
message for poultry, ACIAR projects. A sample of goats from Mindanao was
included in one of these projects.]
‘Today, many small farmers still prefer to raise
chickens based on their ability to survive and Bondoc (1993) stated that it is important to conserve
reproduce under minimal care and management’. native breeds of livestock rather than to continue importing
breeds, while ignoring improvement of native breeds
The control of helminths in small ruminants in the Philippines

Again, this may also be true for sheep and goat that have special attributes such as greater resistance
populations. In the 1986 paper Arboleda tabulated the to disease. He stated that native breeds are:
comparative performance of four exotic goat breeds
and the Philippine Native from several studies. ■ more adapted to the local environment

Like many authors, Arboleda uses the term ‘Native’ for ■ more tolerant of poor nutrition and harsh
sheep and goat populations which have been present environments
in the Philippines for many years and which cannot ■ a vital resource for scientific research and
be assigned to any distinct or recently imported breed. a cultural resource
Because of the island nature of the Philippines, lack
of a sophisticated breeding and marketing system for ■ reservoirs for traits which, if lost, may never
small ruminants and the occasional infusion of exotic be recovered
genes, it is likely that populations of ‘native’ goat will Among the traits that could be used to identify the
be genetically heterogeneous. Lambio et al. (1992) important genetic resources are ‘alternate traits such
used polymorphism of the enzymes transferrin and as disease and parasite resistance’.

134
The technology to make sophisticated estimations of
breeding values (EBVs) for livestock is available in the
Philippines and has been applied to some sets of data
from local livestock populations (Bondoc, 1995).
The application of this ‘Best Linear Unbiased Prediction’
(BLUP) technology can only be made where accurate
and, if possible, extensive pedigrees crossing several
generations of large populations of animals are
available. Equally critical is the need for performance
data which can be manipulated in such a way that
it can all be assessed as if it had been generated at
a single time. This ‘contemporary comparison’ and use
of complex pedigrees can be made possible using
computers which today are commonplace. At the
heart of the use of BLUP (or any breeding program)
Many tools such as this cartoon warning against
is the accuracy of the pedigrees, the quality of the
grazing infected pastures can be used to make farmers
performance data and the ability of livestock breeders
and extension workers aware of technical innovations.
to make decisions based on the numbers produced.
(K.C. Patawaran)
In the study by Bondoc (1995) 324 weaning weights
from the goat farm of UPLB covering 9 years, four sire
breeds (10 sires), four dam breeds, two sexes, three A tantalising abstract from Maglunsod and Natural
types of birth and 87 dams were analysed. This analysis (1988) addressed this question of correlations among
led to the conclusion that weaning weights were bodyweights of Anglo-Nubian and ‘grade’ kids at
decreasing with time but not due to genetic effects. birth and 6, 8 and 12 months of age. The abstract
The study would also have produced estimated refers to some ‘breed’ differences but the correlations
breeding values for weaning weight. If ‘increased are not given. In a related study, Aurelio and Natural
weaning weight’, ‘decreased weaning weight’ or (1988) report that purebred Anglo-Nubian does had
‘no change in weaning weight’ was part of a breeding shorter kidding intervals but 50% Anglo-Nubian 50%
objective for this flock then these EBVs would be Native does had larger litter sizes.
valuable in making the correct selection decisions. Maglunsod (1987) estimated heritabilities of birth
The effect of this on liveweights at later ages could weight of 230 kids from 100%, 75% and 50% Anglo-
not be predicted. Nubian:Native cross does which had been joined to
five Anglo-Nubian bucks. The standard errors of the

135
 heritabilities ranged from 0.66 to 2.04. On this basis
Table 8.5 No. of does of Anglo-Nubian/
it was stated “birth weight is heritable, hence selection
Native crosses at four experimental
for the trait can help bring about improvement of
locations (Aurelio, 1987)
productivity of goats”. This bold statement contrasts with
the more perceptive conclusion made that “overall [despite Location AN 75% 50%
increased birth weight of kids from Anglo-Nubian does] Pampanga 327 102 31
improvement in meat productivity using 50% Anglo-
Bukidnon 36 36
Nubian grades is the most promising compared to the
South Leyte 23 29
75% and purebreeds in terms of overall performance”.
This conclusion is made in part because of the increased Zamboanga del Sur 42 50
litter size of 2.09 seen in 50% crosses compared with
1.64 and 1.58 in 75% and purebreds respectively and
equivalent kidding intervals of 326, 293 and 240 days. Table 8.6 Litter sizes of does of Anglo-Nubian/
Native crosses at four experimental
A smaller study on 20 does joined to either a Saanen
locations (Aurelio, 1987)
or Anglo-Nubian buck sought to measure breed effects
but in fact was measuring sire differences (Udin, 1985). Location AN 75% 50%
In that study all kids were wormed at 1 month of age. Pampanga 1.41 ± 0.53 1.40 ± 0.54 1.59 ± 0.73

A study of goats which were mostly imported (i.e. Bukidnon 1.70 ± 0.65 1.90 ± 0.55
The control of helminths in small ruminants in the Philippines

not born in the Philippines) was conducted by Beltran South Leyte 1.44 ± 0.63 1.53 ± 0.54
(1981). A total of five Saanen, eight La Mancha, nine Zamboanga del Sur 1.15 ± 0.37 1.26 ± 0.44
Toggenbergs, six Anglo-Nubian and 13 locally-born
‘crossbreds’ were compared for milk quality and quantity.
These genotypes were spread unequally and were Table 8.7 Kidding intervals of does of
unbalanced across three farms and little can be Anglo-Nubian/Native crosses at three
concluded about any breed effect. experimental locations (Aurelio, 1987)
Aurelio (1987) analysed a substantial set of data Location AN 75% 50%
from 5 years of records from does at PGSC (Tables
8.5, 8.6 and 8.7). Anglo-Nubian (100%) and 75% Pampanga 282 ± 55 320 ± 120 282 ± 84

and 50% crosses with Native animals were present. Bukidnon 269 ± 62 347 ± 94
His results partly support those of Maglunsod (1987). South Leyte 233 ± 70 321 ± 39

136
The evidence for a systematic effect of breed on
Table 8.8 FEC (in eggs per gram of faeces) over
kidding interval is not so strong in this study and,
the experimental period of 12 weeks
although based on small numbers, the trend from
South Leyte on a total of 23 does suggests that Breed Mean S.D.
Anglo-Nubians have shorter kidding intervals. Anglo-Nubian 108.50 47.98
Native 52.75 26.98
Effect of breed on resistance to parasites Source: Barcelo and Ancheta, unpublished data.
After a trickle Haemonchus contortus infection Native
goats (aged 3–4 months) had a lower FEC, lower worm
burden and higher PCV than Anglo-Nubian grade Table 8.9 Worm counts at the end of the
goats (Barcelo and Ancheta, unpublished data). This experimental period of 12 weeks
is the only evidence so far brought to the attention of
Breed Mean S.D.
the project which indicates a difference in resistance
between any two ‘breeds’ in the Philippines. The group Anglo-Nubian 100.50 58.63
of Native and Anglo-Nubian does which produced the Native 30.00 20.00
progeny used in that trial were joined in an uncontrolled Source: Barcelo and Ancheta, unpublished data.
way (i.e. pooled mating) to between three and five
bucks of each breed.
Caudilla (1983) measured FECs from August to February
Average faecal egg counts over the whole experimental
in ‘confined’ goats at the Dairy Training Research Institute
period are given in Table 8.8.
at Los Banos and presented these results as comparisons
This is not a complete representation of the result. between the three breeds represented in the nine
At week 9 there was a five-fold difference in FEC with animals in the study (three per breed). There were no
Anglo-Nubian the higher of the two breeds. A trickle significant differences between the average FECs of
infection of Haemonchus contortus was given three the Toggenburg, Alpine and Anglo-Nubian animals.
times a week for 3 weeks (a total of about 7000
larvae) and there was little difference in the course of
FEC trajectory until about week 8 of infection when the
FEC of the Anglo-Nubian grades ‘took off’ to a five-fold
difference. At week 12 some kids were slaughtered;
the worm counts are given in Table 8.9.

137
 Use of anthelmintics and Benzimidazole resistance in a field population of
Haemonchus contortus from sheep has been confirmed
anthelmintic resistance in Mindanao (Van Aken et al., 1994). More recently,
Johns (1983) describes albendazole as a useful broad methods have been developed for a larval development
spectrum anthelmintic. Campbell (1987) describes assay (LDA) to be used on farms in such circumstances
ivermectin as an even more useful anthelmintic and (Venturina et al., 2002). Using the LDA the efficacy of
there is a study of ivermectin in sheep under coconuts BZ anthelmintics in the Philippines was estimated by an
(Barcelona, 1994) which shows that it works well in vitro larval development assay using samples from
against gastrointestinal nematodes. over 200 farms representing areas of the country with
high goat and sheep populations (Ancheta et al., 2004)
Dajime (1982) undertook a dose response study The range of BZ efficacy estimated from the LDA results
of albendazole (Valbazen) in 48 male and female was 0–100% with mean efficacy of 82% and 64% for
goats of mixed ages in four groups treated with goats and sheep respectively. There were significant
2.5 to 10 mg/kg and exposed to a natural infection. associations between efficacy and parameters measured
There was a 75% reduction in FEC in the group given to characterise the sampled farms: size of animal
the lowest dose and 100% in the others. From larval management group, FEC of sample, recent importation
cultures Strongyloides was the most common genera, of stock and no access to common gazing were all
with counts as follows: (Strongyloides 2694, Cooperia correlated with decreased efficacy. Likewise, low
211, Haemonchus 115, Oesophagostomum 114, efficacy was associated with reported frequency and
The control of helminths in small ruminants in the Philippines

Trichostrongylus 53 and Ostertagia 27). The author number of years that BZ drenches had been used.
concludes that 10mg/kg is required for complete
clearance of Strongyloides (measured after 5 days).
Measurement of production
Kimwell (1988) tested a single treatment with closantel
(Parasitec Plus®) in 16 female sheep aged 3 years that in grazing environments
were infected with H. contortus. Information on dose
As a guide to the stocking rates that might be used
rate was not provided. Based on FEC it was completely
for different grazing systems in coconut plantations,
effective.
Faylon et al. (1991) recommended a rate of five
Cabrera (1992) gave albendazole at the MRDR to sheep/ha on the basis of the productivity per ewe
does at the 10th and 20th days of pregnancy. One and the overgrazing that took place at 10 head/ha.
out of the eight does gave birth to a kid with forelimb In that trial no impact on coconut yield was detected
abnormalities but cause could not be definitely attributed but it should be noted that no ungrazed areas were
to the drug treatment as there was no comparable used for comparison. Soil structure and organic matter
group of untreated does. also improved at both stocking rates.

138
Sabutan and King (1993) investigated interactions
between sheep and goat growth rates, forage types and
stocking rates in a grazing trial in Kabacan, Cotobato
over 5 months in 1989 and 1990. Of interest to this
project is that the stocking rates ranged from 40 to 80
goats per ha. Elephant grass yielded more and the goats
lost more weight than sheep during the trial, possibly due
to declining pasture availability. Leucaena was available
as browse to all animals.
Posas (1981) compared goat production and impact of
soil, pasture and coconut production at stocking rates of
20, 40 and 60 goats [2, 4 and 6 Animal Units (AU)]
per ha. Rotational grazing was practised and rotation
was initiated by visual inspection of the pasture. Confined
animals grew less well than grazing animals in terms
of gain/ha.year. In discussing these results Posas says
“liveweight, however, is not very important economically
since goats are mostly sold in the market per head”.
This infers that mortality is a more important production
parameter and in that study the overall mortality was
around 27% in both confined and grazing animals.
Neither parasites nor parasite control are mentioned in
the study but it should be noted that the ‘confined’ animals
were released for 1 hour per day for exercise when they
could have been exposed to high levels of parasitism.
On a steeply sloping site (32% gradient) Mandal (1988)
Increased supply of goat and sheep meat provides
showed that goats caused significantly heavier run off opportunities for employment. (G.D. Gray)
and erosion when grazing density reached 3 AU/ha.
year under coconuts.
A study on sheep grazing native vegetation under the thesis states “sheep are the most ideal ruminant
mangoes (Bejo, 1992) showed that 8–16 head/ha to integrate with mango because of its less destructive
was the optimum stocking rate. The introduction to feeding behaviour”.

139
 Under village conditions Parawan et al. (1986) Conclusions
measured the productivity of native sheep. Although the
aim of their trial was to look at the growth of castrates These conclusions are based on an incomplete search
vs. non-castrates they demonstrated that such trials are of the Philippine literature. However we consider it
possible. The trial was based at the ASEAN Goat and unlikely that there have been any major published
Sheep Centre. studies that the authors have not yet encountered in the
sources investigated or as citations in individual articles.
Domingo et al. (1991) measured the performance of
201 grazing ewes and pasture composition during a ■ The range of helminth parasites in sheep and
12-month period finding that there was weight loss in the goats in the Philippines has been documented.
rainy season and weight gain in the dry. No supplements ■ There are worm control recommendations in place
are mentioned in the abstract, nor any parasites, but but these have not been tested against possible
lamb mortality was slightly higher in the rainy season alternatives.
(9.5% compared with 8.7%). Lambing interval of ewes
which lambed in the wet was 22 days longer than for ■ There is little information on the economic impact
those which lambed in the dry. of any helminth parasite of sheep and goats under
farming conditions.
Ramos (1981) compared tethered, confined and
‘loosened’ goats and found that loosened goats had ■ There is no information available on the level and
the highest growth rates and provided the highest net frequency of use of anthelmintics or the extent of
The control of helminths in small ruminants in the Philippines

economic return. anthelmintic resistance.

Finally, a very general paper by Guss (1983) argued ■ Several studies indicate the potential for the use
that grazing goats in the tropics may not be successful of plant extracts as anthelmintics.
and it may be necessary to resort to a totally confined ■ Although such an effect has not been described
system on raised slatted floors. He concludes in the Philippines there is a wide range of nutritional
“In the Philippines … this simple inexpensive options available for improving resistance to
housing system has helped control internal parasites. Ipil-ipil (Leucaena leucocephala) is the
parasitism and has resulted in much better most widely tested proteinaceous supplement and
milk production” there is ongoing research on a tanniniferous legume.

Unless a sustainable system for the control of helminth ■ There is little genetic information available to suggest
parasites can be developed, Guss may yet prove to that any one breed or genotype has superior
be correct. resistance to endoparasites: the sole unpublished
study suggests that Native goats are more resistant
than Anglo-Nubian.

140
■ There have been no detailed comparisons of any Aliling R.C. 1980. Preliminary study on the performance
sheep or goat breeds for productivity under grazing of goats fed with paragrass (Brachiaria mitica Linn.)
or semi-confined conditions. and fresh ipil-ipil (Leucaena leucocephala [Lam.] de
Wit.) leaves with minimal supplementation of
■ There have been studies on grazing sheep concentrates. CLSU Scientific Journal (1985) 6 (1),
and goats that can be used as guidelines for 70 (abstract).
experimental design.
Alvarez F.R., Alvarez N.G., Herrera L.M. and Gonzales
F.S. 1985. Goat production under mango. 1.
Acknowledgments Liveweight gains of goats at different stocking rates.
Philippine Journal of Veterinary and Animal Sciences
The authors would like to thank the following for their 11 (3 & 4), 41 (abstract).
assistance with this review: for identifying articles and Alvarez F.R., Leung A.B. and Supan E.D. 1991. The
locating them, for suggesting new sources of literature performance of nondescript goats as affected by
and for commenting on various drafts: M. Manuel, systems of grazing. Philippine Journal of Veterinary
S. Eduardo, C. Mateo, O. Bondoc, C. Sevilla, and Animal Sciences 17 (1 & 2), 47–48 (abstract).
A. Sarabia, W. Cerbito, P. Barcelo, J. Batolos,
Amonruji M. and Rigor E.M. 1988. Reproductive and
D. Steane, C. Devendra and D. Pezo. The staff of the productive performance of Anglo-Nubian and crosses
UPLB CVM library and the Livestock Research Division in Mindanao. Animal Husbandry and Agricultural
of PCARRD deserve special thanks for all their help Journal 22(7), 12–13 [with copy of abstract in the
and patience. Philippine Journal of Veterinary and Animal Sciences.
1987. 13 (4), 50 and in the Animal Production
Technology Journal. 1988. 4(1), 42].
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Udin Z. 1985. Comparative performance of native goat dreams: a case of sustainable farming. Animal
bred with Anglo-Nubian and Saanen. MS thesis, Husbandry and Agricultural Journal 29(1), 52–53.
University of the Philippines Los Baños.
Yokota H., Cunanan C., Domingo A.T. III, Pusung L.J.,
Van Aken D., Lagapa J.T., Dargantes, A.P. Yebron, M.A., Server J. Jr., Robles A.Y., Lustria U.M., Himizu H.
Vercruysse J. 1994. Benzimidazole resistance in a field and Rigor E.M. 1991. Growth and milk production of
population of Haemonchus contortus from sheep in goats under intensive management. Philippine Journal
the Philippines. Phil. J. Vet. Anim. Sci., 20, 73–78. of Veterinary and Animal Sciences 17 (1 & 2): 15–20.
Venturina, V.M., Ancheta P.B., Dobson R.J., Eduardo S.L.
and Gray G.D. Use of a larval development assay to
estimate anthelmintic efficacy in goats in smallholder
farming systems. Philippine Agriculturist 86: 134–139.

149
9. Worm control for small ruminants in Indonesia
Subandriyo, T. Sartika, Suhardono and G.D. Gray

Introduction
In common with several Asian countries with large and Nari 1980, Ronohardjo et al. 1985, Ronohardjo
Muslim populations, small ruminants are important for and Wilson 1987). Ronohardjo et al. (1985) estimated
farmers with small areas of land, or who are landless the annual loss caused by fasciolosis and haemonchosis
and can access only the forest, cropping or plantation in large and small ruminants at 32 and 7 million USD,
land of others. Of the seven million sheep and 12 million respectively. Thus, several institutions and large projects
goats in Indonesia (FAOSTAT 2002, available at have devoted resources to basic and applied research
http://apps.fao.org/default.htm) 53% of the sheep in this area.
and 90% of the goats are on the island of Java with
The focus of this work has been in Java but one large
sheep being more common throughout the wetter areas
project — the Small Ruminant Coordinated Research
of the country. Sheep and goats are raised for a variety
Project (SR-CRSP) — invested heavily in addressing the
of purposes including meat, milk and manure production,
major constraints to small ruminant production, including
cultural and religious functions, and investment.
internal parasitism, throughout Indonesia. The SR-CRSP
Indonesian sheep (Sumatra thin tail, Javanese thin and was a USAID funded collaborative research program
fat tail) and goat breeds (Kacang and Etawah Grade) carried out between the Research Institute for Animal
are well adapted to the extreme tropical environment, Production (RIAP) of the Indonesian Agency for
temperature fluctuations, high humidity, low quality Agricultural Research and Development and US based
forages and high parasite infestation. The production institutions: the universities of California–Davis, North
system generally consists of confinement at night and Carolina State and Missouri–Columbia, and Winrock
grazing during the day. One of the major constraints International. The many working papers generated by
of this production system is endoparasitic infection this project can be found in the ILRI–Philippines library
(Handayani and Gatenby 1988). Helminth diseases or in the Sustainable Parasite Control in Small Ruminants
regarded as economically important for small ruminants bibliographic database, available on CD or via
in Indonesia are haemonchosis and fascioliasis (Soetedjo the internet (see Preface for details).

151
 This chapter reviews the Indonesian literature on Worm control options
endoparasite control for small ruminants. Literature
reported generally includes journal articles, papers from
meetings and conferences, undergraduate, master and
Grazing management
PhD dissertations, and abstracts and research reports Endoparasitic infection is widespread and a major
published after 1980. Some relevant earlier articles constraint to small ruminant production where continuous
have also been included. grazing is practised, particularly grazing associated
with tree cropping (Carmichael 1990). The findings
of Carmichael et al. (1992), from sheep grazing
Endoparasites of small ruminants rubber plantations, suggest helminthiasis is a perennial,
in Indonesia not a seasonal, problem in Indonesia. It is expected
that reducing the time animals spend in a pasture by
Building on the summary of Carmichael (1993), increasing the frequency of rotation or lengthening the
Table 9.1 lists the most important endoparasites rotational cycle can depress the population of parasites
of goats and sheep in Indonesia. on pasture, and thus increase animal productivity.
Several other endoparasites, of lesser economic Carmichael et al. (1992) showed that sheep grazing
importance, have also been described. They include the pasture under rubber plantations, 12–14 weeks after
genera: Bunostomum, Chabertia, Cooperia, Dicrocelium, contamination with worms, had dramatically reduced
Gongylonema, Moniezia, Ostertagia, Paramphistomum, faecal egg counts compared with sheep allowed to
Schistosoma, Strongyloides, and Trichuris (Arifin et al. graze the pasture within 4–6 and 8–10 weeks. The
1996, Atomowisastro and Kusumamihardja 1989, total worm burdens of sheep allowed to graze 8–10
Beriajaya 1984, Carmichael et al. 1992, Dorny et al. and 12–14 weeks after pasture contamination were
Worm control for small ruminants in Indonesia

1996, Effendy and Sumiaty 1999, Firmansyah 1993, reduced by 83% and 96% respectively, compared with
Mirza et al. 1996, Ridwan et al. 1996, Soetedjo and the 4–6 weeks group. This is consistent with control
Nari 1980). measures based on rapid rotational grazing (Barger
For studies of the biology and pathology of Haemonchus et al. 1994) which depends on relatively short survival
contortus and Fasciola gigantica in small ruminants in of larvae on pasture in the tropics.
Indonesia, refer to the Sustainable Parasite Control in Similar results were reported by Batubara et al.
Small Ruminants bibliographic database (see Preface (1995, 1996) in their studies of infectivity of pastures
for details). contaminated with H. contortus. The lowest mean number
of abomasal worms was found in animals grazing
pastures that had not been grazed for 12 weeks
(average total worm count 29 worms) compared with

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Table 9.1 The most important endoparasites of goats and sheep in Indonesia

Endoparasite References Comments

Nematodes
Haemonchus contortus Atomowisastro and Kusumamihardja 1989, Anaemia, poor growth, low milk
Beriajaya 1984, Beriajaya 1986, Carmichael supply in ewes, weakness, death
et al. 1992, Chotiah 1983, Darmono 1982,
Dorny et al. 1996, Effendy and Sumiaty 1999,
Mirza et al. 1996, Nasution 1988, Ridwan et al.
1996, Soetedjo and Nari 1980, Soetjedjo et al.
1980, Wilson et al. 1993
Trichostrongylus Atomowisastro and Kusumamihardja 1989, Appetite depression,
colubriformis Beriajaya 1984, Beriajaya 1986, Beriajaya poor growth, diarrhoea
and Stevenson 1986, Dorny et al. 1996,
Ridwan et al. 1996
Oesophagostomum Arafin et al. 1996, Beriajaya 1984, Beriajaya Appetite depression, diarrhoea,
columbianum 1986, Soetedjo and Nari 1980 dehydration, extensive nodule formation
and abscesses in small intestine
Oesophagostomum Arafin et al. 1996, Beriajaya 1984, Beriajaya Appetite depression, diarrhoea,
asperum 1986, Carmichael et al. 1992, Soetedjo and dehydration, severe nodule formation.
Nari 1980 Cases of O. columbianum may
actually be O. asperum

Trematodes
Fasciola gigantica Beriajaya 1984, Boray 1985, Effendy and Evidence that primarily a problem
Sumiaty 1999, Soetedjo and Nari 1980 of large ruminants and much less
important in goats and sheep. Indigenous
sheep breeds relatively resistant to
infection (Wiedosari and Copeman
1990, Weidosari et al. 1991)
Eurytrema pancreaticum Carmichael et al. 1992, Dorny et al. 1996, May be more important than currently
Graydon et al. 1992, Soetedjo and Nari recognised as cause of chronic,
1980, Wilson et al. 1993 irreversible ill thrift leading to wasting
and death in adult sheep, particularly
in integrated plantation grazing

153
 animals grazing pastures that had not been grazed for fed control group maintained few worm eggs per gram
nine (37 worms) and 6 weeks (80 worms). Gatenby of faeces (epg) (geometric mean 0.5). Lambs grazed
and Batabura (1994) recommend that pastures should in the morning, midday and afternoon, had geometric
be rested for at least 10 weeks before animals are mean epg values of 48, 15 and 31, respectively. The
returned. lower worm burden of the midday group is attributed
to the dryness of the pasture at midday. Although the
In contrast, Ginting et al. (1996) found that 1-week
stall-fed group had the lowest epg, their weight gain was
grazing followed by a 6-week resting period had
not as high as the midday-grazed group, presumably
better worm control potential than both a 12-week
because the nutrition of the grazed pasture was
grazing with 12-week resting period and 6-week
superior. In 1982 Kusumamihardja studied the effect
grazing with 6-week resting period. Their study looked
of season and time of day on the presence of nematode
at the effects of grazing management and levels of
larvae on grass. Larvae numbers were higher in the
concentrate supplementation on parasite establishment
wet season than in the dry and the number on leaf
in two genotypes of lambs (Sumatra and crossbred blades was highest in the morning. Another study by
St. Croix x Sumatra) infected with Haemonchus Kusumamihardja (1988) also reported that the degree
contortus. Improving the nutritional status of lambs by of nematode infestation during the rainy season was
increasing the level of supplement offered may have significantly higher than in the dry season but found
depressed the establishment of Haemonchus contortus no age group (lambs, young, and adult) effect. In the
in the lambs. The two genotypes had similar faecal dry season, worm burdens were significantly higher
egg counts at a supplement level of 0.5% bodyweight, in the group grazed in the morning than in the group
but at 1.6% bodyweight the crossbred lambs had that grazed in the afternoon. However, there was no
a lower worm burden than the Sumatra ones. significant difference between morning and afternoon
Whatever the optimum period for larval numbers to grazing during the wet season. Carcass dressing
Worm control for small ruminants in Indonesia

decline on pasture, the decision to leave the pasture percentage was affected by season, age of sheep
ungrazed must balance the conflicting needs of feed and period of grazing. Higher carcass percentages
availability, feed quality, ability of sheep and goats to were recorded:
graze tall, regrown pasture, and the need to reduce ■ during the dry than the wet season
infestation with infective nematode larvae.
■ in adult sheep than in lambs
Time of grazing has also been shown to affect
■ in animals grazing in the afternoon than
worm burden (Mirza and Gatenby 1993a, 1993b).
Groups of four lambs were grazed in the morning in the morning.
(0800–1200h), at midday (1100–1500h) or in the The benefits of reduced grazing time, therefore, like the
afternoon (1400–1800h) while a control group was resting of pasture for many weeks, need to be balanced
stall-fed with grass cut in an ungrazed area. The stall- against possible reduced intake and nutritional status.

154
Zabell et al. (1992) reported that washing forage,
using forage from ungrazed areas and allowing
animals to graze in rotational systems all resulted in
lower transmission of strongyles than if contaminated
forage or dried contaminated forage were fed.
To control Fasciola infections, Suhardono et al. (1998)
recommended that animals be fed fresh rice straw that
had not been immersed in water. This was based on
the observation that sheep fed on the bottom wet 10 cm
of the rice stalks, which harbour 98% of the flukes,
become much more heavily infected than those fed
on stalks cut above 10 cm.

Anthelmintics

Plants and plant products as anthelmintics

Traditional veterinary medicine is used extensively
by smallholders in rural Indonesia and has significant
potential to solve sheep health problems (Adjid 1990). Children often care for small ruminants and benefit most
The Small Ruminant Collaborative Research Support from increased family income. (G.D. Gray)
Program conducted a workshop at the Central Research
Institute for Animal Science in Bogor in 1990 to collect and Murdiati (1991), Sangat-Roemantyo and Riswan
information on this topic. Diseases of the digestive tract (1991), Murdiati (1991), Gultom et al. (1991), and
(worms, diarrhoea and bloat) were the ones most Murdiati and Muhajan (1991), lists the most common
frequently treated with traditional medicine. Parts of medicinal plants used to treat worm-infected ruminants
plants used to prepare veterinary remedies include in Indonesia. The most common medicinal plants used
seeds, leaves, fruits, tubers, roots and rhizomes, or, for worms in Bogor, West Java, are the leaves of
for herbs, whole plants. Medicinal plants are fed to Antidesma bunius (huni) and Cyclophorus nummularifolius
animals alone or mixed with other ingredients such (deduitan) (Adjid 1990, Mathias-Mundy 1992,
as eggs, honey, shrimp paste, salt, soy sauce or sugar. Wahyuni et al. 1992).
Table 9.2, which builds on the work of Mathias-Mundy

155
 Table 9.2 Medicinal plants used to treat ruminants with worms in Indonesia

Scientific name Family Local name Part used

Allium sativum L. Amaryllidaceae Bawang putih Bulb

Anacardium occidentale (cashew) Anacardiaceae Gajus Skin of fruit
Ananas comosus L. Merr (pineapple) Bromoliaceae Nanas Fruit/juice of fruit
Antidesma bunius L. Euphorbiaceae Huni Leaves
Areca catechu L. Arecaceae Pinang Seeds
Artemisia vulgaris Asteraceae Sidomolo Leaves
Bamubusa (bamboo)? Gramineae Buluh Shoots
Carica papaya L. Caricaceae Papaya Leaves, latex
Codiaeum variegatum (L.) Bl Euphorbiaceae Puring Leaves
Cucurbita domestica Val Cucurbitaceae Kunyit Rhizome
Cucurbita moschata (Duck) Poir Cucurbitaceae Labu merah Fruit
Curcuma aeruginosa Zingiberaceae Temu hitam/ireng Rhizome
Curcuma heyneana Val. and v. Zijp. Zingiberaceae Temu giring Rhizome
Curcuma xanthorrhiza Roxb. Zingiberaceae Temulawak Rhizome
Cyclophorus nummulariforus Polypodiaceae Deduitan Leaves
Hibiscus tiliaceus Malvaceae Waru Leaves
Languas galanga Zingiberaceae Lengkuas Rhizome
Worm control for small ruminants in Indonesia

Leucaena leucocephala Fabaceae Lamtoro Seeds

Monordica charantia L Cucurbitaceae Paria/Pare fruit Leaves
Morinda citrifolia L. Rubiaceae Pace, Mengkudu Fruit
Musa (banana) Musaceae Pisang Blossoms
Nicotiana tabacum L. Solanaceae Tembakau Leaves
Piper nigrum L. Piperaceae Merica Seeds
Terminalia catappa Combretaceae Ketapang Leaves
Zingiber purpureum Zingiberaceae Bangle Tuber

156
Use of these plants by farmers does not necessarily
mean they are effective as dewormers. Many plants
and their products have been tested in vitro and in
vivo for efficacy and such studies are described here.
The anthelmintic properties of both the seed and sap
of Carica papaya (papaya) have been studied in vitro
and in vivo in sheep. Beriajaya et al. (1997) reported
that 1.5% solutions of ground papaya seed killed adult
H. contortus in vitro within two hours and 1% solutions
of papaya sap had the same effect within 4.5 hours.
Subsequently, Beriajaya et al. (1998) used papaya
seed as anthelmintic on sheep infected with 10,000
larvae. In this study papaya seed was oven-dried at
37°C for 24 hours and ground into a powder. The
powder was given to three groups of experimental
animals at 0.75 g/kg, 1.5 g/kg and 3.0 g/kg body
weight, daily for one week. The numbers of adult worms
present were not significantly different among the three
treatments and the control group, but egg counts were.
It was concluded that papaya seed could be used as
anthelmintic in sheep if given for a long time. Gunawan
Confinement of goats offers employment opportunities
(1992) gave young worm-infected Javanese fat tail
in the cutting and carrying of feed. (G.D. Gray)
rams suspensions of papaya seed at several dosages
(3.6, 7.2, and 10.8 g per 100 ml) and compared
the animals’ egg counts with those of infected rams The effect of papaya sap on sheep artificially infected
treated with levamisole at 8 mg/kg body weight and with H. contortus was reported by Kusnadi (1999).
infected controls. Results showed that papaya seed Four weeks after infection, the animals were divided
effectively reduced the egg count of sheep, but was into five groups: three groups were given papaya
less effective than levamisole. Murdiati (1997) showed sap orally at 0.5, 0.6 or 0.7 g/kg for three days;
that sheep artificially infected with H. contortus given one group was treated with albendazole (Valbazen)
0.75 g/kg body weight of papaya sap had significantly at 5 mg/kg for three days; and the control group was
reduced worm egg counts compared with controls. not treated. Faecal and blood samples were collected

157
 weekly from zero to 6 weeks. At the end of the study The efficacy of Curcuma aeruginosa (temu hitam)
period the animals were slaughtered to obtain worm tuber was compared with 15 mg/kg of mebendazole
counts. Papaya sap at the given dosages had low in sheep infected with digestive tract worms (Agustin
efficacy in reducing H. contortus infection and the 1994). C. aeruginosa and mebendazole both reduced
0.7 g/kg dosage was toxic. Satrija et al. (1999) also egg counts but the commercial product was more
did not recommend using papaya sap for controlling effective. C. aeruginosa tuber at dosages of 3, 6 and
gastrointestinal nematodes in sheep due to high toxicity. 9 g reduced egg counts by 83%, 90.5% and 91%,
Post-mortem examination showed that papaya sap respectively. Bendryman et al. (2000) reported that urea
molasses mineral block (MUMMB) containing Curcuma
seemed to cause haemorrhage as a result of erosion
xanthorrhiza (temulawak) or C. aeruginosa (temu hitam)
in the gastrointestinal mucosa possibly due to proteolytic
roots only, or a combination of the two, can reduce
activity of enzymes in the sap. There is no information
the egg count of sheep infected with H. contortus by
on an increased use of papaya products as a routine
97.20%, 94.81% and 95.68%, respectively. The use
deworming treatment.
of the two plants in MUMMB was proved safe by liver
Karo-Karo (1990) reported the effect of nicotine function tests (SGOT and SGPT) and kidney function
extract. Extract from chopped tobacco leaves (0.94%) tests (blood urea nitrogen and creatinine).
at dosages of 27–207 mg per animal was found to Zingiber purpureum (bangle) tuber was used in the
enhance H. contortus egg production in goats, however, form of infusion and extract against larvae and adult
a dosage of 311 mg depressed egg production by H. contortus in vitro (Herawaty 1998, Murdiati et al.
78%. Nicotine extract was able to reduce egg numbers 1998). Murdiati et al. (1998) concluded that extract
but not the number of adult worms. and infusion of Zingiber purpureum both have
anthelmintic effects.
Beriajaya et al. (1998) studied the effect of Areca
catechu (pinang) seed extracts on adult H. contortus Mahfoed (1995) reported on the anthelmintic
Worm control for small ruminants in Indonesia

in vitro. A. catechu seeds were sliced, oven-dried properties of pressed Monordica charantia (pare fruit)
at 40°C for four days, ground and then sieved with at concentrations of 100%, 50% and 25% with adult
a 75 µm mesh. Solutions of A. catechu were made at H. contortus in vitro. Levamisole solution at 0.0032%
concentrations of 0.1, 0.2, 0.3, 0.4, and 0.5 g/ml. was used for comparison. At a concentration of 100%
All worms were killed when incubated with any of the efficacy of M. charantia did not differ significantly
the A. catechu solutions. The solutions had a similar from that of levamisole with both killing more than 50%
effect on larvae with more larvae being killed as of the worms after seven hours.
the concentration increased. The results of this trial Mulyaningsih (1995) studied the anthelmintic activity
indicated that A. catechu, which contains the alkaloid of Morinda citrifolia (mengkudu) fruit juice in sheep.
arecholine, may have anthelmintic effects in vivo. M. citrifolia juice was administered orally once a week

158
for nine weeks. The juice reduced the worm numbers,
increased body weight and influenced the haematology
of infected sheep. Extraction studies to trace the active
ingredient in the M. citrifolia fruit were reported by
Hildasari (1998) and Murdiati (2000). The chloroform
fraction, containing alkaloid and anthraquinone, was
the most effective against adult worms (100% death
after two hours) and worm eggs. However, Nurhayati
(2000) used the chloroform extract of M. citrifolia fruit
on sheep infected with H. contortus and found that it
did not significantly reduce the number of worms and
egg production of the sheep.

Commercial anthelmintic products

Several studies of the effectiveness of commercial
deworming products have been conducted. The
cost, activity spectrum, effectiveness, and toxicity
of commercial anthelmintics vary significantly.
Soetedjo et al. (1980) found that, despite the presence
of large populations of infective H. contortus larvae
on pasture and herbage grasses, a single injection of
disophenol in smallholder sheep suppressed the numbers Butchers, abattoir workers and associated labourers
of H. contortus to low levels for up to 3 months. benefit from increased supply of animals. (G.D. Gray)

Comparing the broad-spectrum anthelmintic, levamisole- sheep and goats, found that broad-spectrum anthelmintic
phosphate, with the long-acting narrow-spectrum product, significantly increased weight gain. Closantel treatment,
closantel, in naturally infected village sheep showed which was effective in removing Haemonchus but
that levamisole could significantly improve the weight had little effect on the other nematode species, did not
gain of animals (Beriajaya and Stevenson 1985a, result in significant improvement in weight gain. Similarly,
1985b). Based on the slaughter value of the treated no weight gain was seen using disophenol, a long-
animals and the cost of the drug used, there was a acting narrow spectrum anthelmintic given as a single
clear financial benefit from treating the sheep. Beriajaya injection. These results suggest that nematodes other than
and Stevenson (1986), comparing four anthelmintics in Haemonchus are the cause of reduced weight gain.

159
 In a study on albendazole in naturally infected local Thiophanate at 70 mg/kg, albendazole at 5 mg/kg,
sheep in Cirebon, Beriajaya (1986a) reported that pyrantel-pamoate at 20 mg/kg and levamisole HCl at
the group treated with albendazole at a dose rate 8 mg/kg were all effective against strongyle infection
of 3.8 mg/kg every month for six months had a in sheep (Sudarmadi 1989). Thiophanate and pyrantel-
significantly lower average egg count than the pamoate significantly increased the erythrocyte count,
control group. However, in Garut (Beriajaya, 1986b), haemoglobin concentration and percentage PCV.
differences in growth rate were not significant between Albendazole significantly increased the erythrocyte
treated and untreated groups. This is probably because count and haemoglobin concentration but not PCV,
sheep in Garut were confined and so the egg count while levamisole significantly increased PCV, but not
was too low to have a marked effect on growth rate. erythrocyte count and haemoglobin concentration.
Hartati (1989) reported that sheep naturally infected
with gastrointestinal nematodes and then treated with Dorny et al. (1995) studied anthelmintic efficacy in sheep
albendazole at 4 mg/kg grew significantly better on a breeding farm and on seven smallholder farms in
than untreated sheep. However, red blood count, North Sumatra, Indonesia. Albendazole was tested on
haemoglobin, PCV and total plasma protein were all farms and febantel, levamisole and ivermectin just
only slightly higher than those of the control group. on the breeding farm. On the large breeding farm
the efficacy of albendazole, febantel, ivermectin
Noviyanti (1992) used ivermectin dosages of 50, 100
and levamisole was 99%, 100%, 99% and 95%,
and 200 µg/kg in goats and reported that the levels of
respectively. The efficacy of albendazole was 100%
erythrocytes, haemoglobin, PCV, lymphocytes, monocytes
on the seven smallholder farms. The results indicate that
and neutrophils did not significantly differ between
there was no anthelmintic resistance at the study sites.
treated and control animals. Eosinophil count was the
only blood parameter that showed a significant change. The use of anthelmintics to control Fasciola was studied
A comparison of ivermectin and doramectin, at by Brotowidjojo (1975, 1983) and Kusumamihardja
Worm control for small ruminants in Indonesia

a dosage of 200 µg/kg in sheep infected with (1978). Brotowidjojo (1975) looked at the efficacy
gastrointestinal nematodes, found no significant of clioxanide and rafoxanide on F. hepatica in sheep,
difference between the two products in reducing 6 and 12 weeks post-infection with 100 viable
egg count or improving growth rate (Pariyadi 1997). metacercariae. It was concluded that rafoxanide
Tetramisole treatment, combined with farm management at 3.75 mg/kg could be recommended for treating
practices, controlled gastrointestinal helminth infections immature infections of F. hepatica and that 7.5 mg/kg
in sheep (He et al. 1990). However, helminthiasis in was appropriate for adults. Clioxanide, because of its
this group of sheep was found statistically to be 20% substantially reduced efficiency intra-abomasally, was
associated with reduced mean live weight, indicating the not recommended for use against immature flukes but
need for more effective, broad-spectrum anthelmintics was found to provide a variably moderate to high
to improve animal productivity. efficiency against adult infections at the recommended

160
dose rate of 20 mg/kg. Furthermore, it was suggested
fasciolicides that do not contain a nitro-group, such as
clioxanide and rafoxanide, were effective when given
orally (preferably by drenching) without previous oral
administration of copper sulphate solution.
Kusumamihardja (1978) used Dovenix (active ingredient
nitroxinil) against natural gastrointestinal nematodes and
Fasciola infections in five sheep and reported that one
died a day after treatment. Post-mortem examination
showed that Dovenix was very effective against
Fasciola spp., but killed nematodes relatively slowly.
Gatenby et al. (1992a, 1992b) studied the effectivenes
of nitroxynil, praziquantel and albendazole against
pancreatic fluke (Eurytrema pancreaticum). Results
showed that albendazole and praziquantel significantly
reduced the level of pancreatic fluke infection, but neither
drug reduced it to a negligible level. More frequent or
higher doses of the drugs may be more effective, but
would almost certainly not be economical. Nitroxynil
appeared to be ineffective in controlling pancreatic
Theft can be prevented by total confinement while kids
flukes, but it reduced nematode egg counts.
and lambs are fattened for market. (G.D. Gray)
Resistance
Currently, internal parasites are controlled by regular
expenses. This suggests that making anti-parasite
administration of anthelmintics, but resistance to these
treatment available to farmers on a non-subsidised
drugs is emerging in Indonesia and other parts of
free-market basis is viable. The rapid improvements
Southeast Asia (Venturina et al. 2003, Beriajaya et al.
in animal condition from just one treatment, and the
2003; and described in detail in Chapter 4).
provision of practical information, are likely to make
Delivering commercial anthelmintics to farmers farmers willing to invest in parasite control (Scholz 1992).
Cost–benefit analyses of parasite control in sheep using Misniwaty et al. (1994) reported that anthelmintic cost
commercial anthelmintics show good returns on the health was only 1.8–3.0% of the total revenue received from
care investment. Marginal return using parasite control selling fattened sheep.
amounts to Rp 42,000 revenue for Rp 4200 treatment

161
 Possible anthelmintic distribution schemes, via livestock Biological control
traders, local poultry shops and extension workers, were
Beriajaya and Ahmad (1999) investigated the use of
discussed by van Schie et al. (1992). The livestock
nematophagous fungi, Arthrobotrys oligospora, as a
traders cover a large area and are able to visit farmers,
biological control for H. contortus. Twenty young sheep,
but farmers do not trust them as much as extension
free of helminth infection, were orally infected with
workers. Extension officers only visit a limited number of
5000 H. contortus L3 larvae. After 6 weeks, half of
farms. The disadvantage of local poultry shops is that
the sheep were treated with the fungi (four times over
farmers have to go to the shop to buy the product but the
the following period of 6 weeks). Egg counts and
advantage is that they no longer depend on another
faecal cultures indicated that the group that received
person to deliver the medicines.
fungus produced fewer larvae than the control animals.
Kartamulia et al. (1993) stated that there is an urgent This preliminary study shows that nematophagous fungus
need to redefine the respective roles of government and can reduce live L3 H. contortus larvae numbers.
the private sector in the delivery of livestock services.
Biological control for fasciolosis can be targeted at the
In particular, the animal health sector offers attractive
intermediate host of Fasciola, the snail (Lymnaea spp),
opportunities for greater private involvement. Reasons
or at the larvae of Fasciola that still lives in the snail.
why farmers do not use animal health care products
Studies of Echinostoma revolutum larvae as an agent for
include: small flock sizes, the expense of products due
biological control of F. gigantica have been conducted
to the large sizes sold (e.g. 1 L bottles of anthelmintic)
by the Research Institute for Veterinary Science (Balitvet)
and the difficulty in obtaining products at the village
and reported by Estuningsih (1991, 1998a,b).
level. To overcome these problems, an animal health
Estuningsih concluded that the dominant antagonism of
delivery network for distributing anthelmintics was
E. revolutum over F. gigantica in L. rubiginosa and the
developed by the Small Ruminant Coordinated Research
Worm control for small ruminants in Indonesia

reduction of fecundity and longevity of snails infected

Project and Research Institute of Animal Production
with E. revolutum could be useful for biological control
Station at Sungai Putih, North Sumatra together with
of F. gigantica (1991, 1998a).
local livestock services and wholesalers of animal
medicine. This study, reported by Misniwaty and The competitive interaction of snails with Lymnaea
Kartamulia (1993), Kartamulia et al. (1993), Misniwaty rubiginosa, the intermediate host of F. gigantica
et al. (1994) and reviewed by Misniwaty et al. (1996), has also been studied. After 8 months the population
indicated that the most effective way to distribute animal of L. rubiginosa decreased and the population of
health care is via an extension worker who is organized snails Thiara scabra and Physa doopi increased.
as a supplier in a specific area. The competitive interaction does not seem to be due
to competition for food but to chemical factors, possibly
water-soluble pheromones (Estuningsih, 1998b).

162
Table 9.3 Summary of H. contortus vaccination studies in Indonesia

Host Vaccination/infection type Summary of findings References

Sheep Exsheathed larvae No response Beriajaya et al. (1995)

Irradiated larvae Some serological response using Partodihardjo, (1996), Setiawati
range of techniques (1996), Suryastuti (1996), Syah (1994)
Irradiated larvae Reduced pathogenicity Henriana (1997)
Irradiated larvae No effect on egg counts but serum Beriajaya and Partodihardjo (2000)
proteins elevated
Irradiated larvae (double dose) Positive results Partodihardjo et al. (2000),
Partodihardjo et al. (1998)
Extract with range of adjuvants No effect Berliana (1998), Heryani (1998)
Extract No effect on egg count Beriajaya and Suhardono (2000)
Goats Infective larvae No solid immune response Maryani (1997)

Table 9.4 Summary of Fasciola vaccination studies in Indonesia

Host Nature of study/vaccination Summary of findings References

Protein antigen characterisation 2 antigenic proteins identified Estuningsih and Widjajanti (1999)
Sheep Extract + adjuvant Immune response greater with adjuvant Widjajanti (1999a,b)
Irradiated Significant resistance Wiedosari et al. (1996)
Irradiated Decreased infective capability Tuasikal et al. (1996)
Irradiated Good immune response and Arafin and Tuasikal (1998)
decreased infectivity
in vitro Antisera from sheep No cross protection against Estuningsih et al. (1999)
F. hepatica
Sheep Infective metacercariae Goats more resistant to infection Arafin (2000)
& Goats
Goats Irradiated 45 Gy irradiation optimal for Arafin et al. (2000)
decreased infectivity

163
 Suhardono (1998) proposed biological control of In 1988, Ginting reported that supplementation
F. gigantica in rice fields by means of competition of concentrate feed (high plane nutrition) in lambs
between trematode larvae in the snail L. rubiginosa. infected with H. contortus, reduces worm burdens
Ducks naturally infected with trematodes, were used and can reduce the need for anthelmintics to control
as the source of competitive larvae. The study showed endoparasites. Although feed supplementation can
that Fasciola infection in L. rubiginosa was depressed reduce susceptibility to parasite infection, the response
by other trematodes which were more dominant in varies according to breed and level of infection.
infecting the snail intermediate host. This indicates that interaction between genotype and
environment affects susceptibility to parasite infection
Vaccination (Ginting et al. 1996).
Several immunological studies to find candidate Beriajaya and Copeman (1996) studied the effect
vaccines for haemonchosis and fasciolosis have been of season on gastrointestinal nematodes and weight
conducted (Tables 9.3 and 9.4). Research on irradiated gain in recently weaned sheep and goats. The effect
and non-irradiated parasites has been performed mostly of parasitism was assessed by comparing weight gain
at the Research Institute for Veterinary Sciences (Balai of untreated animals with that of animals treated with
Penelitian Veteriner) in collaboration with the Central oxfendazole or albendazole every 2 weeks. There
Research and Development for Isotope and Radiation was no difference in weight gain between treated
Technology, National Atomic Energy Agency (PAIR, and untreated sheep and goats during the dry season.
BATAN). The development of an effective vaccine During the wet season weight gain dropped by half in
remains an important challenge. untreated animals and by about 20% in treated animals.
As faecal egg counts for each group were the same
Nutritional supplementation throughout the year the low level of nutrition during the
Worm control for small ruminants in Indonesia

wet season was the main determinant of pathogenicity

While publications about the effect of nutritional
supplementation on small ruminant production are of worms. Improved nutrition during the wet season,
readily available (Subandriyo 1993), research on particularly for the first 10 weeks after weaning,
the effect of nutritional supplementation on their may remove the need for anthelmintic therapy.
endoparasite infestations is limited. Beriajaya et al. (1995) tested feeding blocks
Handayani and Gatenby (1986, 1988) studied containing 3% phenothiazine in solidified molasses
the effect of four levels of legume supplementation in (Wormolas, Animeal Australia Ltd) for their ability to
conjunction with two grazing management schemes control gastrointestinal nematode infections, and their
and anthelmintic treatment or non-treatment. They found effect on mineral status, in village sheep in Cirebon.
that sheep on low levels of nutrition are more susceptible The mean egg count of the treated group decreased
to helminthiasis than well-fed animals. from 576 epg to 123 epg and the percentage of sheep

164
Table 9.5 Studies of genotypic differences in resistance to H. contortus in sheep

Genotypes compared Findings References

Sumatera thin-tail Javanese fat-tail x Sumatera thin-tail and St. Dorny et al. (1994),
St. Croix Croix x Sumatera thin-tail most susceptible. Romjali et al. (1994),
St. Croix x Sumatera thin-tail F1 Barbados Blackbelly x Sumatera thin-tail Romjali (1995), Romjali
Javanese fat-tail x Sumtera thin-tail F1 most resistant et al. (1997)
Barbados Blackbelly x Sumatera thin-tail F1
St. Croix x Sumatera thin-tail F2
Sumatera thin-tail Faecal egg counts similar for all breeds, Batubara et al. (1994)
Virgin Island and 90% Virgin Island excluding, Virgin Island ewes which had
Virgin Island x Sumatera thin-tail F1 lower egg counts
Barbados Blackbelly x Sumatera thin-tail F1 Time of sample and individual animals
Virgin Island x East Java fat-tail F1 within breeds had significant effect on
Virgin Island x Sumatera thin-tail F2 counts
Sumatera thin-tail At high levels feed supplementation St. Croix Ginting et al. (1996)
St. Croix x Sumatera thin-tail crosses better able to withstand parasitism Ginting et al. (1999)
25% Barbados Blackbelly, 25% St. Croix, Sumatera thin-tail more susceptible to
50% Sumatera thin-tail internal parasites than composite genotype
Sumatera thin-tail Barbados Blackbelly x Sumatera F1 Mirza et al. (1994)
Barbados Blackbelly x Sumatera thin-tail F1 and St. Croix x Sumatera F2 had lowest
Javanese fat-tail x Sumatera thin-tail F1 egg counts
St. Croix x Sumatera thin-tail F1 No substantial differences between
St. Croix x Sumatera thin-tail F2 genotypes in terms of worm counts
Sumatera thin-tail Javanese fat-tail x Sumatera thin-tail much more Gatenby et al. (1995)
Javanese fat-tail x Sumatera thin-tail F1 susceptible to parasitic infection
St. Croix and Sumatera thin-tail F1
St. Croix and Sumatera thin-tail F2
Javanese thin-tail Observed variation of resistance within genotypes Gatenby et al. (1991)
Sumatera thin-tail Carmichael et al. (1992)
Barbados x Sumatera F1 Romjali (1995)
Javanese fat-tail x Sumatera F1
St. Croix x Sumatera F1
Sumatera thin-tail No variation in resistance within genotypes Batubara et al. (1995)
St. Croix x Sumatera F1
Barbados x Sumatera F1
25% Barbados, 25% St. Croix, 50% Sumatera
Sumatera thin-tail No significantly difference in susceptibility or Batubara (1997)
St. Croix x Sumatera resistance between genotypes but large variation
Javanese fat-tail x Sumatera within each genotype
Barbados x Sumatera Hair sheep cross breeds similar to Sumatera
25% Barbados, 25% St. Croix, 50% Sumatera in terms of H. contortus infection

165
 producing viable larvae decreased from 50% to 24%. Indonesian thin-tail sheep are relatively resistant to
In contrast, egg counts of the control group increased the liver fluke. Wiedosari (1988) and Wiedosari and
from 768 epg to 4840 epg and the percentage of Copeman (1990) first showed that Indonesian thin-tail
sheep producing viable larvae increased from 65% to sheep, in this case Javanese thin-tail, expressed high
84% over the same period. In the treated group the innate resistance to challenge with metacercariae
number of Haemonchus larvae declined significantly from F. gigantica when compared with an equivalent
(36% to <6%) and at the end of the trial Trichostrongylus challenge in buffalo and cattle. Rumantiningsih (2000)
larvae predominated in larval cultures (>80%). Mineral showed that Javanese fat-tail sheep were more
analysis of untreated sheep revealed deficiencies in susceptible to F. gigantica than Javanese thin-tail
sodium and copper, low levels of zinc and normal levels ones. Spithill and colleagues confirmed the resistance
expressed by Indonesian thin-tail sheep in comparison
of potassium, calcium, magnesium and phosphorus.
with Javanese fat-tail and Merino sheep (Wiedosari
The feeding block significantly affected sodium and
et al. 1994, Roberts et al. 1995 1996a 1966b
zinc status but not copper although sufficient levels of
1997a 1997b 1997c, Estuningsih et al. 1996,
this element were available. Comparison of bodyweight
Spithill 1996).
gains showed a significantly higher rate of increase
in the treated animals Roberts et al. (1997a) deemed the basis of the
acquired resistance in Indonesian thin-tail sheep to
Genetic variation in resistance to parasites be an exceptional immunological capacity to respond
to an antigen, or an immunological suppressant, peculiar
Genetic variation in resistance to parasites has been
to F. gigantica. That molecule, produced by juvenile
reported in a series of studies conducted by the Small
parasites, warrants further study, as a candidate for
Ruminant CRSP in collaboration with the Research
a vaccine.
Institute of Animal Production and Research Station
Worm control for small ruminants in Indonesia

of Central Research Institute for Animal Sciences at A series of studies by Roberts et al. (1995, 1996a,
Sungai Putih, North Sumatra. Results were reviewed l997c) showed that a dominant gene may induce the
by Subandriyo et al. (1996) and Subandriyo and mechanism of resistance in Indonesian thin-tail sheep.
Widjajanti (1999). They also found indications that IgG2 acts as blocking
Genetic research on differences in resistance to antibody that interferes with the mechanism of resistance.
H. contortus among sheep breeds is summarised Hansen et al. (1999) postulated that IgG2 could act
in Table 9.5. as a blocking antibody for protective effector responses
against F. gigantica in sheep and that the Indonesian
Studies of the resistance of sheep to the liver fluke,
thin-tail sheep, by downregulating IgG2 responses, have
F. gigantica, have been mostly conducted by the
an enhanced capacity for killing F. gigantica in vivo.
Research Institute for Veterinary Science (RIVS, Balitvet)
in collaboration with ACIAR. Research shows that

166
A worm control program
in Indonesia
In developing health control strategies at least three
non-veterinary factors must be considered: farmer needs,
production systems and climatic factors (Wilson et al.
1996). The priority given to solving problems identified
by farmers has led to a farmer-first approach using
participatory methods such as those described in
Chapter 3. Strategies to minimise disease problems
include intervening in animal and pasture management,
using chemical agents, and developing host resistance
though breeding and nutrition. These strategies and their
delivery must be developed as part of an integrated
approach to disease control incorporating research,
extension, government and private sectors, suitable The support of diagnostic services is essential to make
technology, training and recognising the needs of good decisions about deworming. (G.D. Gray)
farmers. The farmer-first approach implies that research
and extension must at least include farmers and ideally During the Small Ruminant Collaborative Research
be led by them. Support Program, researchers designed training materials
to teach farmers improved strategies for animal raising.
The problems of farmers, however, are rarely simple
This information became the basis for a manual titled the
and, even if identified as being caused principally
Sheep and Goat Production Handbook for Southeast
by parasites, will often include several genera of
Asia (Merkel and Subandriyo 1997). The book contains
nematodes and flukes. According to Brotowidjoyo
a wealth of information relevant to the development
(1990) parasitic infections in domestic animals are
of an integrated approach to worm control. The third
generally polyparasitic rather than monoparasitic and
edition was developed to be used by:
are dependent upon a myriad of hosts, parasites and
environmental factors. Currently, parasite control is usually ■ farmers as an information source
based on chemical treatments that have disadvantages
■ extension personnel as a reference and
such as drug resistance (Beriajaya and Batubara 1996).
storehouse of training materials
This has proven to be the case in recent studies
(Venturina et al. 2003, Beriajaya et al. 2003) ■ scientists as a starting point in their quest to
on farms that use anthelmintics intensively. improve village sheep and goat production.

167
 As Merkel states, ‘The greatest impact and benefit ■ Several immunological studies to find candidate
will occur when all three: farmers, extensionists and vaccines for haemonchosis and fasciolosis have
scientists, work together’ (Merkel and Subandriyo 1997). been conducted but the development of an effective
vaccine remains an important challenge.

Conclusions ■ A wide range of information on the use of

nutritional supplementation to improve production
■ Small ruminant endoparasites in Indonesia, exists. However, there is little data about the effect
and their intermediate hosts, have been of nutritional supplements on parasite infestation.
well-documented.
■ There is little or no difference in susceptibility or
■ Grazing management studies show that rotational resistance to H. contortus between sheep genotypes
grazing, cutting forage at midday and/or at but large variation within each genotype. Indonesian
10 cm above the ground, and washing forage, thin-tail sheep appear to have innate resistance
all reduce levels of worm infection. to F. gigantica.
■ Smallholder farmers, particularly in Java, use ■ There is little data on worm control for goats
traditional veterinary medicine against worms. in Indonesia.
The efficacy of the medicinal plants must be
confirmed scientifically. Despite the extensive basic and applied research
on parasite control in Indonesia, worms remain a
■ Several studies of the effectiveness of commercial constraint to small ruminant production. There has
deworming products have been conducted. been little evaluation of the benefits of this research.
However, information on the level and frequency The impact upon communities may be difficult to
of anthelmintic use and the extent of anthelmintic measure, for example, the spillover benefits of using
Worm control for small ruminants in Indonesia

resistance is limited. appropriate chemicals at correct dosages, and greater

■ An animal health delivery network for distributing numbers of better-trained extension workers, are hard
anthelmintics and treatment information has been to quantify. Many of the technologies work well in
developed. It needs to be further tested and controlled settings but have had low levels of adoption
extended to other locations. by farmers. Hence, the need for a new approach to
improving the control of worms in sheep and goats,
■ Preliminary information on biological control using a model like that described in Chapter 3.
options for fasciolosis and haemonchosis has
been reported.

168
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Sheep Grazing in Rubber Plantation in North Sumatra. contortus male and female worms on sheep at Bogor
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antigen from Fasciola gigantica of different age) pencernaan kambing yang dipotong di rumah potong
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of worm find in the goat digestive tract that slaugtered
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at Tuban Regency Abatoir). Thesis. Fakultas Kedokteran
Lymnaea rubinosa in West Java. MSc (Veterinary) Thesis.
Hewan, Universitas Airlangga (Faculty of Veterinary
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Agriculture, James Cook University of North
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three drugs to control pancreatic fluke (Eurytrema domba terhadap tingkat infeksi Haemonchus contortus
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of sheep n the humid tropics – experiences in North concentrate supplementation on parasite establishment
Sumatra. Working Paper No 164, Small Ruminant in two genotypes of lambs infected with Haemonchus
Collaboratuve Research Support Program, PO Box 1 contortus. Jurnal Ilmu Ternak dan Veteriner 2 (2),
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infections of sheep in rubber plantations in Sumatra. concentrate supplementation on parasite establishment
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anthelmintic treatment on the performance of lambs production and fecundity of worm Haemonchus
in North Sumatera. Trop. Anim. Health Prod. 20, contortus (Rudolphi, 1803) on local sheep). Thesis.
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lokal yang diinfeksi dengan Haemonchus contortus
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breed infected with Haemonchus contortus (Rudolphi, pada domba yang diberi larva tiga dan ekstrak
1803). Thesis. Fakultas Kedokteran Hewan, Institut larva tiga Haemonchus contortus irradiasi (The effect
Pertanian Bogor (Faculty of Veterinary Medicine, of irradiated and extract infective larva Haemonchus
Bogor Agricultural University), Bogor. contortus on blood composition of sheep). Thesis.
Fakultas Biologi, Universitas Nasional, Jakarta.
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UGM 9(1), 7–10. cacing Haemonchus contortus Rudolphi secara in vitro
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He, S., Tiuria, R. and Satrija, F. 1989. Taksiran kerugian
(Zingiber purpureum Roxb) on Haemonchus contortus
produksi daging akibat infeksi cacing saluran
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pencernaan pada ternak domba (Estimated meat
Matematika dan Ilmu Pengetahuan Alam, Institut Sains
production loss due to infection of gastro-intestinal
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20–22 Agustus 1988, pp. 481–493. Perkumpulan Penyuntikan Ekstrak Cacing Haemonchus contortus
Pemberantasan Penyakit Parasit Indonesia, Jakarta. yang Telah Ditambah Adjuvan (Blood composition of
sheep resulting from injection of Haemonchus contortus
He, S., Kusumamihardja, S., Retnani, E.B. and Satrija,
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terhadap cacing lambung (Haemonchus contortus R) contortus, Rudolphi) pada kambing (Capra hircus Linn.)
secara in vitro (Sieving of chemical content and (Effectivity of nicotine extract of tobacco leaves toward
anthelmintic effect test of Mengkudu fruit (Morinda gastric worm (Haemonchus contortus, Rudolphi) in goat
citrifolia Linn.) on gastric worm (Haemonchus contortus (Capra hircus Linn.). Master Thesis. Sekolah Pasca
R) by in vitro). Thesis. Jurusan Farmasi, Fakultas Sarjana, Institut Pertanian Bogor, Bogor.
Matematika dan Ilmu Pengetahuan Alam, Institut
Sains dan Teknologi Nasional, Jakarta. Kartamulia I., Misniwaty, A. and Knipscheer, H. 1993.
Development of the private animal health delivery
Hill, T., Mirza, I., Batubara, A., Gatenby, R.M. and network in North Sumatra, Indonesia. Small Ruminant
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Ilman. 1995. Pengaruh temperatur terhadap daya tetas
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contortus pada domba (The effect of temperature on hemoglobin) kambing lokal—Effect the infection
the hatchability and survival ability of Haemonchus of Haemonchus contortus on blood composition
contortus larvae). Thesis. Fakultas Biologi, Universitas (number of erythrocyte, packed cell volume value
Nasional (Faculty of Biology, National University), and haemoglobin content) of local goat. Thesis.
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J.A. and Spithill, T.W. 1999. Studi komparatif S. and Spithill, T.W. 1994. High resistance of
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ST.Croix, Merino dan persilangan ITT dan St.Croix, Abstract. 8th International Congress of Parasitology,
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10. Worm control for small ruminants in Malaysia
R.A. Sani, M. Adnan, T.S. Cheah and P. Chandrawathani

Introduction
Although small ruminant production has been an This review covers work reported after 1980 on
important part of Malaysian agriculture for many years small ruminants pertaining to control of gastrointestinal
it is relatively minor compared with other sectors of the parasitism in Malaysia. The details of some studies that
livestock industry. Since the mid 1980s efforts to expand could contribute to formulating control measures are
the industry have focused on integrating sheep into included. Significant recommendations of some reports
the more than four million hectares of oil and rubber are also included.
plantations (Ibrahim 1996). The endoparasites found in goats and sheep in Malaysia
The 2000–01 figures from the Department of were described by Shanta (1982), Sani et al. (1985,
Veterinary Services, Malaysia, estimate the goat 1986), Amin et al. (1990) and Wahab and Adanan
and sheep populations to be about 235,000 and (1993). Common endoparasites include:
131,000, respectively. ■ Haemonchus contortus
Only one study, by Fadzil in 1977, has attempted to ■ Trichostrongylus spp.
measure the cost-effects of parasitism in small ruminants ■ Oesophagostomum spp.
in Malaysia. Losses (deaths, treatment costs and
■ Cooperia curticei
condemnation in abattoirs) in goats due to parasitism
were estimated at RM 44,400 (now USD 11.7). ■ Strongyloides papillosus
This is considered a gross underestimate because it ■ rumen flukes
was extrapolated from a 5-year record of the Central ■ pancreatic flukes
Animal Husbandry Station, Kluang, which recorded that
Ostertagia spp. and the lungworm Dictyocaulus spp.
only one in 937 goats died of parasitism each year.
were reported by Shanta (1982) as rare and were not
Other more recent studies, which record mortality, quote
found in the later studies. Perhaps these parasites were
much higher figures.
from imported goats and sheep.

189
 To assess the natural resistance of goats to parasitism, Epidemiological studies in goats suggest that grazing
46 goats, monitored from birth to 14 months, were not goats ingest many infective H. contortus, T. colubriformis
given any dewormer (Daud et al. 1991). Post-mortem and O. columbianum larvae at all times of the year
examinations revealed that 32% of deaths were due to in Malaysia (Sani et al. 1985, Dorny et al. 1995,
worms (mean H. contortus count 808, T. colibriformis Ikeme et al. 1986, Cheah and Rajamanickam 1997).
1177) and 30% of deaths to pasteurellosis pneumonia.
Further studies of the biology and pathology of
The goats that died of pneumonia also harboured worms
endoparasites in Malaysia have been conducted (Sani
(mean H. contortus count 236, T. colubriformis 203).
et al. 1994, Sam-Mohan et al. 1995, Cheah and
It was postulated that the worm burden, representing mild
Rajamanickam 1997, Daud et al. 1991, Dorny et al.
haemonchosis, weakened the goats so they subsequently
1995, Sam et al. 1995, Israf et al. 1996a, 1996b).
succumbed to infection by Pasteurella sp., leading
to pneumonia.
Pasteurella haemolytica is part of the normal flora of the Worm control options
nasopharynx of various animals and causes pneumonia
when animals are stressed. Zamri-Saad et al. (1994) Grazing management
demonstrated that sub-clinical haemonchiasis (dosing Studies of trichostrongyles on open pasture and on
with 4000–5000 infective larvae), without significant vegetation under tree crops found that eggs developed
reductions in total serum protein or packed cell to infective larvae in a minimum time of 3.5–4 days
volume, stressed goats enough to induce sufficient after faecal deposition and most larvae developed
immunosuppression and allow the development of within 7 days. Infective larvae on open pasture
experimentally induced pneumonic pasteurellosis. survived for 5–6 weeks, on vegetation under rubber
In a 15-month study on 13 goat smallholdings in the trees for 6–7 weeks and on vegetation under oil-palm
Worm control for small ruminants in Malaysia

state of Selangor, the mortality rate for animals up to trees for 5–8 weeks (Sani et al. 1994, Sam-Mohan
1-year-old was high at 74% (Symoens et al. 1993). et al. 1995, Cheah and Rajamanickam 1997). Earlier
Adult mortality was 34%. Pneumonia, mainly caused it was thought that larvae survived much longer in the
by Pasteurella sp., and haemonchosis were found microenvironment under the canopy of tree crops (Sani
to be the major causes of deaths in all age classes. and Rajamanickam 1990). The relatively short larval
Sam-Mohan et al. (1995) noted a mortality of 16% survival times observed allows for the integration of
from clinical haemonchosis in lambs and ewes that grazing management with worm control. Small ruminants
grazed on vegetation under oil palm trees. can safely graze for 3–4 days in an area which is
‘rested’ for 5–6 weeks.

190
During a 5-month trial, sheep grazing in a rotation
system, with 3–4 days on and 31 days off each
paddock, had significantly lower mean egg counts
compared with sheep permanently grazing the same
pasture and receiving a monthly drench of closantel
(Chandrawathani et al. 1995). A three and a half-
month study showed that sheep perpetually grazing
the same area under mature rubber trees had higher
egg counts compared with ones rotationally grazing
in a hedgerow planting system—3–4 days on and
35 days off each area (Sani et al. 1996).

Anthelmintics The Sanat Ines sheep from Brazil is one of several breeds
imported to Malaysia for evaluation. (G.D. Gray)
Commercial products
The control of worms in small ruminants in Malaysia, Resistance to anthelmintics
like elsewhere, relies heavily on chemical de-wormers or
anthelmintic drugs. Shanta et. al (1978, 1980, 1981a, Anthelmintic resistance has been suspected in Malaysia
1981b) published a series of reports on the use of since the 1980s with unofficial reports of drug failures.
benzimidazole compounds against gastro-intestinal worms In the early 1990s unpublished reports, particularly from
of goat. These trials report a high level of efficacy. institution farms, noted the ineffectiveness of anthelmintics.
However, in the 1980s and 1990s, other anthelmintics Dorny et al. (1991) in an investigation of the efficacy
were also used. Avermectin derivatives were noted as of currently available anthelmintics in Malaysia in
being highly successful in numerous reports (Sani and 10 smallholder goat farms, reported suspected
Siti-Suri 1989, Rajamanickam et al. 1990, Wahab benzimidazole resistance of H. contortus on two of
et al. 1993, Wahab 1997, Chandrawathani et al. the farms, using the faecal egg count reduction (FECR)
1998a). Closantel was also reported to be effective test. Levamisole resistance was also detected on two
(Dorny et al. 1994a, Chandrawathani and Adnan of the farms investigated.
1995, Chandrawathani et al. 1996a). A postal survey A nationwide survey reported the presence of
on the use of anthelmintics suggested that most farmers benzimidazole resistance in 33 out of 96 smallholder
used the four major classes of drugs (Chandrawathani goat farms by means of an egg-hatch assay (Dorny et al.
et al. 1994). 1994b). Correlation was found between drenching
frequency in the previous 2 years and the presence of

191
 benzimidazole resistant worms. Wahab (1994) also increasing. On a large government farm that served
reported resistance to benzimidazole by H. contortus on as a sheep breeding centre, anthelmintic resistance
eight out of 10 commercial goat farms in the northern increased in 3 years from being a moderate problem to
region of the country. one where total chemotherapeutic failure has occurred
(Chandrawathani et al. 2003).
Chandrawathani et al. (1996b) successfully used
a netobimin-levamisole combination drench in goats Medicated feed blocks
with a benzimidazole resistant strain of H. contortus.
Rajamanickam et al. (1992) tested an imported
However, 40 days after treatment, as a result of
commercial anthelmintic feed block on a group of
re-infection, the FEC reached pre-treatment values.
sheep and found relative success in reducing the FEC
Hence, a drug-dependent method of control is only
below levels in conventionally drenched sheep and
a short-term solution.
untreated controls. This is particularly significant as all
Ivermectin and benzimidazole-resistant strains of three groups grazed together with other sheep that had
H. contortus were isolated on an institution sheep farm no access to the block and that were not drenched.
that served as the source of breeding stock to farmers In a study of sheep grazing under rubber trees,
in Malaysia (Sivaraj and Pandey 1994). (Sani et al. 1995) animals were given locally made
Simultaneous resistance of H. contortus to urea molasses block with: no anthelmintic, 0.5g/kg
benzimidazoles and ivermectin and of T. colubriformis fenbendazole, or supplemented with palm kernel cake
to benzimidazoles and levamisole was found in sheep on meal. There was little difference between egg counts
another institution farm (Sivaraj et al. 1994). Moxidectin of animals receiving fenbendazole and those getting
was found to be effective against both worm species the unmedicated blocks. Even the supplemented animals
present on the particular farm, however, the authors were able to minimise the incidence of new infections.
do not recommend using moxidectin when ivermectin
Worm control for small ruminants in Malaysia

It is assumed that, provided the larval challenge is

resistance is known. Resistance to three anthelmintic ‘light’, the improved nutrition provided by the blocks,
classes on the same farm is particularly serious irrespective of incorporation of anthelmintic, as well
when the farm supplies breeding stock to smallholder as the supplementation, is sufficient to effectively reduce
farmers, and is hence ‘exporting’ animals with drug- the incidence of new infections. Further work by Maria
resistant worms. et al. (1996), where urea molasses blocks, medicated
The investigation by Chandrawathani et al. (1999) of or not, were effective in reducing new infections, lends
39 sheep and nine goat farms showed that most had support to this assumption. Hence, it is recommended
worm populations resistant to all classes of anthelmintics, that unmedicated blocks be given when supplementation
providing clear evidence that anthelmintic resistance is needed, so reducing the likelihood of anthelmintic
in parasites of small ruminants in Malaysia is rapidly resistance.

192
Chandrawathani et al. (1997) gave medicated
urea molasses blocks to all animals in a smallholder
sheep farm at a restricted economical intake of
60g/day/animal. The animals grazed permanently
on heavily contaminated vegetation (indicated by egg
count >7000 epg) under oil palm trees. After an initial
moxidectin drench and access to the blocks, egg
counts remained below 300 epg over 3 months.
Plants as anthelmintics
This aspect of ethnoveterinary medicine is at a fledgling
stage in Malaysia although there are undocumented
reports of the use of tamarind juice and legumes to
treat worms in goats. Large-scale sheep and goat production is commercially
viable where there is strong demand and efficient
When fresh leaves of the neem tree (Azadirachta indica)
marketing. (R.A. Sani)
were fed to a group of trichostrongyle-infected sheep,
faecal egg counts and larval recoveries were reduced.
The number of worms recovered in the neem-fed farm of 42 female 50% Poll Dorset x Malin (Malaysian
sheep was only 5–15% that of the control sheep indigenous breed) wool sheep and 20 female 25%
(Chandrawathani et al. 2002c). Neem leaves were Cameroon hair sheep grazing together, showed no
acceptable to the animals and there was no indication difference in egg counts from birth to 13.5 months (Sani
of toxicity. Clearly, there is potential for more investigation 1994). It is important to note that the wool sheep on
into the anthelmintic properties of the plant. this particular farm have been selected for improved
production and hence, inadvertently, possibly also
Breeding for worm resistance, for more than 15 years.

There are few reports in Malaysia on genetic resistance A newly imported hair breed from Brazil, the Santa Ines,
to parasites. Over a period of 9 months, worm egg was studied for worm resistance purely because there
counts were monitored in weaned lambs of the local were many animals available from which nucleus flocks
long-tail wool sheep and compared with those of the of resistant and susceptible animals could be created.
imported ‘Cameroon’ (Djallonke) hair sheep crosses Selection of this breed, based on field and challenge
(Pandey 1995). This study found that the crossbreeds infections, showed 20–30% resistant individuals.
were more resistant to H. contortus than the local Mating of the resistant individuals produced resistant
wool sheep. However, a later study on the same offspring (Sani et al. 2000).

193
 Biological control
Initial bio-control research in Malaysia used the fungus,
Arthrobotrys oligospora, found in cattle dung, on
Strongyloides papillosus larvae (Chandrawathani
et al. 1998b).
Investigations of the more robust Duddingtonia flagrans,
as a nematophagous inclusion in animal feed are
continuing. Studies of D. flagrans began with a faecal
survey for naturally occurring nematode-trapping fungi
(Chandrawathani et al. 2002a). The fungus was grown
on local media such as wheat grains, padi and millet,
prepared for feeding to small ruminants and also
Goats kept on coastal fringes of eastern Malaysia eat only
incorporated into urea molasses blocks. These two
shrubs and have no worm burdens. (P. Dorny)
delivery methods (feed granule supplement and nutrient
block) were found to be suitable for feeding sheep and
goats. Studies of an isolate of D. flagrans, identified spores/kg, spores tended to reduce pasture
by the Veterinary Research Institute, showed that it contamination, thereby lowering the rate of re-infection
could reduce larval development by nearly 95% of sheep, over a period of 3 months. Untreated controls
in worm-infected animals fed six million spores each had higher faecal egg counts as a result of continuously
(Chandrawathani et al. 2002b). When spores were grazing contaminated pastures. The total worm counts
incorporated into feed blocks, the spores were less of tracers indicated a higher level of larval contamination
effective. Furthermore, how blocks containing fungal in the pastures grazed by the untreated control sheep.
Worm control for small ruminants in Malaysia

spores are stored affects the efficacy of the fungus.

In the final trials on large-scale sheep farms in Infoternak
It is ideal to store them in cold room facilities as this
and Calok, fungal spores were fed at a dose rate
can extend the shelf life of the spores.
of 500,000 spores/kg. Results clearly showed that
Further trials were conducted on penned animals simultaneous use of spores and a 10-paddock, rapid,
artificially infected with H. contortus, using dose rates rotational-grazing strategy was an effective way to
of 125,000 and 250,000 spores per kg as a feed reduce pasture contamination to a minimum, such
supplement, as well as via blocks. The spores were that anthelmintics need not be used. This demonstrates
able to reduce larvae by 80–90% within 48 hours and the ultimate use of nematode-trapping fungi in systems
the effect was seen at least 3–4 days post treatment. for which anthelmintics are ineffective because
In another trial on grazing sheep fed with 500,000 of resistance.

194
Conclusions the medication in the block. This has been clearly
demonstrated by comparing the performance of
The worm profile of small ruminants in Malaysia, and non-medicated and medicated blocks.
the nature of infection in traditional smallholdings, on
Breeding for resistance works well in the hands of
open pastures and under plantation crop management
have been documented. This provides for a sound researchers but as there is no organized breeding
foundation to formulate control programs for worms plan for worm resistance on government farms this
in the various animal management systems. The wide approach to worm control has not been adopted by
availability of the major groups of anthelmintics coupled government breeders and multiplier farms. Selection
with government subsidies for ruminant health has led of breeding animals is based on body weight and
to the emergence of widespread anthelmintic resistance. breed conformation. Sheep breeding farms are now
However, chemical dewormers remain the most used using only hair breeds which were imported because
form of control. Strategic treatment based on faecal egg of their reputation for resistance to worms.
count (FEC) appears to be well adopted on government
Biological control using nematophagous fungi is
and commercial farms. The animal health worker
in the developmental research stage.
monitors the FEC of the farm by sending samples to
the nearest government laboratory. The managers are When animal rearing is a secondary source of income,
advised to treat if 30–40% of the flock has FEC>1500. farmers are less willing to experiment with, or commit
When treating animals it is recommended that drugs to, techniques to improve their husbandry. Smallholder
are rotated (ie, two drugs per year) and that strict farmers usually depend solely on chemical control.
precautions, such as fasting animals before treatment The farmers who succeed in making small ruminants
and calculating dosage based on the heaviest animal, a primary enterprise are those who have invested
be adopted. heavily in their farms and are open to suggestions.
Grazing management using rotational systems based on Entrepreneurial producers use a worm control program.
epidemiological knowledge is a success on government They ensure good sanitation, apply principles of good
farms that use the practice consistently. Rotational nutrition and provide proper housing with raised,
grazing has not been well adopted in plantations slatted flooring. They do this in the name of good
because plantation managers are not convinced of the management rather than consciously thinking of
benefits. Moreover, plantations currently prefer rearing sustainable parasite control. After their considerable
cattle, rather than small ruminants, as cattle appear
investment in the small ruminant enterprise these farmers
to be less problematic and provide better returns.
will adopt other practices instead of depending on
Feed blocks are very popular but their cost is a chemical dewormers. Farmers who face anthelmintic
constraint. Their popularity stems from improved resistance confine their animals and feed them cut-
productivity from increased nutrition, rather than and-carry forages.

195
 The future for work on worm control in small ruminants Chandrawathani, P., Adnan, M., Jamnah, O.
in Malaysia, apart from exploring medicinal plants, is to and Rajamanickam, C. 1996b. The efficacy of
expose farmers to the available options. The continuing netobimin-levamisole against benzimidazole resistant
strains of Haemonchus contortus in goats in Malaysia.
education process of animal health workers who are
Journal of Bioscience 7(1), 83–85.
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overemphasised. Chandrawathani, P., Adnan, M., Maria, J. and Wan Zahari,
M. 1997. The use of medicated urea molasses block
(limited intake) for the control of helminths in sheep.
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11. Worm control for small ruminants in Thailand
S. Kochapakdee and S. Saithanoo

Introduction
Thailand has about 150,000 goats and 43,000 Co Ltd imported a large number of Boer and Saanen
sheep (FAOSTAT 2003). Almost 90% of the total goat goats from South Africa and Australia.
population is found in southern Thailand, mainly in the
This chapter compiles the results of research relevant
five provinces close to the Thai–Malaysian border where
to the control of internal parasites in small ruminants
Thai Muslims are concentrated. In contrast, sheep occur
in Thailand. As little research has been conducted in
across the country. Gastrointestinal parasites increase
mortality in small ruminants, slow growth of young sheep, the chapter focuses on worms in goats and
animals and affect the performance of adult animals. discusses best control options for this species.
They are likely to be a significant constraint to sheep
and goat productivity in Thailand (Kochapakdee et al.
Prevalence of worms
1993a, 1993b, Pralomkarn et al. 1994).
Sheep
There are fewer goats and sheep than large ruminants,
such as cattle and buffalo, and they are less important Only two publications on the prevalence of endoparasites
economically. However, most small ruminants are owned in sheep in Thailand have been located (Sukapasana
by smallholder farmers, and are therefore economically 1987, Churnnanpood et al. 1988). The following
important to the rural people. The government has been endoparasites were found in the faeces of lambs grazing
trying to increase goat numbers in the country by at a research station: Strongyloides papillosus, Cooperia,
providing loans to farmers to buy breeding goats from Haemonchus, Oesophagostomum, Trichostrongylus spp.
government farms. Farmers have formed cooperative and Moniezia benedeni (Sukapasana, 1987). Oocysts of
groups to raise goats to sell as breeding stock to other coccidia were also found. S. papillosus and M. benedeni
farmers. In recent years, goats have attracted the were only found in 20 and 60% of the sampled sheep,
attention of private companies because of the high price respectively. All of the other endoparasites were found
they command at market. In 2000, the CP Hybrid in 100% of samples. Moreover, the first eggs/oocysts

201
 were found in the faeces 3–5 weeks after birth, which spp.), tapeworm (Moniezia spp.) and coccidia (Eimeria
suggests that lambs were ingesting parasite eggs/oocysts spp.) (Suttiyotin 1987, Kochapakdee et al. 1991).
immediately after lambing. However, the degree of infestation of these parasites
should be compared in terms of percentage of infection
Churnnanpood et al. (1988) reported a case
and numbers of eggs per gram of faeces (epg), both
of paramphistomiasis in sheep from 40 herds in
mean and range. Suttiyotin (1988) found that the
Nakomswan Province, central Thailand with morbidity
frequency of animals infected with gastrointestinal
and mortality rates of 50–90%. Sick animals did not
nematodes, coccidia, Strongyloides, Trichuris and
respond to broad-spectrum antibiotics and sulfa drugs,
Moniezia were 92, 83, 55, 11 and 0%, respectively.
or to anthelminthic drugs such as Trodax and Citarin-
Kochapakdee et al. (1991) also found the infection
L. Post-mortem and histological examinations were done
with coccidia (96%), stomach roundworm (95%),
and many immature flukes of Paramphistostomum spp.
Strongyloides (62%), Trichuris (19%) and Moniezia (4%).
were found in the upper part of the small intestine.
Counting the number of eggs (or oocysts) in faeces is
Recently, Chatchawal et al. (unpublished data) reported
a simple way to quantify the degree of infection with
the prevalence of endoparasites in sheep flocks
parasites. In a study by Kochapakdee et al. (1991)
belonging to the Department of Livestock Development
in village goats, the average egg count of stomach
in southern Thailand and found that gastrointestinal
roundworm was 1264, with 33% of sampled animals
parasites, particularly Haemonchus contortus, are
having counts above 1000. The average oocyst count
a major constraint to sheep production in the area.
of coccidia was 2293 and 58% of the animals had
Chatchawan (unpublished data) reported the prevalence counts greater than 1000. The counts for Strongyloides
of worms in female sheep raised at Thepa Livestock eggs were low (295 eggs/g) and 88% of the sampled
Breeding Station in southern Thailand. He found that animals had counts less than 500. The findings
suggest that only stomach roundworm, coccidia and
Worm control for small ruminants in Thailand

in November (season of heavy rain) the average egg

count for Longtail sheep was 2041 while the average Strongyloides are commonly found in goats in Thailand
for Longtail-Barbados crossbred sheep was 1502. and, based on count data, that only stomach roundworms
Moreover, 58.1% of Longtail sheep had egg counts and coccidia may affect the productivity of goats.
greater than 1000, but only 43.1% of Longtail-Barbados Several factors affect prevalence of endoparasite
crossbred sheep had egg counts at that level. in goats, including: season, type of management,
Goats genotype and age of the animals. Suttiyotin (1987)
found that worm egg counts were higher during the
Endoparasites found in goats in Thailand are stomach monsoon months (October–December) than in the dry
roundworms (H. contortus and Trichostrongylus spp.), period. However, Kochapakdee et al. (1993a) did not
threadworm (Strongyloides spp.), whipworm (Trichuris find differences in counts of gastrointestinal nematodes

202
when sampling monthly from October to January but
this was probably due to higher than average rainfall
occurring in January of the year of study.
The type of management system employed affects
the prevalence of endoparasites. Kochapakdee et al.
(1991) found that egg counts for stomach roundworms
were greater for goats raised in fishing villages than for
those raised in rice/rubber villages (1415 vs 1149).
In fishing villages, goats typically graze together in
lowland areas where conditions are well suited to
parasite infestation. In contrast, most goats in rice and
Research in stations, such as the KHK research
rubber villages are raised by tethering, with four to six station pictured here, can provide understanding
per family, so the spread of parasites is low. In another of the epidemiology and production characteristics
study, Kochapakdee et al. (1993b) compared worm of local and imported breeds. (S.Saithanoo)
egg counts of weaned goats raised on two different
research farms belonging to the university. Egg counts
raised under research farm conditions were 491, 1982
were much higher at the farm with wet, tall and dense
and 2320 for Thai-native, 25% Anglo-Nubian cross and
pasture, ideal for larval survival and ingestion, than
50% Anglo-Nubian cross, respectively. Choldumrongkul
at the site with dry and sparse pasture.
et al. (1997) and Pralomkarn et al. (1997) also found
Research suggests that animals may gain some form of that Thai-native kids had much lower egg counts than
immunity to worms as they get older or have a more Anglo-Nubian cross kids suggesting they have some
prolonged exposure to infection. Suttiyotin (1987) form of genetic resistance.
reported that pre-weaned kids had higher egg counts
than weaned ones (370 vs 208). Kochapakdee et al.
(1991) also found that young goats with milk teeth had Effects on production and
higher egg counts than mature goats (1523 vs 1004). blood constituents
Studies of the effect of genotype on egg count had
Kids at Hat Yai farm had higher pre-weaning growth
varying results. No difference in egg count was found
rates and weaning weights than those raised at Klong
between Thai-native goats and Thai-native x Anglo-
Hoi Kong farm (Kochapakdee et al. 1993b). One
Nubian crosses grazing together under village conditions
reason for this difference is the effect of gastrointestinal
(Kochapakdee et al. 1994). However, Kochapakdee
nematodes with egg counts at Klong Hoi Kong farm
et al. (1993b) found that egg counts of weaned goats
being higher than those at Hat Yai farm (3655 vs 117).

203
 The effect of gastrointestinal parasites on the growth
Table 11.1 Least-square means for growth rate
rate of Thai-native and Anglo-Nubian cross goats was
(g/kg0.75/day) of goats with different
studied in a village environment in southern Thailand
anthelmintic treatments and genotypes
(Kochapakdee et al. 1995b). Goats were grazed on
native pasture without supplementation from 0 to 9 weeks Period of study1
and then provided with a concentrate supplement from
0–9 9–18 0–18
9 to 18 weeks. They were also divided into three groups weeks weeks weeks
according to anthelmintic treatment (untreated, 3-week
Treatment
interval treatment or 9-week interval treatment). The
egg count of goats in the untreated group reached 1250 Control 0.4ab 5.4b 2.9b
and remained at this level throughout the experiment. Goats 3-week interval 1.1a 11.5a 6.3a
treated every 3 weeks had higher growth rates than 9-week interval –0.9b 7.9b 3.5b
those in the untreated group or the 9-week-treated
Genotype
group. However, without concentrate supplementation,
treated goats only gained slightly. In contrast, goats Thai-native 3.5b 5.6a 5.6a
grew faster with concentrate supplementation, even the 25% Anglo-Nubian cross 1.1 10.2b 5.6b
untreated ones (Table 11.1). There was no significant 50% Anglo-Nubian cross 0.2 9.0b 4.6b
difference in growth rate among the genotypes during (1) 0–9 week: without concentrate supplement; 9–18 week: with concentrate
the period of no supplementation. However, when fed supplement. (a, b) factors in same row with different superscripts differ
significantly (P<0.05). Source: Kochapakdee et al. (1995b)
a concentrate supplement, the Thai-native goats had
significantly lower growth rate than the 25% Anglo-
Nubian or 50% Anglo-Nubian crosses (Table 11.1). untreated female weaners (Pralornkam et al. 1994) and
Kochapakdee et al. (1993a) and Pralomkarn et al. the average egg count was lower. The lower egg count
Worm control for small ruminants in Thailand

(1994) also found that 50% Anglo-Nubian male may be due to rotational grazing every 4 weeks.
weaners grazed on native pasture without supplement This suggests that, in addition to nutrition, improved
only maintained their weight, while they gained weight management could be a way to control parasite
substantially when supplemented with concentrate. These infestation.
findings suggested that without adequate nutrition,
Four studies investigating the association between
crossbred goats do not outperform the natives and that
parasite infestation and blood constituents in goats have
anthelmintic treatment alone does not result in increased
been conducted in Thailand, one in village conditions
weight gain unless the nutritional status is also improved.
(Kochapakdee et al. 1995) and three under improved
Under improved management, however, no significant management systems (Pralornkarn et al. 1994,
difference was found in the growth rate of treated and Pralornkarn et al. 1997, Choldumrongkul et al. 1997).

204
In a village where goats were continuously grazed in
Table 11.2 Efficacy of anthelmintics used in
one paddock, Kochapakdee et al. (1995b) found that
goats, expressed as faecal egg
after 9 weeks of grazing, the average egg count of
untreated goats was 2289 while the average for goats count percentage
treated with anthelmintics every 3 weeks was only Anthelmintic Study 1a Study 2b Study 3c
46. Packed cell volume and haemoglobin concentration
Albendazole 58.2 88.0 24.8
were lower in the untreated group. These findings
Fenbendazole 54.7 – 25.1
contrast with those from goats rotationally grazed at the
university farm (Pralornkarn et al. 1994) where treated Ivermectin – 93.0 98.9
and untreated goats had similar blood constituent levels. Levamisole – 98.0 94.1
The difference between the two studies is probably due Oxfendazole 63.4 – –
to the severity of infestation with the egg count of the Sources: a Kochapakdee et al. (1993a): b Choldumrongkul et al.
untreated group in the study of Pralornkarn et al. being (1994); c Kochapakdee et al (1995b)

only 600. Under continuous gazing at the university

farm, Choldurnrongkul et al (1997) did not find
differences in blood constituents between treated Kochapakdee et al. (1993a) compared the efficacies
and untreated kids either. of three anthelmintics — fenbendazole, oxfendazole
and albendazole — in a village, using 24 Thai-native
Pralornkarn et al. (1997) found that artificially infected
x Anglo-Nubian cross, weaner bucks. Choldumrongkul
weaner kids had decreased packed cell volume, et al. (1994) reported a study conducted on the university
haemoglobin, total protein and albumin, compared with farm using 24 Thai-native x Anglo-Nubian cross
non-infected goats. This decrease occurred between female weaners which compared the anthelmintics
week 4 and week 9 of infection, which relates to the fenbendazole, albendazole and ivermectin. In another
maturity of the worms. Moreover, weight gain of kids experiment 84 goats raised on the university farm were
in this study was 36–64% lower than in control kids. treated with albendazole, fenbendazole, levamisole
or ivermectin (Kochapakdee et al. 1995). In all three
studies faecal samples were collected from individual
Worm control options animals on day 0 and then once again 2 or 4 weeks
Anthelmintics later: on day 14 (study 2 and 3) and day 28 (study 1).
The efficacies of the anthelmintics were calculated by
Anthelmintics are used extensively to control
faecal egg count reduction test (Table 11.2).
gastrointestinal nematodes in goats, especially on
research/institutional farms. Fenbendazole, albendazole, The lower efficacy of anthelmintics in study 1 may be
ivermectin and levamisole have been used sequentially due to the time of faecal sampling rather than to the
at the Prince of Songkla University farm since 1985. drugs themselves. Anthelmintics had not been used in

205
 the village previously so resistance is not likely to occur. During the course of infection, Thai native goats
Reinfestation of parasites may have occurred by day exhibited less change in blood parameters than
28 and resulted in higher counts. In study 2, all their crosses with Anglo-Nubian goats.
anthelmintics were effective at reducing egg counts.
Choldurnrongkul et al (1997) also found a difference
However, in study three, only ivermectin was highly
in egg count between genotypes: Thai-native kids had
effective and worms showed resistance to albendazole
much lower egg counts than the Anglo-Nubian crosses.
and fenbendazole.
Best-bet options in Thailand
Both the Department of Livestock Development and
Prince of Songkla University agreed that farmers should Based on our experience in Thailand we have
deworm their goats for the first time at the age of proposed eight best-bet options for controlling worms
8–10 weeks. After that, treatment should depend upon in sheep and goats. The best choice for individual
the severity of infestation. If animals are severely infested, farmers will depend upon their objectives in raising
they should be treated again at weaning (aged 3–4 small ruminants and their available resources or the
months). Adult goats should be treated every 2–3 months level of resources they are prepared to invest. The
during the rainy season and every 4–6 months in the proposed methods are listed below.
dry season. 1) Stall feeding: this option has already been adopted
Genetic resistance among farmers who raise goats for live sale, meat
or milk. Many farmers already know the benefits of
There is evidence of genetic variation in resistance to this option and are willing to invest the necessary
helminths between and within breeds (Gray et al. 1995). resources.
Therefore, breeding of animals resistant to internal
parasites is an alternative method, complementary to 2) Stall feeding and tethering: tethering alone, even
when they are moved frequently, cannot supply all
Worm control for small ruminants in Thailand

other methods of control. The effect of trickle infection

with a sheep strain of H. contortus in Thai-native, 25% the nutrients animals need. Therefore, goats should
be provided with extra feed, minerals or supplements
Anglo-Nubian cross and 50% Anglo-Nubian cross
during the night in the form of stall feeding.
was evaluated (Pralomkarn et al. 1997). Thai-native
goats were more resistant to H. contortus in terms of 3) Proper housing: good quality housing with an
parasitological and blood parameters compared with elevated slatted floor is commonly used and farmers
the Anglo-Nubian crosses. This may be due to the appreciate the benefits it provides. The roof and
evolution of Thai native goats in an environment where walls should be designed to protect goats from drafts,
H. contortus is an important parasite. In this study, strong winds and rain. Steps should not be too
a large variation among goats within and between steep or slippery and ideally should have something
genotypes in parasitological variables was observed. to prevent the animals from falling down. Feed and

206
 water troughs should be built so that animals cannot
soil the feed. Some farmers light a fire under the
house to keep it warm. Smoke from the fire can also
repel insects and other external parasites. Fire also
keeps the ground and faeces underneath dry. Mineral
blocks are cheap, easily available and contain all
the minerals which the animals need, so they can
replace salt containers.
4) Shrub/tree leaf supplementation: plants such
as leucaena (Leucaena leucocephala) jackfruit
(Artocarpus heterophyllus) and Streblus asper have
been used as fodder for goats. Many farmers believe
Evaluation of control options under village conditions
that goats that eat grass plus tree leaves grow better
is essential. (S. Saithanoo)
and are healthier than those that eat grass alone.
They believe goats obtain extra nutrients and medical
compounds from the alternative forage. However, 6) Controlled breeding has the following objectives:
fast-growing trees like Gliricidia sepium, Sesbania ■ prevent in-breeding
(S. sesban; S. grandiflora) can also be used as
a buffer for leucaena or in areas unsuitable for ■ prevent mating when breeding animals
growing leucaena. If this option is to be adopted, are not ready
it needs adequate numbers of trees to meet the ■ mate the best males and females
amount of feed that the animals need. Trees also
■ plan on lambing or kidding at times suited
need to be lopped regularly and have fertiliser
to the farmers.
applied to obtain maximum production.
For this option to succeed, good records need
5) By-product supplementation: in southern Thailand,
to be kept and an appropriate method used to
where oil palm is one of the major industries,
keep males and females apart.
by-products, especially palm kernel cake (PKC)
or palm kernel meal (PKM), are a good source 7) Medicated urea mineral molasses blocks: these are
of energy and protein. These can be used as not used in Thailand although urea mineral molasses
feed supplements. blocks have already been used for large ruminants
and therefore could easily be introduced to small
ruminants.

207
 8) Rotational grazing: is one of the best options. References
It not only minimises parasitic infection, but
also enhances pasture utilisation. However, this Anderson, N. 1982. Internal parasites of sheep and goats.
option needs a large area and/or more fencing. In: Coop, L.E., ed., Sheep and Goat Production.
Elsevier Scientific Publishing Company, pp. 175–191.
Smallholder farmers do not seem to adopt it.
Choldumrongkul, S., Kochapakdee, S., Loe, S. and
Puttaragsa, W. 1994. Efficacy of albendazole,
Conclusions levamisole and ivennectin to gastrointestinal nematodes.
Songklanakarin Journal of Science and Technology,
■ Endoparasites found in sheep are Strongyloides
16, 393–397 (in Thai).
papillosas, Cooperia, Haemonchus,
Oesophagostomum, Trichostrongylus spp., Moniezia Choldurnrongkul, S., Lawpetchara, A., Pralomkarn, W. and
benedeni, Paramphistostomum spp. and coccidia. Pandey, V.S. 1997. The prevalence of gastrointestinal
nematodes and the effects of genotype, sex and birth
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impact on production, economic impact or methods pre-weaning kids. Thai Journal of Agricultural Science,
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■ Most published results on endoparasites in goats Chumnanpood, P., Warahatsawapati, W., Numtoom,
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Worm control for small ruminants in Thailand

Ruminant. ACIAR, Canberra, Australia, pp. 206–212.

■ There is evidence of nematode resistance to
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S., Saithanoo, S. and Norton, B. W.1991. Prevalence
■ A study under village conditions showed that of internal parasite in Thai native female goats. In:
anthelmintic treatment alone did not improve Saithanoo, S. and Norton, B. W. ed., Goat Production
performance of crossbred goats unless the in the Asian Humid Tropics. Proceedings of the seminar
nutritional status was also improved. held on 28–31 May 1991 in Hat Yai, Thailand,
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■ One study suggests that Thai native goats are
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Anglo-Nubian crosses. Pralornkarn, W. 1993a. The effects of internal parasites
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Rahman, W.A. and Collins, G.H. 1991. Change
Kochapakdee, S., Choldumrongkul, S., Saithanoo, in liveweight gain and blood constituents in
S. and Pralomkarn, W. 1993b. Prevalence of experimental infection of goats with goats-derived
gastrointestinal nematodes and Eimeria spp. in compared with a sheep-derived strain of Haemonchus
weaned goats. Songklanakarin Journal of Science contortus. Veterinary Parasitology, 38, 145–150.
and Technology, 15, 23–29 (in Thai).
Saithanoo, S. 1990. Breeding Systems for Village Goat
Kochapakdee, S., Pandey, V.S., Pralomkam, W., Production in Southern Thailand. Ph.D. Thesis, The
Choldumrongkul, S., Ngarnpongsai, W. and University of Queensland, Brisbane, Australia, 179 pp.
Lawpetchara, 1995a. Anthelmintic resistance
Saithanoo, S., Cheva-Isarakul, B. and
in goats in southern Thailand. Veterinary Record,
Pichaironarongsongkrarn. K. 1991. Goats production
137, 124–125.
in Thailand. In: Saithanoo, S. and Norton, B. W.,
Kochapakdee, S., Pralomkam, W ., Choldumrongkul, S. ed., Goat Production in the Asian Humid Tropics.
and Saithanoo, S. 1995b. Change in live-weight gain, Proceedings of the seminar held on 28–31
blood constituents and worm egg counts in Thai native May 1991 in Hat Yai, Thailand, pp. 30–39.
and crossbred goats raised in village environments in
Saithanoo, S., Kochapakdee, S. and Pralornkam,
southern Thailand. Asian-Australasian Journal of Animal
W. 1992. Productivity of goats under village
Science, 8, 241–247.
environments in southern Thailand: preliminary report.
Pralomkarn, W ., Kochapakdee, S., Choldumrongkul, S. In: Reodecha, C., Sangdid, S. and Bunyavejchewin,
and Saithanoo, S. 1994. Effect of supplementation and P. ed., Proceedings of the Sixth AAAP Animal Science
parasitic infection on productivity of Thai native and Congress held on 23–28 November 1992 in
crossbred female weaner goats. I. growth, parasite Bangkok, Thailand, Vol. 3, p. 173.
infection and blood constituents. Asian-Australasian
Suttiyotin, P. 1987. A survey of internal parasites
Journal of Animal Science, 7, 547–554.
of native goats in Songkla. Sonklanakarin Journal
Pralomkarn, W., Pandey, V.S., Ngampongsai, W., of Science and Technology, 9, 7–18 (in Thai).
Choldumrongkul, S., Saithanoo, S., Rattanachon,
Sukapasana, W. 1987. Variation in the number of
L. and Verhulst, A. 1997. Genetic resistance of three
worm eggs in the feces of lambs. Proceeding of
genotypes of goats to experimental infection with
the 6th Annual Livestock Conference, 18–20 May
Haemonchus contortus. Veterinary Parasitology, 38,
1987, Bangkok, Thailand, pp. 77–83 (in Thai).
79–90.

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12. Goat production, parasites and testing of
control options in Lao, Cambodia and Vietnam
R.A. Sani, Dinh Van Binh, Nguyen Duy Ly, Sorn San and Viengsavanh Phimphachanhvongsod

Introduction
There is very little documentation on small ruminants in farmer in Lao, Cambodia and Vietnam respectively.
Lao, Cambodia and Vietnam. This chapter comprises There is constant demand for goats at relatively stable
information available from annual reports of these prices. The price for goat and sheep in liveweight is
three countries which were produced according to the higher than for pigs and cattle. Goat rearing requires a
objectives of the IFAD TAG 443 project. The information low labour input compared to cropping. Hence, many
from Lao is basically on goat production, its constraints, poor families show interest in participating in goat projects
technical training needs and ongoing research. because they have available labour, the necessary
Cambodia had conducted a survey of goat distribution feed resources and it is easy to develop as part of
and prevalence of parasites as well as a series of trials the traditional farming system. Goat production has a
to study the effect of nutrition on parasitism. Vietnam significant impact on farmer households and so goats
tested several technologies for worm control at the farmer can be a first step out of poverty.
level and assessed the impact. This chapter is devoted
to describing the goat situation in these three countries
as well as the related research that was conducted. Health problems
Diseases were the main cause of small animal mortality
but the diseases were not identified in Lao. However,
Goat production
goat owners complained of footrot, orf (facial eczema)
The population of small ruminants in Lao, Cambodia and and worms in their stock. A survey conducted in six
Vietnam is 150 000, 5000 and 550 000 respectively, villages in Luang Prabang province indicated that the
comprising almost exclusively meat-type goats. The goat highest mortality of goats was in two upland villages
population in Cambodia was estimated very recently with an average of 2.0–2.5 head per household
but the figure is likely to be only 60% of the actual annually. Goat mortality also appeared in two villages
population. Goats are mainly kept by village farmers in the mountainous agroecosystem with an average
with 3–10 head, 10–49 head and 6–20 head per of 1.5–2.0 head per household annually. There was

211
 no goat mortality reported in the lowland. There are Cambodia and Vietnam identified the internal parasites
no reports on epidemiological studies of nematode commonly found in goats (Table 12.1). The worms are
infections in goats in Lao. listed according to importance.
Foot and Mouth Disease (FMD) was the most reported
disease in goats in Cambodia. There is no vaccination Technology options tested
available for FMD. Farmers also reported deaths of goats
but the causes were not known as there is no diagnostic in Cambodia
facility in the provinces. Farmers report diarrhoea and Three trials were conducted at the University of Tropical
skinny goats which may be linked to parasitic diseases. Agriculture attached to the Royal University of Agriculture
The common complaints or constraints in rearing goats in Phnom Penh as follows:
were skinny goats and not enough feed which, again,
Goat production, parasites and testing of control options in Lao, Cambodia and Vietnam

■ Effect of cassava foliage, legume foliage, banana

may be linked to parasitic diseases and poor nutrition.
leaves or grass on growth and nematode
Flock productivity data from village production systems infestation in goats fed a high protein diet
in Vietnam indicated that mortality rate of kids and
■ Effect of cassava foliage or grass on growth and
immature goats was 35–45% and of adults was 8.5%.
nematode infestation in goats fed a high protein diet
Although the exact contribution of roundworm parasitism
to annual flock mortality is unknown, it was estimated ■ Effect of cassava foliage or grass on growth and
that about 15% adult mortality and 51% kid mortality nematode infestation in goats fed a low protein diet
were closely related to gastrointestinal parasitism. The goats in all three trials were confined individually
in raised floor wooden pens with slatted floors. Water
Table 12.1 Identified internal parasites of goats was always available.
in Cambodia and Vietnam In Trial 1, the basal diet was fresh brewer’s grains (high
Cambodia Vietnam
protein) offered at 20% above observed intakes and
supplemented with the foliages fed at approximately
Haemonchus contortus Haemonchus contortus 10% (fresh basis) of the liveweight of the Bach Thao
Trichostrongylus spp. Fasciola sp. goats. Foliage from cassava supported the highest
Fasciola sp. Trichostrongylus growth rate in the goats and the lowest faecal worm
Oesophagostomum spp. Moniezia spp. egg counts. Worm egg counts were highest in goats
fed the natural grasses and growth rates were 30%
Strongyloides papillosus Nematodirus sp.
lower compared to cassava. Very low growth rates were
Oesophagostomum spp.
observed when the legume, Flemingia, was fed. It was
Ostertagia sp. concluded that cassava has a high potential as a
protein-rich feed for goats kept in confinement.

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In Trial 2, a basal diet of fresh brewer’s grains at a
restricted level of 50% of the expected ad libitum intake
was provided to Bach Thao goats. The supplements
were foliage from cassava, cut natural grasses or a
mixture of the two on a 50:50 basis given ad libitum.
The feeds were offered twice a day. All animals were
treated with ivermectin before starting the experiment.
With foliage supplementations using cassava only,
cassava + grass, and grass only, the average daily
weight gains were 91.7g/day, 115 g/day and 80
g/day respectively and faecal egg counts were 67,
63 and 466 epg. The high growth rates and good
feed conversion in this trial probably relate to the breed
and higher protein content of the diet. The lower egg
counts in goats supplemented with cassava suggest
there is a possible direct anthelmintic effect on parasites,
or an indirect effect though additional protein or
condensed tannins in cassava.
In Trial 3, native goats were fed a basal diet of wheat
bran (low protein) supplemented with foliage from
cassava, cut natural grasses or a mixture of the two on
a 50:50 basis given ad libitum. The animals were not
Banana stems are a good feed resource but require
dewormed except for a fourth group given grass alone,
family labour. (G.D. Gray)
which was dewormed with ivermectin. The average
daily gains were modest, mainly because the goats
were slow to adapt to the cassava foliage. Worm On-farm technology testing
egg counts declined steadily from initial high values
in the cassava groups. However, egg counts in the in Vietnam
grass group remained low throughout the experiment. In Vietnam, the process of selecting technologies to be
Considering the results of the three experiments, it would tested was to fully discuss all available options with
appear that cassava foliage could contain compounds farmer groups and, once agreed, the farmers took part
— possibly condensed tannins — that are useful in in trials which were designed and run by the project
preventing parasitism in goats. team with the farmers fully cooperating and benefiting

213
 from the results. The researchers led the process and Improved nutrition. This control option was selected
provided the technical and, in some cases, financial to study the effect of improved nutrition on the worm
support. This process has resulted in some very burden of growing goats. Six three-month-old weaner
promising and practical options which are being goats each on 10 farms were fed with foliage and
carried forward to participatory farmer evaluation. given concentrates at 1% bodyweight. The concentrates
were given twice a day; in the morning before grazing
Grazing compared to confinement. These two systems
and in the afternoon after grazing. After 5 months
of managing goats were compared to study the effect
they attained an average daily bodyweight gain of
of confining goats in order to prevent access to worm
62 g/day compared to the unsupplemented goats
larval stages. All goats were treated with an anthelmintic
at 33 g/day, an improvement of over 87%. Although
at the beginning of the trial; one group of goats grazed
there was no significant difference in FEC between the
freely without supplementation and the other group was
two groups of animals, during the trial period the FEC
Goat production, parasites and testing of control options in Lao, Cambodia and Vietnam

confined and fed foliages. At the end of the 4-month

in the control goats was 10–27% higher compared to
trial period the average daily weight gain of the confined the FEC of supplemented goats. Farmers understand that
goats was 10 g more and the FEC was 40–60% less improved nutrition increases animal productivity and
than their grazing cohorts. Although the results of the health. However, this requires investing in feeds and
trial appeared promising, the farmers considered that building of sheds. Some farmers have applied this
confining goats was too tedious as it meant having to option especially in dairy weaner goats to increase
cut grass or foliage. They prefer goats to graze, which bodyweight before selling.
minimises labour.
Sanitation. In Vietnam bad hygiene is common in
Biological control. This option of worm control used traditional animal management. It is closely related to the
two approaches; one was to use ducks to kill snails, transmission of disease and parasites. This procedure
which are an intermediate host of trematodes, and aimed to show farmers the benefits of good hygiene
the other was the mechanical dragging of soil to kill practices. On nine goat farms manure was disposed
pasture mites which serve as intermediate hosts of of daily and clean water provided while another nine
cestodes. Using ducks to kill snails reduced Fasciola farms maintained their traditional management. All goats
infections by 60%. When goats were raised on farms were dewormed before the start of the trial. During the
which turned over their soil the incidence of cestode trial period of 6 months the FEC on the `clean’ farms
infection was lessened by 57% compared to the was 20% lower than on the farms not practising good
farms which did not practise soil turnover. This option sanitation. Differences in the first 3 months of the trial
was found to be suitable for the farmers in Vietnam were much higher suggesting that the sanitation had
because it also improves crop cultivation. delayed the re-infection of the animals. Bodyweight
gains of the goats over the trial period were also 20%
higher on the `clean’ farms (60 g/day) compared to

214
those in the traditional system (50 g/day). This study
clearly demonstrated that good sanitation and the
provision of clean drinking water reduced infections
with worms and increased weight gains in goats
under village conditions.
Improving on-farm hygiene as a measure to control
internal parasites is simple to apply and maintain and
will probably be adopted easily by farmers. Farmers
see the benefits — diarrhoea decreases, weight gain
increases and there is organic fertiliser for crops.
Chemical deworming. Farmers in Vietnam do not
often use chemical drenching. The purpose of this trial
was to study the efficacy and impact of conventional
dewormers. The following efficacies against nematodes
were found: levamisole, 80–92%; mebendazole and
fenbendazole, 70–80%; and ivermectin, 75%. These
results are a combination of results from 50 goats on Formal training courses for extension students build
five village farms and 50 goats from the Goat and capacity among agriculture graduates. (Dinh Van Binh)
Rabbit Research Center (GRRC). When goats were kept
on farms practising good hygiene and with sufficient
Breeding management. Good bucks were provided to
nutrition, deworming could be done at 7–9 month
farmers to improve breeding on the focus farms. Farmers
intervals; 50% of such goats had FECs of 0–1250 were informed of the negative effects of inbreeding
epg and diarrhoea was not frequently sighted, while and introduced to animal management and controlled
42% of goats kept in the traditional system had FEC breeding. For this, they needed to build housing.
of 1000–2500 epg. Farmers were supplied 30% of the total value of a
Farmers in the trial obtained knowledge about chemical buck, while very poor farmers were supplied 100%.
dewormers and on how and when to deworm. Where After 2 years, bucks were transferred to other farms.
anthelmintics were provided to four sites to control From 5 months onwards, all male kids were managed
parasites; goat production increased by about 15–20%. and grazed in separate areas.
The technical team was also educated on the sensible After 2 years the results of using improved goat
use of anthelminthics and warned that frequent use of breeding showed in increased production.
chemicals can lead to drug-resistant parasites.

215
 Medicinal plants. Initial results indicated that mimosa, on their farms. Farmers selected options to suit their
papaya and leucaena have detrimental effects on situation. To evaluate the impact of the various options,
larvae of Haemonchus in vitro. Some plants used participatory assessment was done with focus and other
in the treatment of diseased animals were identified farmers in villages with the participation of extension
to contain anti-parasitic activity. officers to compare between the new and old (traditional)
systems. After 1 year, results are good (Table 12.2).
This option is easily available to control parasites,
On these farms mortality was reduced by 51%,
especially in rural areas. However more research
production increased by about 69% and there was an
is needed.
income benefit of 56% (Table 12.3). In the new system
42% of goats had low FEC of ≤500 epg and 58% had
Applying technology options on farm medium to high FEC of 500 to > 3000 epg while in
the old system only 11% of goats had low FEC and
Goat production, parasites and testing of control options in Lao, Cambodia and Vietnam

After testing and evaluating technology options for 89% had medium to high FEC. Therefore, in the new
control of gastrointestinal parasites on farms, best bet system 35% fewer goats had medium to high FEC.
options were packaged by discussion and ranking with Other non-participating farmers are beginning to
participant farmers. Meetings with farmers were held show interest in applying these new technologies on
in the villages to introduce technology options for their farms to improve production and reap benefits.
controlling parasites that farmers could select to apply

Table 12.2 Results of goat production in Vietnam

Old system New system Change

Parameters (125 goat farms) (80 goat farms) (%)

Number of goats (head/farm) 13 22 69

Mortality (%) 35 17 -51
Diseases (Diarrhoea) (%) 24 10 -58
Weight gain (g/day) 37.5 46.3 23.5
Goats with FEC of 500–>3000 epg (%) 89 58 35
Level of infection (epg) 2270 1560 -32
Sanitation (%) 10 100 900
Supplement concentrate (%) 10 100 900
Supply clean water (%) 5 35 600
Deworming (%) 10 100 900
Breeding management (%) 6 75 1150

216
 Table 12.3 Results of socio-economic change

Old system New system

Parameters (125 goat farms) (80 goat farms)

Income (average/person/year, million VND) 2.55 3.99

Knowledge of goat husbandry (%) 30 100
Knowledge of goat health (%) 20 100
Innovative farmers (%) 20 60
Attitude change (%) 20 60
Change of habit (%) — 60
Note: Income was measured by identifying total income (from cultivation, husbandry and other sources) and dividing by the total number of people in the household.

Constraints in goat production Training needs

There were four main constraints according to farmers A workshop was conducted as part of the TAG 443
who responded to a survey in Lao and these were project entitled `Goat Production and Management
similar to constraints identified from discussions held in Lao PDR’ and held on 16–20 December 2002 for
with farmers in Cambodia, which were: 24 technical and extension livestock officers from four
■ Lack of knowledge about goat husbandry, provinces in Lao. Comments and suggestions from the
health and sanitation — the problems identified workshop participants for further training were:
were internal and external parasites, ignorance ■ practical sessions on feed formulation, faecal egg
of deworming practices and not recognising counts, slaughtering, GoatFlock computer model,
disease symptoms making silage and mineral blocks
■ Lack of feed — a shortage of animal feed during ■ information on animal drugs (including antibiotics),
the dry season while available crop residues, fodder the use of herbal medicines and traditional
trees or pasture grasses as part of the livestock treatments for animal health
system were underutilised
■ techniques on goat breeding, mating and A.I.
■ Lack of extension capability — to promote
improved animal nutrition and husbandry ■ improved extension and communication
techniques with farmers
■ Lack of capital — access to credit by smallholders
was generally difficult and expensive

217
 ■ information about integration of goats and crops The 80 goat farms in the new system are from the
initial 125 farms investigated. They were monitored
■ information and discussion on investment for goat
production, cost-benefit and goat marketing for 1 year applying different technology options.
Data were compared using percentage change
■ a specific training workshop on livestock research between the two systems. Gastrointestinal parasite
infection was animals with worm eggs present.
Goat production, parasites and testing of control options in Lao, Cambodia and Vietnam

218
13. Worm control for small ruminants in Fiji
P. Manueli

Introduction
This chapter brings together the results of small ruminant
worm control research in Fiji. Where the results have Table 13.1 The important parasites of small
not been published in the scientific literature, an attempt ruminants in Fiji
is made to provide as much information as possible on Frequency
the research trials. If the research has been previously Species Site observationa
published, only a brief description is provided. It is +++
Haemonchus contortus Abomasum
hoped that the information will be useful in the design
Trichostrongylus axei Abomasum +++
of best-bet worm control options and that, through the
sharing of these results, costly duplication of research Trichostrongylus colubriformis Small intestine +++
activities can be avoided. Strongyloides papillosus Small intestine +++

Moniezia expansa Small intestine +++

Gastrointestinal parasites have been a constraint to small
ruminant production in Fiji ever since small ruminants Oesophagostomum Large intestine ++
were introduced into the country in the 1850s. It is columbianum
of interest that much of the early literature on livestock Trichuris spp. Large intestine +
production in Fiji does not mention worms as a constraint *
Haemonchus similis Abomasum
to goat production. It is thought this is because goats *
Haemonchus placei Abomasum
tended to be reared in small herds under close
Mecistocirrus digitatus Abomasum *
supervision. However, early attempts at sheep farming in
Fiji were modeled on the extensive systems of Australia a +, Occasional; ++, Common; +++, Very Common; * Present in cattle

and New Zealand with the aim of producing wool for and potentially infectious

export and mutton for local consumption. Under this

management system worms were found to be a major
constraint to the establishment of a local sheep industry.
Table 13.1 contains a list of the important parasites of
small ruminants found in Fiji.
219
 Importance of gastrointestinal of the small ruminant industries in Fiji. During the survey
the farmers identified three dimensions of the worm
parasites problem that need to be addressed. These were:
Despeissis (1922) in a paper in the Agricultural Circular ■ availability of anthelmintics
entitled ‘Sheep in Fiji’ stated that: ‘Of all pests, worms
■ cost of anthelmintics
are probably the most serious’. This view was supported
by Turbett (1929) who wrote: ‘Worm infestation ■ effect of worms on production.
probably causes a greater loss than is recognised as,
These areas will now form the basis for worm control
where the inspection of flocks and pastures is not carried
research and extension initiatives by the Division of
out regularly, sheep which die are not missed until the
Animal Health and Production.
counting of the flock at the general muster…’. By 1940
(Turbett 1940) it was apparent that of all reasons given
for the failure of the sheep industry in Fiji to prosper: Early research into worm
… infestation with worm parasites was the epidemiology and control
most important.
The first documented report of research into helminth
This view is still current today and it is generally control in Fiji is that of Baker (1970). This report
acknowledged that worms comprise the major animal documents 5 years of research work carried out from
health problem limiting small ruminant production in 1965 to 1969 on the newly established Government
Fiji (Walkden-Brown and Banks 1986, Manueli 1996) Sheep Farm at Nawaicoba. Trials into gastrointestinal
with Haemonchus contortus and Trichostrongylus parasitism during this period include a comparison of
colubriformis being the most common. Effects of worms locally available anthelmintics and the use of a rotational
on small ruminant production include stock mortalities, grazing system.
reduced animal productivity and increased production
Worm control for small ruminants in Fiji

A study was conducted comparing the effects of the

costs from preventative treatments.
anthelmintics phenothiazine, thiobendazole and minitic
The development of anthelmintic resistance in some on growth rates of yearling sheep transferred to the
small ruminant herds and flocks in Fiji (Banks et al. Animal Quarantine Station on the wet side of the island.
1987) has made the importance of the development Lamb liveweight gains did not increase greatly after
of sustainable parasite control methods imperative treatment with any of the specified drugs nor was there
for the survival of small ruminant industries in Fiji. any retardation in weight gain in animals in the period
A recent participatory survey of 34 progressive small before the next anthelmintic treatment. No information
is available on the total worm burdens or faecal egg
ruminant farmers (Manueli unpublished data) indicated
counts of animals in the trial although it is reported
that worms remain a major constraint to the expansion

220
that larvae of all of the normal species of bowel worms
were cultured and that eggs of Dicrocoelium dendriticum
were seen in one faeces sample. The results of the trial
indicated that worms were not a major problem with
yearling stock in the wet zone.
The development of a rotational grazing system was also
studied during this period. Unfortunately there is little
available information on the design of the trials and
no parasitologcal data are presented in the report.
The results of the research indicated that the adoption
of a system of grazing paddocks for 4 days followed
by a 28-day spell was effective for controlling parasites
in adult stock, and that only two to three drenches Soil erosion from overgrazing can be prevented by
a year are needed to maintain health. providing supplementary forages in the dry season.
(ACIAR)
At the conclusion of the research program
recommendations on parasite control made
to farmers were to: stocked drenched (SD), rotationally grazed undrenched
(RU) and rotationally grazed drenched (RD). The mean
■ rotationally graze all stock as far as possible liveweights of the RD and SD groups were found to be
given economic constraints on building fences higher at the completion of the trial than those of the
■ drench adult stock as necessary and definitely SU and RU groups. Egg counts of all groups were
once before the start of the wet season, once recorded at 4-weekly intervals. Egg counts of the SU
during the wet season and once again after and RU groups were higher than those of the RD and
the wet season SD groups at all stages of the trial, and eggs were
recovered from the faeces of animals in SU and RU
■ drench growing stock fortnightly during the wet
season and monthly during the dry season groups more frequently than in the SD and RD groups.
Some sheep in the undrenched groups needed to be
■ alternate anthelmintics used for successive drenches. drenched three or four times during the trial to prevent
Singh et al. (1972) compared suppressive fortnightly deaths. From these results Singh et al. (1972) concluded
anthelmintic treatment as recommended by Baker (1970) that helminth control was absolutely necessary for sheep
for growing stock with a 30-day rotational grazing rearing in Fiji, that it would be feasible to drench animals
system using five paddocks. The 9-month trial used less frequently than fortnightly, and that rotation with a
four groups of animals: set stocked undrenched (SU), set 4-weekly resting period was useless.

221
 With the initiation of a series of ACIAR-funded drug to which no parasite resistance was found with
collaborative research programs between the Ministry 54% of the farms carrying strains of parasites resistant
of Agriculture (Fiji) and CSIRO (Australia) in 1984 the to either fenbendazole, levamisole or a combination of
level of parasitology research in Fiji increased. The series both levamisole and fenbendazole (Banks et al. 1987).
of four projects, starting in1984, covered a wide range
Seasonal fluctuations of larvae on pasture
of topics and were titled as follows:
The research trial investigated the survival and
■ ACIAR PN8418: The epidemiology and control
seasonal pattern of egg hatching of H. contortus and
of gastrointestinal nematodes of small ruminants
T. colubriformis on pasture at two sites, wet zone and
in the Pacific Islands
dry zone (Banks et al. 1990). Each month, a separate
■ ACIAR PN8913: Ecological and host-genetic pasture plot at each site was contaminated at weekly
control of internal parasites of small ruminants intervals with H. contortus and T. colubriformis eggs.
in the Pacific Islands The plots were sampled at regular intervals and the
infective larvae identified and counted.
■ ACIAR PN8523: Self-medication of ruminants
in tethered husbandry systems Infective larvae numbers on pasture were highest
7 days after the last contamination and there was
■ ACIAR PN9132: Nutritional and chemotherapeutic
considerable seasonal variation in the survival of larvae
strategies for sustainable control of gastrointestinal
on pastures. In the wet zone, survival was shorter in the
parasites of ruminants
wet season (5–9 weeks) than the dry season (13–17
weeks). Larval survival on the dry zone plots was found
ACIAR PN8418: The epidemiology to be much more variable. T. colubriformis larvae were
found on pasture in all months except the 2 driest
and control of gastrointestinal (August and September). The survival of H. contortus
nematodes of small ruminants larvae on pasture appeared to be more sporadic
Worm control for small ruminants in Fiji

possibly in response to changes in available moisture.

in the Pacific Islands
Effect of season on egg hatching on pasture
Survey for anthelmintic resistance
The development of worm eggs and larvae on pasture
Twenty-four herds were surveyed for anthelmintic was investigated. Pasture plots were contaminated with
resistance. Management practices varied from tethering known numbers of parasite eggs in the faecal pellets of
through uncontrolled grazing to fenced commercial farms. naturally infected does. Recovery of eggs and larvae
A random selection of 40 goats or sheep on each from faecal pellets on pasture at 12-hour intervals was
farm were used to evaluate the effects of anthelmintic carried out in July, October, January and April.
treatment on faecal egg counts. Ivermectin was the only

222
By 72 hours after exposure to parasites 97% of eggs
had developed to the first larval stage, with the first
third-stage larvae (L3) appearing by 96 hours after
contamination. Development to the L3 stage appeared
to occur faster in January and April (96 h) than in July and
October (144 and 108 h respectively) (ACIAR, 1990a).
Natural history of trichostrongylidosis in goats
The experiment investigated seasonal patterns of
worm burdens and the effects of physiological status
in grazing goats in the wet and dry zones of Fiji over
a 12-month period. Groups of 20 does were set
stocked on paddocks in the dry (five does/acre) and
wet (10 does/acre) zones of Fiji and drenched at 6
and 4-weekly intervals, respectively, to maintain health.
Every 2 months, four young worm-free tracer animals
were introduced to the herds for 2 months and then
slaughtered. In May and June worm-free dry (four) and
lactating (four) does were introduced into the herds for
In larger sheds, pregnant, non-pregnant and young
2 months and also slaughtered.
animals can be fed separately. (ACIAR)
H. contortus and T. colubriformis were the dominant
parasite species but Oesophagostomum columbianum counts between lactating and dry does were small,
and Taenia ovis were also sometimes found. Tracers which was indicative of an absence of immunity.
became infected throughout the year although worm There was no evidence of arrested development in
burdens were higher in the wet zone. Mean worm H. contortus indicating that development to adult
counts varied considerably from month to month at stages occurred throughout the year (ACIAR 1994).
both sites and no reliable pattern of infection was
detected, although it appeared that H. contortus and Simulation model of parasites on pasture
T. colubriformis burdens were highest during the cool Data collected from epidemiological studies was used
months (July and August) in the dry zone. Worm counts to develop a simulation model of parasites on pasture.
of mature dry does appeared to be similar to those of Development of the simulation model was then continued
young growing animals indicating that there was little in a following project, ACIAR 8913 (ACIAR 1988).
development of age resistance. Differences in worm

223
 Testing potential worm control measures Testing potential worm control measures
in goats — Phase 1 in goats — Phase 2
Trials were carried out in the wet and dry zones The following three treatment regimes were compared
to compare the following three treatment regimes: in the wet and dry zones:
1. NORM — normal control measures of 4-weekly 1. NORM — as above
(wet zone) and 6-weekly (dry zone) drenching
2. RRG — rapid rotational grazing of eight paddocks
in set-stocked goats
with animals grazing a paddock for 4 days before
2. RG — rotational grazing where animals grazed resting the paddock for 28 days
a paddock for a period (4 weeks in the wet zone,
3. SD — as above.
6 weeks in the dry zone) before being drenched
and moved to a second paddock while the first was Individual animals in NORM and RRG groups were
spelled for an equivalent period of time drenched when their egg counts exceeded 1000 epg.

3. SD — strategic drenching using 6 fortnightly In the wet zone, egg counts of NORM animals
drenches of ivermectin, with a dose of closantel exceeded 1000 epg three and five times, respectively,
administered with the last dose of ivermectin. in the two replicates. In the dry zone animals in the
NORM replicates required 10 and seven drenches,
In the wet zone, faecal egg counts and larval cultures respectively. Egg counts of SD animals remained low
showed no differences between the RG and NORM until 25 weeks after the start of the trial (13 weeks after
treatments with larval cultures indicating that H. contortus the last closantel dose). They then rose to levels similar
and T. colubriformis were present. Egg counts of the to those in the NORM group. Animals in the RRG group
SD animals were low (but never falling to zero) during needed less frequent drenching than the NORM animals
the drenching period, and increased as soon as with replicates in the dry zone needing four and six
drenching had ceased, necessitating the termination treatments, and replicates in the wet zone needing
Worm control for small ruminants in Fiji

of the SD treatment 7 months later. In the dry zone both two and nil treatments, respectively (ACIAR 1990a).
the NORM and RG treatments had low egg counts
Sustained release capsules for worm control
over the duration of the trial and this may have been
due to low levels of pasture contamination resulting Goats
from the drought before the start of the experiment. Two groups of 10 does were grazed on pastures naturally
There were no differences between either the NORM infected with H. contortus and T. colubriformis. Five does
and RG treatments in egg counts, although liveweight in one group received ewe-strength albendazole capsules
gains were slightly lower in the RG group (ACIAR 1988). containing 3.85 g of albendazole (ET) and five were
maintained as controls (EC). Five does in the second

224
group received lamb strength capsules containing 2.1 g
of albendazole (LT) and five does were maintained
as controls (LC). The capsules were designed to release
the anthelmintic over 3 months. Forty-eight hours after
capsules were inserted all does were drenched with
a double dose of ivermectin (400 ug/kg) to remove
adult worms.
The use of both lamb and ewe albendazole capsules
appeared to delay the establishment of patent infections
by 2 weeks in comparison to controls, however, after
6 weeks the egg counts of treated animals were
equal to or greater than those of control animals.
The experiment was terminated after 8 weeks as
The gums of sheep and goats made anaemic by
the capsules were clearly unsuitable for use in goats
Haemonchus are pale and can be examined quickly.
(ACIAR 1988).
(ACIAR)
Sheep
Forty ewe hoggets naturally infected with H. contortus lambs and hoggets monthly, and dry ewes only when
and T. colubriformis were drenched with ivermectin and they had signs of infection. After a year, only 19 of the
allocated to one of two paddocks. One group of 600 ewes had required anthelmintic treatment over
20 ewes received ewe strength albendazole capsules and above the treatments allocated to lactating ewes
containing 3.83 g of albendazole (ET). The other group (ACIAR 1990a).
acted as a control and was drenched every 8 weeks.
Transmission and identification of Mecistocirrus
The albendazole capsules totally suppressed the
digitatus in goats
production of parasite eggs in the faeces of treated
animals for 120 days. This suppression occurred in Mecistocirrus digitatus had previously been identified
spite of the fact that capsules used were ‘90 day’ in cattle in Fiji but not in goats. Eggs were recovered
(ACIAR 1990). from female worms from the abomasum of cattle at
slaughter and incubated for 8 days in a sterile culture
Minimal drenching program for sheep
medium. Infective larvae were recovered and used to
The entire sheep flock at the Nawaicoba Station was infect two goats (200 larvae/goat). The M. digitatus
converted to a minimal drenching program. This involved larvae exhibited only a low ability to establish in goats
drenching lactating ewes three times during lactation, (ACIAR 1990).

225
 Night yard trials in goats ewes had since dried off) leaving the group composition
at 20 dry ewes and 20 weaners. Faecal egg counts
Sixty mature does were drenched with a double dose
were monitored.
of ivermectin (400 ug/kg) at the beginning of the dry
season and allocated to one of two treatment groups: At slaughter, total worm counts for weaners differed
night yarding (N) or shedding at night (S). The animals significantly from those of dry ewes. Egg counts
grazed the same pastures but were separated at night of weaners gradually decreased over time. At the
when they were either locked in a shed (S) or a night termination of the experiment weaner egg counts had
yard (N). Does in both groups had similar worm burdens, not yet fallen to the same levels as those of the ewes.
despite the fact that infective larvae numbers were By this time weaners were 14-months old indicating that
age resistance had not yet developed (ACIAR 1990a).
much higher in the night yard than in the pasture ones
(ACIAR 1988).
Faecal egg count heritability pilot study ACIAR PN 8913: Ecological and
A pilot study was done to estimate the heritability of host-genetic control of internal
faecal egg count in goats. Blood and faecal samples parasites of small ruminants
were taken from 129 kids, 3–4 months old and sired
by six bucks on a government goat station, 6 weeks in the Pacific Islands
after they had been drenched with ivermectin. Project 8913 was designed to build on the results of
Significant effects of sire were seen on egg counts the epidemiological studies of ACIAR project 8418.
and haemoglobin, but not packed cell volume. In addition, the project investigated the heritability of
The heritability of egg count was estimated at 0.45. faecal egg count in goat and sheep populations in
Investigations into the heritability of faecal egg count Fiji to examine the feasibility of breeding for parasite
were continued in ACIAR Project 8913 (ACIAR 1988). resistance.
Worm control for small ruminants in Fiji

Age resistance of sheep to internal parasites Pharmacokinetics of albendazole in small ruminants

Twenty weaner lambs, 20 dry ewes and 20 lactating Six goats and six sheep were maintained under
ewes were drenched with ivermectin and grazed controlled conditions and fed a complete ration for
together on a 15 ha paddock naturally infected a period of 2 weeks. Each animal received a single
with H. contortus and T. colubriformis. Ten dry ewes, intra-ruminal dose of 7.5 mg/kg albendazole directly
10 wet ewes and 10 weaners were slaughtered after into the rumen and 10 ml blood samples were collected
2 months to obtain worm counts. After slaughter, 10 at 0, 2, 4, 8, 12, 24, 30, 36, 48, 72, 96 and 120
additional weaners were added to the group (lactating hours after dosing. Two of the sheep were not included

226
in the analysis as no anthelminitic was detectable
in their plasma samples. The systemic availability of
albendazole metabolites was the same in both goats
and sheep. Peak albendazole sulphone levels occurred
earlier, and fell off faster, in goats than in sheep,
indicating a faster rate of albendazole metabolism
in goats (ACIAR 1994).
Host genetic control of internal parasites
The results of investigations into host genetic controls
have previously been published in the scientific literature
(Woolaston et al. 1995, Woolaston et al. 1996,
Woolaston et al. 1992) and so will only be
discussed briefly.
Goats
Faecal egg count data were collected from 1513 A good quality ram with little wool cover and good
weaner goats (<365 days old) and 951 adult (>365 conformation. (ACIAR)
days old) goats on government research stations from
1988 to 1992. During 1988 and 1989 animals were
Haematological data collected in 1988 and
carrying naturally acquired, mixed parasite infections,
1989 when H. contortus was present in the worm
but in 1991 and 1992 animals were treated with
burden indicated that neither packed cell volume nor
closantel 1 month before sampling. Goats were treated haemoglobin measures were of use as indicators for
to remove H. contortus from their worm burdens in an resistance. It was concluded that there was very little
attempt to minimise between animal variation in the scope for within-herd genetic improvement.
ratios of H. contortus and T. colubriformis.
Sheep
There appeared to be an effect of age on egg count
(adult: 508 epg, weaner: 1385 epg) indicative of a Egg-count data were collected from a total of 1826
possible age-acquired immunity to parasites. Birth status weaner sheep from 1988 to 1993. During 1988 and
appeared to affect egg counts with twins and triplets 1989 the sheep were carrying naturally acquired mixed
having higher values than singles. Heritability estimates parasite infections, but from 1991 to 1993 H. contortus
of faecal egg count obtained in both weaners and was removed by drenching with closantel 4–6 weeks
adult goats did not differ significantly from zero. before sampling.

227
 Age (younger<older), sex (female<male) and year fenbendazole by delivering it in a feed block. This was
affected egg counts. Heritability estimates for the pooled seen as a potential way to maintain high blood levels of
data were 0.23 ± 0.07. The results indicate that there fenbendazole metabolites to increase its effectiveness
is a good chance of selecting for reduced faecal egg against worms that had already developed some levels
count. Faecal egg count has since become a criterion of resistance to the drug.
for the selection of replacement rams on government
Fenbendazole dose-rate trial in goats
sheep stations.
The initial trial carried out during the program was aimed
Haematological data from the 1988 and 1989
at determining appropriate daily fenbendazole (FBZ)
samplings showed that the ‘Fiji Sheep’ had higher
dose rates to control worms in goats as a simulation of
PCV values than pure-bred Barbados Blackbelly
the delivery of FBZ using a medicated block. The trial
sheep, but there were no breed effects on
was carried out using dry adult does (mean liveweight
haemoglobin values or faecal egg counts.
35 kg) which were divided into four groups of 5, 5, 5
Haematological data from the 1991–93 weaners and 4 animals and treated daily with doses of 0, 0.75,
showed significant sex (male>female) and age 1.5 or 5 mg/kg liveweight of FBZ, respectively, for 6
(older>younger) effects on circulating eosinophil weeks. Faecal egg counts were monitored weekly and
counts, however neither breed nor sire effects could be group larval cultures grown to determine the species
detected. There was a negative phenotypic correlation composition. The results indicated that at a dose rate
between faecal egg count and eosinophil count of 3.0 mg/kg FBZ was able to reduce egg counts
suggesting that eosinophil counts would be of little and the production of viable larvae to zero (ACIAR
value as indicators of resistance. 1990b). From the dose-rate trial, urea molasses blocks
were formulated and FBZ powder incorporated at a
rate of 0.75 g/kg of block. The blocks were then used
ACIAR Project 8523: Self medication
in field trials in goats and sheep to test their efficacy.
of ruminants in tethered husbandry
Worm control for small ruminants in Fiji

Fenbendazole-medicated feed blocks in goats

systems
A 36-week experiment compared three treatment groups
Several experiments investigated the use of urea molasses of 20 animals each. Group 1 was given unrestricted
blocks as a delivery mechanism for fenbendazole in access to FBZ medicated urea molasses blocks (FBZ-
small ruminants in goats and sheep over the duration UMB); group 2 was given unrestricted access to
of the project. As resistance to fenbendazole had unmedicated urea molasses blocks (UMB); and group
already been detected on some goat farms in Fiji, the 3 was kept under normal station management (NORM),
research program hoped to increase the efficacy of the which included supplementation with 250 g/head/day

228
of a 50:50 coconut meal to mill mix ration. Individual
animals whose egg counts exceeded 1000 epg were
drenched to maintain good health.
Results indicated that the medicated blocks were
efficacious in controlling egg counts: on average,
animals in the FBZ-UMB group required only 1.9
treatments per animal to maintain health as compared
with 7.25 for the UMB and 7.35 for the NORM groups.
FBZ-UMB and NORM groups exhibited similar and
significantly higher liveweight gains than those of the
UMB group. For the NORM group this is thought to be
due to nutritional supplementation. Analysis of plasma
fenbendazole levels in the FBZ-UMB varied between
individual animals, which indicated variations in block
intakes (ACIAR 1991). A wide range of ingredients can be incorporated into urea
Alternate strategies for fenbendzole-medicated feed molasses blocks for manufacture on farm and in small
blocks in goats (A) enterprises. (ACIAR)

Sixty yearling does from the previous experiment were 12, 36 and 26 per respective group. Average body
dosed with ivermectin and allocated to one of the weight gains for the period were 6.3 kg, 5.0 kg, and
following three treatment groups (two replicates/treatment):
4.5 kg, respectively and average medicated block
1. FBZ-UMBAUR — unrestricted access medicated intakes were 4.0 g/head/day, 31.9 g/head/day,
blocks and 13.4 g/head/day (ACIAR 1992).
2. FBZ1-UMB2 — access to medicated block for Alternate strategies for fenbendazole-medicated
1 week, then unmedicated block for 2 weeks feed blocks in goats (B)
3. FBZ1-UMB3 — access to medicated block for This experiment was similar in design to the previous
1 week, then unmedicated block for 3 weeks.
experiment but a fourth group, managed as per normal
Individual animals were drenched when their egg counts station practices (4–6 weekly drenching and daily
exceeded 1000 epg. supplementation 150 g/head/day of a 50:50 coconut
FBZ-UMBUR animals had lower egg counts than meal to mill-mix ration), was included (NORM). FBZ-
other animals on most occasions. Numbers of animals UMBUR, FBZ1-MB2 and FBZ1-UMB3 treatments had
requiring drenching over the 22 weeks of the trial were lower egg counts than the NORM treatment throughout

229
 the trial. Drenching of animals was done on 30, 24,
and 26 occasions for the FBZ-UMBUR, FBZ1-MB2
and FBZ1-UMB3 treatments, respectively, compared
with 81 for the NORM treatment. H. contortus and
T. colubriformis dominated larval cultures. Body weight
gains were 3.0 kg, 3.1 kg, 3.6 kg and 6.6 kg,
respectively (ACIAR 1992).
Fenbendazole-medicated feed blocks
in periparturient goats
Sixty-four pregnant does were divided into two even
groups and allocated to separate 7 ha pasture plots.
The experiment began mid-May and the does were
expected to kid in the last week of June. Does in one
group (FBZ-UMB) were given access to unmedicated
blocks until one month before their expected kidding Urea molasses blocks can be mixed by hand in a drum
date, when they were drenched with ivermectin and or in a small concrete mixer. (ACIAR)
their blocks were changed to medicated. No does were
drenched unless they showed clinical signs of infection. Fenbendazole-medicated feed blocks
The second group was subjected to normal station in periparturient sheep (A)
management including regular drenching (NORM).
Sixty pregnant female sheep were allocated
Egg counts of the FBZ-UMB group were lower than to the following three groups:
those of the NORM group on all occasions. They also
1. FBZ-UMB — medicated blocks
Worm control for small ruminants in Fiji

needed fewer drenches than the NORM group (25 and

78, respectively). H. contortus and T. colubriformis 2. UMB — unmedicated blocks
dominated larval cultures. Average doe liveweights and
3. CON — no blocks.
kid birthweights were similar for the two treatments.
Weaning weights of the NORM group were higher All animals were grazed during the day and housed
as a result of their access to coconut meal supplements at night. The FBZ-UMB and UMB had access to their
from birth; kids of the FBZ-UMB group were not blocks at night. A fourth group was later selected from
supplemented during the trial (ACIAR 1992). the general herd for comparison. They were not housed
at all but subjected to normal station management
(NORM). The trial was run for 18 weeks.

230
Animals in the FBZ-UMB group tended to have lower treatments. The lower egg counts in the UMB group
egg counts throughout the trial. The UMB group had appear to be due to improved nutrition as a result of
lower egg counts than the CON and NORM, though access to the blocks. During the trial, block intakes in
it was necessary to drench all UMB animals in week the UMB group were much higher than the FBZ-UMB
12 to prevent mortalities. group. Liveweight of UMB lambs was higher than
those of other groups at the completion of the trial but
Block intakes in the UMB group over the duration of the
this appeared to be due to their higher initial liveweights
trial were much higher than in the FBZ-UMB groups.
(ACIAR 1992).
There was no significant effect of treatment on ewe
body weights, but there was a major difference in Fenbendazole-medicated feed blocks
the weight of lambs at weaning. Lambs of the UMB in periparturient sheep (B)
group were 5 kg heavier than those of the FBZ-UMB
Sixty pregnant ewes were dosed with Ivomec and
and CON groups. The weaning weights of the lambs
then allocated to one of two treatment groups and
of the NORM group were a further 2 kg behind the
FBZ-UMB and CON groups. There appeared to be a grazed in separate 2 ha paddocks. One group had
benefit from improved nutrition in both egg count and access to medicated blocks (FBZ-UMB) in its night
weaning weights in the UMB treatment. Low block shed, the other to unmedicated blocks (UMB). Egg
consumption appears to have limited the effectiveness counts were significantly lower in the FBZ-UMB group
of the FBZ-UMB in this trial. At weaning the ewes were on all occasions. It was not necessary to treat any
removed from the trial and the lambs retained in their of the ewes and the FBZ-UMB effectively suppressed
treatment groups for experimentation (ACIAR 1991). the periparturient rise in egg count.

Fenbendazole-medicated feed blocks in lambs Ewes in the UMB group all needed to be treated
after weaning (A) in the third month of the trial. FBZ-UMB block intakes
were higher than for UMB (38.8 g/head/day vs
Lambs weaned from ewes in the previous experiment
1.4 g/head/day). H. contortus and T. colubriformis
remained in their respective treatment groups (FBZ-UMB,
dominated larval cultures, Oesphagostomum spp.
UMB, CON and NORM). If group sizes were not even,
was also present in small numbers.
additional lambs of similar weights and ages were
added. Animals not receiving blocks were supplemented Ewe liveweights and lamb birth weights were not
with a 50:50 coconut meal to mill-mix ration as per significantly affected by treatment, but lamb weaning
normal station management. weight at 3 months of age was significantly higher in
Animals in the NORM treatment exhibited high egg the FBZ-UMB treatment than the UMB treatment (17.2
counts and needed to be drenched monthly. Over kg vs 14.6 kg). At weaning, the ewes were removed
the trial period egg counts were lowest in the UMB from the trial and the lambs retained in their treatment
group followed by the FBZ-UMB, CON and NORM groups for further experimentation (ACIAR 1992).

231
 Fenbendazole-medicated feed blocks Fenbendazole-medicated feed blocks in conjunction
in lambs after weaning (B) with rapid rotational grazing
Lambs born in the previous experiment were retained This experiment was designed to test the use of
in their respective treatment groups (FBZ-UMB and medicated blocks in conjunction with rapid rotational
UMB). If group sizes were not even, additional lambs grazing in a 10-paddock, 35-day rotation scheme. Sixty
of similar weights and ages were added. All animals pregnant does were allocated to one of three treatment
were drenched with ivermectin at the start of the trial. groups each with two replicates of 10 does per group:
Individual animals with egg counts above 4000 epg
1. FBZ-UMB35 — rotational grazing with medicated
received salvage treatments. A breakdown of the block
blocks for the first cycle of rotation
mixer meant that blocks were not available for the
FBZ-UMB and UMB groups for 55 and 38 days, 2. FBZ-UMB70 — rotational grazing with medicated
respectively, though average daily block consumption blocks for the first two cycles
was similar for both treatments (40.3 g/head/day 3. UMB — unlimited access to unmedicated blocks.
and 47.4 g/head/day).
A separate group of 20 does, maintained under normal
Egg counts were significantly lower in the FBZ-UMB station management (NORM), were kept nearby.
group than the UMB group. H. contortus and T. NORM does were fed a ration of 250 g/head/day
colubriformis dominated larval cultures. At the completion of a 50:50 coconut meal to mill-mix ration from 28 days
of the trial the initial 2.6 kg weaning weight advantage before their expected kidding date, until the end of
of the FBZ-UMB group had increased to 4.3 kg with the trial, which ran for 30 weeks. Animals with egg
the FBZ-UMB group weighing 30.1 kg and the UMB counts above 1000 epg were drenched to maintain
group weighing 25.8 kg (ACIAR 1993). good health.
Does in the FBZ-UMB70 treatment had significantly
ACIAR PN9132: Nutritional and lower egg counts over the period of the trial. During
Worm control for small ruminants in Fiji

periods when the FBZ-UMB70 and FBZ-UMB35

chemo-therapeutic strategies for
treatments had access to medicated blocks no parasite
sustainable control of gastrointestinal eggs were detected in their faeces. Goats in the NORM
treatment had the highest egg counts at all times,
parasites of ruminants
followed by the UMB treatment. Numbers of animals
Project 9132 was an extension of project 8523. A trial requiring anthelmintic treatment to maintain health were
was carried out to investigate the possibilities of using 6, 25, 38, and 25 for the respective treatment groups.
medicated and unmedicated blocks to control worms in Doe liveweights at the completion of the trial in the
goats managed in a rapid rotational grazing program. FBZ-UMB70, FBZ-UMB35 and NORM treatments were

232
similar, but liveweights of does in the UMB treatment access to medicated blocks (FBZ-UMB at 0.75g
were lower. A similar pattern was seen in the liveweights FBZ/kg), two groups to unmedicated blocks (UMB)
of kids at weaning. and two received no supplementation (CON). Animals
with egg counts above 3000 epg were drenched with
Nutritional supplementation given to the NORM group
anthelmintic to avoid unnecessary mortalities. Egg counts
appears to have been sufficient to compensate for the
were lowest for the FBZ-UMB group and highest for the
losses in production seen in the UMB treatment. This
CON group, while the UMB group was intermediate
resulted in final doe liveweight and mean kid weaning
(Figure 13.1).
weight being similar to those of the FBZ-UMB70 and
FBZ-UMB35 treatments. During the experiment it was necessary to salvage treat
FBZ-UMB, UMB and CON ewes 13, 55 and 92 times,
Effect of worm control and nutrition on development
respectively. Larval cultures indicated that Haemonchus
of young ewes (9132 A)
spp. and Trichostrongylus spp. were dominant.
Manueli et al. (1995) investigated the effects of worms Oesophagostomum spp. were also present but in low
and nutrition on young Fiji sheep at pasture. Six groups numbers. At mating, after 7 months of experimentation,
of 30 ewes (11 months old) were each placed into the FBZ-UMB and UMB groups had gained more weight
2 ha paddocks. Two groups were allowed unlimited than the CON group (10.5 kg, 10.0 kg, and 5.8 kg,

Figure 13.1 Trends in Faecal Egg Counts 9132A

4000
3500
FBZ-UMB
3000 UMB
2500 CON
FEC (epg)

2000
1500
1000
500
0
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18

Sampling Period

233
 respectively). Ewe conception rates, lambing
Table 13.2 Effect of Fenbendazole-medicated
percentages and total weight of lambs weaned
and unmedicated feed blocks on
were increased by FBZ-UMB and UMB with the
former providing a greater increase. The benefits in reproductive and lambing performance
reproductive performance are thought to be caused FBZ-UMB UMB CON
by the higher mating liveweights of the FBZ-UMB
Ewes lambing 40 34 22
and UMB groups. The large benefits in total weights
of lambs weaned per treatment are caused by Lambs born 44 40 24
nutritional benefits from UMB and the benefits of Total weight born (kg) 144 126 66
worm control and nutrition in the FBZ-UMB treatment Lambs weaned 40 39 20
(Table 13.2). In comparison with unsupplemented Lamb weaning weight (kg) 13.2 10.4 11.1
controls, weight of lambs weaned per treatment
Total weight weaned (kg) 528 405 222
was increased by 82% and 138% for the UMB
and FBZ-UMB treatments, respectively. Lamb mortality rate (%) 9.1 2.5 16.6
FBZ-UMB = urea molasses feed block containing fenbendazole, UMB =
At the completion of the trial the ewes were returned urea molasses feed block with no anthelmintic added, CON = control,
no block
to the main flock and subjected to normal station
management. An investigation of their performance

Figure 13.2 Treatment Effects on Faecal Egg Counts 9132B

3000
Faecal Egg Count (EPG)

2500 FBZ-UMB
Worm control for small ruminants in Fiji

2000 UMB
CON
1500

1000

500

0
1 2 3 4 5 6 7 8 9 10 11 12
Period

234
in the 1995 lambing season reveals no significant
Table 13.3 Effect of fenbendazole-medicated
differences in pre-mating liveweights or their subsequent
and unmedicated feed blocks on
reproductive performance, indicating that there is
lambing performance
no carryover effect of early suppressive anthelmintic
control (FBZ-UMB) or nutritional supplementation (UMB) FBZ-UMB UMB CON
on ewe reproductive performance. Lambs born 46 43 41
Effect of worm control and nutrition on lambing Total weight born (kg) 173 146 134
performance of maiden ewes (9132 B) Lambs weaned 36 31 19
The results of the previous experiment demonstrated the Total weight weaned (kg) 537 382 206
benefit of the continuous use of the medicated blocks. Lamb mortality rate (%) 21.7 28 53.6
A second trial was designed to investigate the effects FBZ-UMB = urea molasses feed block containing fenbendazole, UMB =
of strategic use of the fenbendazole medicated blocks urea molasses feed block with no anthelmintic added, CON = control,
no block
(FBZ-UMB) to reduce usage of the anthelmintic and
costs and to avoid possible problems of drug resistance
that could develop with the extended use of the (CON). Animals whose egg counts exceeded
fenbendazole blocks. Manueli et al. (unpublished) tested 3000 epg were drenched with anthelmintic to avoid
a program of short-term use of FBZ-UMB in conjunction unnecessary mortalities. Egg counts were lowest for
with unmedicated blocks (UMB) to determine the optimal the FBZ-UMB group and highest for the CON group
time for their prophylactic use. A group of 150 ewes while the UMB group was intermediate (Figure 13.2).
(15-months old) were divided into six even groups
During the experiment it was necessary to salvage
according to bodyweight and allocated to 2 ha
treat individual FBZ-UMB, UMB and CON ewes 4,
paddocks. The two groups were given:
14 and 32 times respectively. Larval cultures indicated
■ unlimited access to UMB for 8 weeks that Haemonchus spp. and Trichostrongylus spp. were
■ substitution of UMB with FBZ-UMB (0.75g FBZ/kg) dominant and that Oesophagostomum spp. were also
4 weeks before, and 7 weeks during, mating present but in low numbers. Treatment differences in
ewe reproductive performances and liveweights during
■ return to UMB until 4 weeks before parturition, the experiment were not significant. Treatment had a
and then substantially positive effect on numbers of lambs weaned
■ access to FBZ-UMB again until lambs were weaned. and the total weight of lambs weaned (Table 13.3).

Another two groups had unlimited access to UMB and

the remaining two groups received no supplementation

235
 Effect of worm control and nutrition on performance entering the trial and this may have affected mean
of periparturient maiden ewes treatment egg counts and milk yields. Four, 12 and
39 salvage treatments were required for the FBZ-UMB,
The results of trials 9132A and 9132B clearly
UMB and control groups, respectively.
demonstrated beneficial increases in weight gain
by using FBZ-UMB and UMB compared with The mean daily milk production of ewes from the
unsupplemented controls. However, the experiments FBZ-UMB group was significantly higher than production
failed to clearly identify the mechanisms by which the from the UMB and CON groups. Milk composition
benefits accrued. In an attempt to identify the mechanism (as a percentage) was not affected by treatment,
by which this occurred, Manueli et al. (unpublished) however, there was a significant effect of treatment on
investigated the effects of FBZ-UMB on the growth of mean daily milk yield, mean daily milk fat production
lambs and the milk production of ewes. Seventy-two and mean daily milk protein production (Table 13.4).
pregnant, 21-month old, Fiji ewes were divided into The differences in milk production were reflected in
six even groups according to bodyweight and allocated numbers of lambs weaned and total weights of lambs
to 1 ha paddocks. Two groups had unlimited access weaned in the various treatment groups (Table 13.5).
to FBZ-UMB (0.75g FBZ/kg), two to UMB and two
received no supplementation (CON). Animals with
egg counts above 3000 epg were drenched with
Research into biological control
anthelmintic to avoid unnecessary mortalities. Ewe milk of gastro-intestinal parasites in Fiji
production was estimated three times at monthly intervals
using the oxytocin injection (1 ml oxytocin) and hand Research into the use of nematophagous fungi to control
milking method and the milk fat and milk protein worms in small rumiannts in Fiji began in 1996. The
contents were determined. Mean 63-day milk yield first investigations, in conjunction with the CSIRO and
was estimated by multiplying mean daily milk yield under the aegis of ACIAR, involved conducting a survey
by the number of days between the three milk- to try to collect the nematophagous fungus Duddingtonia
Worm control for small ruminants in Fiji

production estimates. flagrans from local small ruminant farms (Manueli et

al. 1999).
Log transformed (Log(FEC+1)) egg counts were lowest
for the FBZ-UMB group (370 ± 288 epg) and highest Some 2712 faecal samples were collected and
for the CON group (2878 ± 290), while the UMB cultured from a total of 26 sheep and goat farms
group (2790 ± 291) was intermediate. Despite the use in Fiji. The survey yielded 23 nematophagous fungi
of salvage treatments some ewes died (FBZ-UMB: 2, isolates. Eleven of these were lost and a further 12 were
UMB: 6, CON: 10) from an outbreak of haemonchosis identified as belonging to one of four species of the
during the latter part of the trial. Ewes that died were genus Arthrobotrys.
replaced with animals that had been drenched before

236
 Subsequently, an isolate of D. flagrans was imported
Table 13.4 Effect of fenbendazole-medicated
from CSIRO in Australia and a series of pen and field
and unmedicated feed blocks on
trials conducted. D. flagrans chlamydospores were fed
ewe milk production
to animals carrying naturally acquired worm infections,
FBZ-UMB UMB CON and the percentage of their faecal egg counts recovered
Mean daily milk yield 607 418 381
as infective larvae was monitored.
(ml/day) (se ±) (45.4) (46.8) (50.5) D. flagrans was effective in trapping infective larvae
Mean daily milk fat 29.8 21.4 17.59 in faecal cultures at a range of dose rates (Manueli
production (se ±) (2.7) (2.8) (3.2) unpublished data). The trapping of infective larvae
Mean daily milk protein 44.2 29.1 25.4 resulted in reductions of up to 90% in the numbers of
production (se ±) (5.1) (5.2) (5.6) larvae recovered from larval cultures. Replicated field
63 day milk yield (l) 38.2 26.3 24.0 trials aimed at investigating the use of D. flagrans under
FBZ-UMB = urea molasses feed block containing fenbendazole, grazing conditions are on-going. Initial results are
UMB = urea molasses feed block with no anthelmintic added, variable with larval recoveries from grazing animals
CON = control, no block
fed D. flagrans daily, ranging from 0 to 60% of those
from control animals without access to D. flagrans.

Table 13.5 Effects of fenbendazole-medicated

and unmedicated feed blocks on Conclusions
lambing performance ■ Anthelmintic resistance means that it is necessary
FBZ-UMB UMB CON to develop sustainable parasite control measures.

Lambs born 23 24 21 ■ The most important worms of small ruminants in Fiji

Total weight born (kg) 78 76 62
are H. contortus and T. colubriformis; M. digitatus
does not readily infect goats.
Lambs weaned 18 15 8
Total weight weaned (kg) 318 196 118 ■ Larvae survive on pastures all year round. Infective
Lamb mortality rate (%) 21.7 37.5 62
larval stages are generally available on pasture
by 4 days after faecal contamination with
FBZ-UMB = urea molasses feed block containing fenbendazole,
UMB = urea molasses feed block with no anthelmintic added, parasite eggs.
CON = control, no block
■ Rotational grazing using eight paddocks over
28 days or 10 paddocks over 35 days can be
effective for the control of worms in small ruminants.
Reducing the number of paddocks in a 28-day
rotational grazing system makes it ineffective.

237
 ■ It is not necessary to drench young stock fortnightly. ■ FBZ-UMBs can reduce the need for drenching in
small ruminants. The strategic use of FBZ-UMBs with
■ Albendazole sustained-release capsules are not
unmedicated blocks can be effective in controlling
effective in goats but are extremely effective in
worms in small ruminants. FBZ-UMBs can be used
sheep. Albendazole is metabolised faster in goats
in conjunction with RRG to control worm infections
than it is in sheep.
in small ruminants.
■ Night yarding has no effect on faecal egg counts
■ Improved nutrition can be beneficial in helping
in goats.
worm-infected small ruminants overcome and/or
■ Evidence for the development of age immunity in withstand the effects of infection.
goats is equivocal. Epidemiological studies indicate
■ In young ewes worms can affect reproduction
that little age resistance occurs, though the genetic
by delaying the attainment of oestrous, resulting in
studies found evidence of an age effect.
fewer lambs. This is exacerbated by sub-optimal
■ Faecal egg count is not heritable in goats in Fiji. nutrition. This effect does not carry over. These
However, it is heritable in sheep and can therefore effects on reproduction do not occur in well-grown
be used in selection programs. Eosiniphil count is ewe hoggets.
not a good predictor of faecal egg count in sheep.
■ Worms cause reductions in ewe total milk yields,
■ Fenbendazole administered at a dose rate of total fat yields and total protein yields. Worms affect
3.0 g/kg liveweight can reduce egg counts and the growth rates of lambs from birth to weaning.
larval hatch rates to zero. Fenbendazole medicated
■ Nematophagous fungi surveys were unable to
blocks (FBZ-UMB) can be used to control worms
identify D. flagrans in Fiji.
in sheep and goats provided block intakes are
adequate. There is much variation within flocks ■ Biological control using D. flagrans has potential but
and herds in FBZ-UMB intakes. problems of delivery and fungal culture methods need
Worm control for small ruminants in Fiji

to be addressed. Pen trials have been successful

though results in field trials have been variable.

238
References ACIAR. 1996. Third Annual Report, ACIAR Project
No: 9132, Strategies for sustainable control of
ACIAR. 1988. Third Annual Report—1988, Project gastrointestinal parasites of ruminants using urea-
No. 8418: The Epidemiology and Control of molasses blocks, ACIAR, Australia.
Gastro-Intestinal Nematode of Small Ruminants
ACIAR. 1997. Forth Annual Report, ACIAR Project
in the Pacific Islands.
No: 9132, Strategies for sustainable control of
ACIAR. 1994. Termination Report on ACIAR Project gastrointestinal parasites of ruminants using urea-
No. 8913: Ecological and Host Genetic Control molasses blocks, ACIAR, Australia.
of Internal Parasites of Small Ruminants in the Pacific
Baker, J.L. 1970. Sheep Farm Nawaicoba: a report
Islands, ACIAR, Australia.
on five years operations 1965–1969, Mimeo,
ACIAR. 1990a. Fourth Annual Report on ACIAR Project Department of Agriculture, Fiji.
No. 8418: The Epidemiology and Control of
Banks, D., Singh, R. and Pratap, B. 1987. Goats,
Gastro-Intestinal Parasites in the Pacific Islands, ACIAR
Annual Research Report, Research Division,
AustraliaACIAR. 1990b. Annual Report 1989–1990,
Ministry of Primary Industries, Suva, Fiji.
ACIAR Project No. 8523: Self Medication of Ruminants
in Tethered Husbandry Systems, ACIAR, Australia. Banks, D.J.D, Singh, R., Barger, I.A., Pratap, B. and
Le Jambre, L.F. 1990. Development and Survival
ACIAR. 1991. Annual Report 1990–1991, ACIAR Project
of Infective Larvae of Haemonchus contortus and
No. 8523: Self Medication of Ruminants in Tethered
Trichostrongylus colubriformis on pasture in a tropical
Husbandry Systems, ACIAR, Australia.
environment, International Journal for Parasitology,
ACIAR. 1992. Annual Report 1990–1991, ACIAR 20, 5–160.
Project No. 8523: Self Medication of Ruminants
Despeissis, A. 1922. Sheep in Fiji, Agricultural Circular,
in Tethered Husbandry Systems, ACIAR, Australia.
pp. 99–102, Department of Agriculture, Fiji.
ACIAR. 1993. Annual Report 1992, ACIAR Project
Manueli, P.R. 1996. Sustainable control of parasites in
No. 8523: Self Medication of Ruminants in
Small Ruminants, Country Paper, Fiji, In: Sustainable
Tethered Husbandry Systems, ACIAR, Australia.
Parasite Control In Small Ruminants, LeJambre, L.F.,
ACIAR. 1994. Termination Report on ACIAR Project Knox, M.R., ed., Proceedings of an International
8913: Ecological and Host-Genetic Control of Workshop sponsored by ACIAR and held in Bogor,
Internal Parasites of Small Ruminants in the Pacific Indonesia 22–25 April 1996, Australian Centre For
Islands, ACIAR, Australia. International Agricultural Research, Proceedings No.
74, pp. 92–97.
ACIAR. 1995. Second Annual Report, ACIAR Project
No: 9132, Strategies for sustainable control of
gastrointestinal parasites of ruminants using urea-
molasses blocks, ACIAR, Australia.

239
 Manueli, P.R., Waller, P.J., Faedo, M. and Mohammed, Woolaston, R.R., Manueli, P.R., Singh, R., Tabunakawai
F. 1999. Biological Control of Nematode parasites N. and LeJambre L.F. 1995. Breeding to assist control
of Livestock in Fiji: Screening of Fresh Dung of Small of gastrointestinal parasites of small ruminants in the
Ruminants for the Presence of Nematophagous Fungi, Pacific Islands, In: Gray, D.G., Woolaston, R.R.,
Veterinary Parasitology, 81, 39–45. Eaton, B.T., eds., Breeding for resistance to Infectious
Disease in Small Ruminants, Australian Centre for
Singh, D.R., McIntyre, K.H. and Mua, M. 1972.
International Agricultural Research, Canberra, Australia,
The effects of drenching and rotational grazing on
pp. 179–186.
gastro-intestinal parasites of sheep, Fiji Agricultural
Journal, 34, 11–14. Woolaston, R.R., Manueli, P.R., Barger, I.A., Eady, S.J.,
Le Jambre, L.J. and Windon, R.G. 1996. The value
Turbett, C.R. 1940. The Livestock Industry in Fiji,
of circulating eosinophil counts as a selection criterion
Transactions and Proceeding of the Fiji Society
for parasite resistance of sheep to Trichostrongyle
1938–1954, National Archive of Fiji, Suva, Fiji.
parasites, International Journal for Parasitology, 25,
Turbett, C.R. 1929. The Sheep Industry in Fiji, Agricultural 123—126.
Journal, 2(1), pp. 1 –11, Department of Agriculture, Fiji.
Woolaston, R.R., Singh, R., Tabunakawa, N., Le Jambre,
Walkden-Brown, S.W. and Banks, D.J.D. 1986. L.F., Banks, D.J.D. and Barger, I.A. 1992. Genetic
Integrated Small Ruminant and Cropping Systems and environmental influences on worm egg counts
in Fiji with Health as a Major Constraint, In: Small of goats in the humid tropics. Proceedings of the
Ruminant Production Systems in South and South-East Australasian Association for Animal Breeding and
Asia, Proceedings of a Workshop held in Bogor, Genetics 10, 147–150.
6–10 October 1986, International Development
Research Centre, Canada, pp. 289–310.
Worm control for small ruminants in Fiji

240
14. Internal parasites of small ruminants in Papua New Guinea
A.R. Quartermain

Introduction
Internal parasites are seen as a primary threat to the 3. Highlands from 1200 m up to the limit of cultivation,
expansion and improvement of smallholder production about 2700 m. The highlands are cooler with an
of sheep and goats in the humid tropics. This chapter even temperate climate. There are occasional frosts
reviews the literature on internal parasitism of small above 1800 m, and rainfall is between 2000 and
ruminants in Papua New Guinea (PNG). Documentation 3500 mm, with slight seasonality.
is limited because, in the past, small ruminants in PNG
Essentially there are two types of sheep and one type
have been perceived to be less important than pigs,
of goat in PNG, as discussed by Quartermain (2002).
poultry and cattle. Accordingly, human and financial
Tropical PNG Priangan sheep predominate in zones
resources available for research have been limited.
1 and 2 while sheep now called Highlands Halfbred,
PNG has extremely variable agro-ecological conditions. derived from crossbreeding temperate wooled sheep
Although it is entirely in the wet tropics, altitude ranges (mainly Corriedale and Perendale from New Zealand)
from sea level to above 4000 m and annual rainfall with Priangans, are found in zone 3. Priangan sheep
varies from 1000 mm to more than 6000 mm. For the comprise around 2000 of the total sheep population of
purposes of the present review, it is possible to restrict 15,000. The goat population is estimated at 20,000
discussion to the following three broad climatic zones. and there appears to be no genetic differentiation by
zone. Although derived from early introductions of mainly
1. Permanently wet lowlands and mid-altitude areas up
dairy animals, goats are now kept almost exclusively
to 1200 m, with rainfall from 2000 to 5000 mm.
for meat production (Quartermain 2002). Smallholder
2. Dry or seasonally dry lowlands with rainfall less sheep and goat owners generally keep fewer than
than 2000 mm and pronounced dry periods of 10 animals which they allow to range freely during
up to six months of the year. the day, and house at night.

241
 Endoparasites present in small Table 14.1 Worm species identified in sheep
ruminants of PNG and goats of PNG
Worm Sheep Goats
The first recorded list of parasites of sheep and goats
was derived from a government veterinary laboratory Trematoda
and field reports by Anderson (1960). Egerton and Fasciola hepatica * *
Rothwell (1964) updated Anderson’s list with confirmed Cestoda
diagnoses. At that time they estimated there were only Cysticercus tenuicollis *
500 sheep and 6500 goats in PNG, mainly in the
Moniezia expansa * *
highlands (i.e. above 1200 m). The list is shown
Nematoda
in Table 14.1.
Bunostomum trigonocephalum * *
Subsequently, Asiba (1987) added Mecistocirrus sp.,
Cooperia sp. * *
previously reported in cattle, to the list for sheep, while
Haemonchus contortus * *
Owen (1988,1998a), identified Trichostrongylus axei,
Cooperia curticei, Trichuris ovis and possibly Trichuris Nematodirus sp. * *
skrijabini in sheep. It appears, from the few studies with Nematodirus spathiger *
larval culture, that the dominant genera are Haemonchus, Oesophagostomum columbianum * *
Cooperia, Trichostrongylus and Oesophagostomum. Oesophagostomum asperum *
Internal parasites of small ruminants in Papua New Guinea

Fasciola hepatica is economically important, but Oesophagostomum venulosum *

geographically restricted, while cestodes are thought
Strongyloides papillosus * *
to be unimportant (Asiba 1987).
Trichostrongylus colubriformis * *
Trichuris globulosa * *
Studies of internal parasitism Trichuris ovis *
in small ruminants of PNG
Other than lists of identified species, there are no also apply to goats. In the mixed-species, institutional
published studies of internal parasitism in goats in flocks that are managed with intensive daytime grazing
PNG. It might be expected that parasitism would be in paddocks, both species are treated alike in receiving
less of a problem for goats, which browse more, than regular (usually monthly) dosing with anthelmintics.
for sheep, but this has yet to be verified. The findings Manua (1994) reported a study of smallholder sheep
and comments made in this chapter for sheep, generally and goat farms in the highlands and stated that, although

242
animals were not drenched, they were found to be even with egg counts up to 36,000. Strongyloides
healthy and losses from gastro-intestinal parasites to papillosus was frequently seen in lambs, constituting
be small. However, no data are included to support up to 50% of the larvae with egg counts over 3000.
this statement. Oesophagostomum columbianum and C. curticei
were present at low levels. Pastures remain infective
Dry lowlands all year round and more so in the wet season. There
was little variation from year to year. Parasitism,
Studies on Priangan sheep in the dry lowlands have
generally due to lack of timely treatment, was linked to
been carried out in three locations. The first was the
the deaths of only five ewes and five lambs over the
National Veterinary Laboratory, where a small flock
15 years. Five Corriedale ewes present during the first
(established in the 1950s) grazes on a small area
few years showed little resistance to parasites and had
of pasture with supplementary feeding as necessary.
consistently higher egg counts than the Priangans. It
The area has an annual rainfall varying from 500
was concluded, overall, that the majority of the
to 1500 mm and a seasonal dry period from May
Priangan animals showed a level of either resistance
to November. From 1980 to 1994 the flock, ranging in
or tolerance that enabled them to survive and produce
size over the years from nine to 35 ewes, was monitored
under poor nutritional and high parasite challenge
weekly for faecal egg counts (Owen and Awui 2000).
conditions.
No anthelmintics were used up to 1984 but thereafter
sheep were treated when egg counts (eggs per gram) Another study, carried out with the Priangan flock at the
were higher than 5000 or sheep showed symptoms. National Veterinary Laboratory (Owen 1988), was
Pre-weaning mortality to 12 weeks averaged 20.2%. designed to evaluate closantel as an anthelmintic with
Over all years, only 0.06% of rams and 0.36% of ewes residual activity and high efficacy against H. contortus.
had egg counts higher than 10,000, with most high Sheep with egg counts above 500 were treated with
counts in ewes coinciding with lambing. This lambing either 7.5 or 15.0 mg/kg. After treatment, egg counts
rise occurred in 64.2% of births, usually peaked at dropped markedly within 3 days and remained low
5000 and returned to normal within 4–8 weeks without for 7–10 weeks, depending on the dose rate.
treatment. Counts in lambs were more variable with Haemonchus eggs vanished from the faeces of the
14–76% of yearly average egg counts lower than 500 treated sheep but gradually increased during weeks
and 0–6% higher than 10,000. Most lambs showed 5–8 and reached pre-treatment levels by weeks 12–13.
a rise between 7 weeks and 3 months of age. Haemonchus remained at 69% of the larval population
Haemonchus contortus was the most prevalent parasite in untreated cohorts. When all sheep were dosed with
in egg counts over 3000 but otherwise Trichostrongylus 15 mg, control continued for 21 weeks and egg counts
species prevailed. The former could cause death with were only half of the pre-treatment levels at 26 weeks.
egg counts over 10,000 but the latter was not lethal The proportion of Haemonchus larvae dropped from

243
 51% to nil within 3 days, began to re-appear in week Larval cultures showed Haemonchus and Cooperia
9 and gradually increased back to 50% in week 23. to be dominant at Erap and Trichostrongylus at Urimo.
Trichostrongylus larvae dominated when Haemonchus It appears that parasitism is a minor problem for these
was absent and declined as the latter reappeared. sheep, under these conditions, at low stocking rates.
It was concluded that the benefits of closantel are Observations at Erap also suggest that housing sheep
only realised when all sheep are dosed, with benefits on slatted floors at night did not reduce parasitism.
lasting up to 5–6 months.
The other two dry lowland locations where sheep were
Wet lowlands
studied were Erap in the Markham Valley, and Urimo The only formal study in the wet lowlands was at
on the Sepik Plains. The former has an average annual another treatment site used in the levamisole study
rainfall of 1250 mm with a little seasonal variation, by Holmes and Absolum (1985). The site was on
while the latter has a similar climate but with a higher the coast and had an annual rainfall higher than
rainfall (1850 mm). The government Priangan flock at 4000 mm. Twenty sheep grazed freely over about
Erap was derived from the sheep of Southeast Asian 40 ha of swampy pasture during the day and were
origin accumulated in 1971 from scattered remnants housed at night on a slatted floor. Egg counts were
and, subsequently, was used to establish the other main low in all groups, the monthly average ranging from
institutional flocks and the Highlands Halfbred sheep. 8 to 270 in the untreated sheep. Treatment reduced
Holmes and Absolum (1985) reported the results of a trial counts but differences among drenching intervals were
where, at each site, a total of 20 wethers aged 6–18 inconsistent. Although drenched wethers grew faster than
Internal parasites of small ruminants in Papua New Guinea

months were divided into groups and treated with untreated animals, this was only significant for the
levamisole (Nilverm). The sheep were drenched at 0, smaller, younger sheep. Across all three sites in the
4, 8 or 12−week intervals over a period of 12 months Holmes and Absolum (1985) study, small drenched
at Erap and 9 months at Urimo. Erap sheep were set- wethers grew at 0.54 kg/week compared with 0.32
stocked at five sheep/ha on pasture while those at Urimo for untreated sheep. In spite of this response, it was
grazed over a large area during the day and were concluded that even under these very wet conditions,
housed at night. Egg counts were measured every 4 with a low stocking rate, internal parasitism is a
weeks. The treated wethers out-performed the controls minor problem.
at both sites but only marginally at Urimo. The highest
In the two larger institutional flocks of goats and
monthly average egg count in the untreated sheep was
Priangan sheep in the wet lowlands — at the PNG
only 3060 at Erap and 856 at Urimo. Drenching
University of Technology and the National Agricultural
reduced egg counts but there were no differences
Research Institute — all animals are currently drenched
among drenching intervals. The response was greater
monthly with benzimidazole (Panacur), as a safeguard
in the younger sheep but there were no correlations
against mortality. Both flocks graze pasture at a high
between growth rates and counts within or across sites.
stocking rate and are housed at night on slatted floors.

244
Highlands
Most of the data for the highlands zone come from
the government sheep-breeding flock held at Menifo
in the Eastern Highlands Province. The Menifo station,
at 1608 m, was the site for the introduction of sheep
from New Zealand under the Sheep Development
Project which started in 1975. The average annual
rainfall varies from 1000 to 1500 mm with a drier
period between June and September. It has a drier
climate than most of the highland zone. Owen (1998a)
monitored Corriedale sheep on intensive grazing over Priangan sheep with some locally adapted meat goats.
2 years from July 1997 and used worm-free tracer (A.R. Quartermain)
lambs to monitor parasite species. Of the nine species
of worms found (all previously listed) the most prevalent Owen (1998b) studied the possible role of mixed
were H. contortus and Trichostrongylus colubriformis. grazing of sheep and cattle as a management option
The latter became dominant when the former was for parasite control in areas where the climate allows
controlled. Natural seasonal availability of larvae on the year-round development and survival of parasites on
pasture could not be determined because anthelmintic pasture. Priangan X Corriedale and Corriedale sheep
treatment was started in December 1977, when egg were grazed together with Brahman X steers and
counts were high, and became a regular program from monitored in two separate one-year trials at Aiyura,
May 1978. Nevertheless, larvae were plentiful on in the Eastern Highlands, which had rainfall of 1860
the pasture at all times (although at lower levels in the and 1877 mm in the two respective trial years. Egg
second year, probably because of the treatments). High counts were measured every 4 weeks in the first year
egg counts could occur at any time and Haemonchus and every 2 weeks in the second. Sheep grazing with
could dominate at any time. The longevity of free-living cattle had lower overall egg counts than sheep grazing
stages of Haemonchus after hatching, as evidenced alone but this reduction was not enough to prevent
by the tracer lambs after specific dosing of the other haemonchosis and the need for drenching. Haemonchus
sheep, ranged from less than 12 days, at the end and Trichostrongylus dominated in sheep, with the latter
of the wetter season, to about 3 weeks. This short dominant during the drier months of the second year.
survival time would appear to be the key for control Corriedale sheep had consistently higher egg counts
of Haemonchus with the strategic use of closantel or than crossbreds. Steers had negligible egg counts for
rafoxanide, together with a broad spectrum drench, about 8 months each year after being dosed with
before any expected rainy season build-up of parasites. levamisole or rafoxanide. Mixed grazing resulted in

245
 a 50% increase in weight gain for the wether hoggets highlands station (2,240 m) are grazed on pasture and
but much of this could be attributed to better pasture all sheep are drenched monthly. However, drenching
growth and utilisation. Mixed grazing with sheep and is not practised by 10 smallholder keepers of sheep
cattle is not a practical option for most smallholder and goats in the Tambul area (F. Dua, pers. comm.).
farmers in PNG.
The only trematode of concern is F. hepatica which was
Asiba (1987) drew attention to the lack of information inadvertently introduced from Australia with early sheep
about basic health and production of smallholder sheep introductions and established itself in the highlands where
flocks but stated that gastrointestinal nematodes cause its intermediate host, the snail Lymnaea viridis, thrives,
significant losses in flocks set-stocked for any length of given suitable environments. Distribution of the snail is
time. Subsequently, he elaborated on the situation in limited by temperature to areas above 600 m and is
the highlands by drawing on his own experiences as uneven. Fasciolosis is a particular problem at Menifo.
a regional veterinarian, and on National Veterinary Owen (1989) has described the epidemiology, using
Laboratory reports from 1977 to 1994 (Asiba 1995). fluke-free weaner lambs over a period of 22 months
However, much of this information again came from at Aiyura. Metacercariae can be found on pasture
Menifo. Supported by evidence from autopsies, the throughout the year if sheep have access to snail-
majority of deaths could be attributed to parasitism. contaminated sites. The presence of swampy areas,
Pneumonia commonly showed up in post mortems and drainage lines or ponds gives persistent snail populations
this could be secondary to stress caused by parasitism. which can spread onto pasture whenever prolonged
Evidence from a prolonged dry spell in 1993 suggests heavy rain saturates pastures and soils. It appears that
Internal parasites of small ruminants in Papua New Guinea

poor nutrition as a predisposing factor. Fifteen sheep 125 mm of rain in a 4-week period is necessary for
monitored in successive weeks in February 1994 had infected snails to move onto saturated pasture and
egg counts ranging from 120 to 11,740. The author liberate cercariae. There was considerable variation
suggests that eggs persist on the pasture in the Eastern between lambs with one weaner having 446 flukes in
Highlands for up to 5–6 months and hence egg its liver after only 2 months of grazing exposure while
counts remain high even after dosing with benzimidasole another had only one fluke. Sheep are liable to acquire
or levamisole drugs. The suggestions for institutional low level infection leading to chronic fasciolosis at any
flocks in the highlands are controlled grazing, improved time when continuous contamination of pasture occurs.
nutrition, and monitoring of egg counts so treatment can However, acute fasciolosis may occur with heavy
be applied as needed. Strategic drenching immediately grazing under wet conditions when snails migrate
after weaning, at the onset of the rainy season if one onto flooded pastures or when sheep have access
exists, and before lambing could be useful. Sheep of to areas that remain permanently wet.
the National Agricultural Research Institute at the Tambul

246
Conclusions References
■ Parasite species identified include one trematode, Anderson, J.L. 1960. Animal health picture of the Territory
two cestodes and 14 nematodes. of Papua and New Guinea. Papua and New Guinea
Agricultural Journal 13, 52–58.
■ No work has been done specifically on goats.
Asiba, G.B. 1987. Small holder flock health.
■ In the lowlands, H. contortus and species of In: Sivasupiramaniam, S. and Tupper, G., ed.,
Trichostrongylus, Strongyloides, Oesophagostomum Proceedings of the First Symposium on Sheep and
and Cooperia appear to dominate. Goat Production in Papua New Guinea, held at
■ Parasitism is only a problem, even under very Goroka 1–2 December 1987. Village Livestock
high rainfall conditions, with intensive grazing Development Project, Department of Agriculture
and Livestock, Goroka. pp. 14–18.
or set-stocking.
Asiba, G.B. 1995. Health problems of sheep in the
■ Control can be achieved with strategic drenching,
highlands of Papua New Guinea. Harvest 17,
especially if targeted at Haemonchus.
24–30.
■ Local Priangan sheep appear to have some
Egerton, J.R. and Rothwell, T.L.W. 1964. The Distribution
tolerance or resistance to endoparasites.
of Infectious and Parasitic Diseases of Animals in
■ In the cooler highlands, H. contortus and Papua and New Guinea. Research Bulletin No.1,
T. colubriformis dominate. Eggs and larvae Veterinary Science Series, 1964. Department of
are available at all times on intensively grazed Agriculture and Livestock, Port Moresby. 31 pp.
pastures although Haemonchus larvae have Holmes, J.H.G and Absalom, P. 1985. Growth rates of
a short survival time. Priangon crossbred sheep and some effects of internal
■ Although mixed grazing of sheep and cattle has parasitism in the lowlands of Papua New Guinea.
Papua New Guinea Journal of Agriculture, Forestry
proven beneficial it is not a practical option for
and Fisheries 33, 109–113.
most smallholders.
Manua, P.N. 1994. Performance of sheep and goats
■ F. hepatica is locally important in the highlands
in small-holder farms in Eastern Highlands Province
and infestation requires management solutions.
of Papua New Guinea. Harvest 16, 10–11.
■ In general, under conditions in which parasite Owen, I.L. 1988. Field trials with closantel and
problems exist, solutions depend on grazing Haemonchus contortus in sheep in Papua New
management and strategic drenching. Guinea. Australian Veterinary Journal 65, 267–270.
■ Smallholder farmers seem to manage adequately
without treating their stock with drugs.

247
 Owen, I.L. 1989. The epidemiology of fasciolosis in Quartermain, A.R. 2002. Conservation of Domestic
Papua New Guinea. Australian Veterinary Journal Animal Genetic Resources in Papua New Guinea.
66, 58–60. NARI Technical Bulletin Series, Technical Bulletin
No. 4. National Agricultural Research Institute,
Owen, I.L. 1998a. A study of the contamination of sheep
Lae. iv + 31 pp.
pasture with nematode larvae in the highlands of Papua
New Guinea. Science in New Guinea 24, 3–9. Talbot, N.T. 1969. New recordings of animal parasites
in Papua and New Guinea. Papua and New
Owen, I.L. 1998b. Mixed grazing of sheep and cattle in
Guinea Agricultural Journal 20, 89–94.
the highlands of Papua New Guinea and its effect
on worm burdens of sheep. Science in New Guinea
24, 11–22.
Owen, I.L. and Awui C. 2000. Long-term Performance of
Priangan Sheep Under Intensive Management in the
Dry Lowlands of Papua New Guinea. Technical Report
20/1, December 2000. Department of Agriculture
and Livestock, Port Moresby. 24 pp.
Internal parasites of small ruminants in Papua New Guinea

248
15. Internal parasites of small ruminants in Nepal
B.R. Joshi

Introduction
Small ruminants are an important source of cash The national small ruminant population is mainly
generation and livelihood for resource-poor farming comprised of indigenous sheep and goat breeds,
communities in Nepal. The livestock sector contributes each found in a particular region of the country
about 31% of Nepal’s gross domestic product and small (Table 15.2). Management and production systems
ruminants alone comprise roughly 12% (LMP 1993, for small ruminants in Nepal have been described
APP 1995). The 6.61 million goats and 0.84 million in detail by Ghimire (1992).
sheep in the country (FAOSTAT 2002) are reared under
Diseases and parasites are regarded by farmers as the
either sedentary or migratory management systems.
most important constraints to small ruminant productivity
Migratory management is used for about 65% of sheep
in Nepal and this view has been supported by various
and about 35% of goats (LMP 1993) in the northern
studies. Lohani and Rasali (1993/95) calculated the
districts of Nepal, adjoining the southern flank of the
economic loss caused by animal diseases, based on
Himalayas, while sedentary management is used in
the rest of the country. Goats are primarily reared for
meat and manure and are regarded by farmers as the Table 15.1 Distribution and importance of small
second most important animal species for generating ruminants in different regions of Nepal
cash income (Gatenby et al. 1990). Sheep are kept Population distribution Terai Hills Mountains
for wool, meat and manure. In the eastern region of the
Goat population (in ‘000) 1828 3396 855
country about 80–85% of farming families are involved
Sheep population (in ‘000) 122 385 361
in sedentary goat management (Gatenby et al. 1990).
Percentage of households
However, on average, the percentage of households
keeping goats 46.8 54.2 55.5
involved in sheep and goat rearing varied between 46
Percentage of households
and 55%, depending upon the region of the country,
keeping sheep 1.8 4.2 6.5
increasing from the low terai regions to the mountain
Data from: Livestock Master Plan (1993), Statistical Information on
regions (Table 15.1). Nepalese Agriculture 1997/98 and Agriculture Perspective Plan (1995).

249
 Table 15.2 Distribution and management of sheep and goat breeds in Nepal

Species Breed % Total Region Altitude (m) Climate Management

Goat Chyangra 6 Mountain >2500 Cool temperate Sedentary/migratory

Sinhal 35 Mountain >2500 Cool temperate Migratory
Khari 50 Hills 300–2500 Warm temperate Sedentary
Terai 9 Terai <300 Subtropical/tropical Sedentary
Sheep Bhyanglung 4 Mountain >2500 Cool temperate Sedentary/migratory
Baruwal 41 Mountain >2500 Cool temperate Migratory
Kage 43 Hills 300–2500 Warm temperate Sedentary
Lampuchhre 12 Terai <300 Subtropical/tropical Migratory
(Adapted from: Wilson 1995)

survey data from six districts, to be about 885 million Worm species
rupees annually, equivalent to 17.7 million USD
in 1995. In sheep and goats, losses from parasitic A detailed survey of the worms of small ruminants in
diseases (including flukes, gastrointestinal worms and Nepal (Joshi 1997) gave similar findings (Table 15.3)
tapeworms) have been estimated at 80% of the total to earlier studies at the generic level (Singh et al. 1973,
losses from disease; roughly 1.5 million USD (sheep) Morel 1985, Thakur and Thakuri 1992, Jha et al. 1993)
and 0.25 million USD (goats). A later study reported except that Nematodirus was not recorded in this study.
Internal parasites of small ruminants in Nepal

that the annual loss from parasitic gastroenteritis alone As well as the worms listed in Table 15.3, some
would be about 9.2 million USD (Joshi 1996). These uncommon parasites have also been recorded in sheep
estimates may vary but together they indicate the and goats in Nepal, namely Eurytrema cladorchis
national importance of this problem. (Mahato 1987) and Dinobdella ferox (Mahato et al.
1989). The presence of Fasciola gigantica, Fasciola
This chapter collates information on gastrointestinal
hepatica and the intermediate form of Fasciola species
nematode infection of small ruminants in Nepal.
from the goats of Palpa district was reported by Lohani
Relevant production research is also included. It attempts
and Jaeckle (1981/82). Moniezia, Stilesia, Coenurus
to include not only the published literature but also cerebralis, Echinococcus granulosus, Fasciola gigantica
unpublished information presented in annual reports and Paramphistomum and lung worms were also
and similar documents. recorded in the study by Singh et al. (1973).

250
Table 15.3 Gastrointestinal parasite species Prevalence and impact of worms
of small ruminants rared under Jha et al. (1993) analysed the autopsy records of 266
sedentary and migratory goats from Pakhribas Agricultural Centre, Dhankuta and
management systems in Nepal attributed 6.4% of mortality in goats to gastrointestinal
Worm Sedentary Migratory nematodes and 3.7% and 1.9% mortality to fasciolosis
and paramphistomosis, respectively. In a retrospective
Haemonchus contortus * *
analysis of eight years data with 41,944 clinical cases
Trichostrongylus axei * *
also from the Pakhribas Agricultural Centre and seven
T. colubriformis * * hill districts in the eastern region, Chand Thakuri et al.
T. vitrinus * * (1994) found that the major clinical problems in goats
T. orientalis * * were caused by parasitic diseases which accounted for
Bunostomum trigonocephalum * * 74% of the total treated cases. These workers concluded
that infection by helminth parasites was a pressing
Cooperia curteici * *
constraint for improving the productivity of goats. Of
C. punctata * *
the 20,449 cases of helminth parasites recorded in
Oesophagostomum asperum * *
the hill districts, the proportions infected by liverfluke,
O. venulosum * * gastrointestinal nematodes and tapeworm were 34,
Trichuris ovis * * 65 and 1%, respectively.
Strongyloides papillosus * *
Later, a more detailed study was carried out in the
Teladorsagia circumcincta * * western hills of Nepal by Joshi (1995, 1998, 1999).
T. davtiani * Dung samples from sheep and goats of the village flocks
T. trifurcata * reared under migratory and sedentary management
Ostertagia leptospicularis * systems were analysed at monthly intervals with more
O. nianquingtanggulaensis *
than 4090 faecal samples collected over 12 months.
Prevalence of worm infection ranged between 60–100%
Grossospiculagia occidentalis *
in ewes, 7–97% in lambs, 15–100% in adult goats
Chabertia ovina *
and 6–100% in goat kids. Faecal egg counts were
Skrjabinema ovis * higher in sheep (in both adult and young age groups)
than in goats. Similarly, the faecal egg counts were
higher in sheep and goats raised under the sedentary
system than in those raised under the migratory one.

251
 Epidemiology Joshi (unpublished) studied the development and survival
of H. contortus larvae at different altitudes in the hill
Thakur and Chand Thakuri (1992) reported that region and recorded that eggs and larvae survived
June–August was the main season for worm infection considerably longer at the lower altitudes and during
in goats in the eastern hills of Nepal and that there was the cold winter months. Eggs became larvae within
100% infection during the month of July. Further, Joshi one week from May to October at both altitudes but
(1995) studied various aspects of the epidemiology needed six to eight weeks during January and February.
of worms in sheep and goats from sedentary and The longest survival was recorded for the larvae put
migratory management systems in the western hills of
on the pasture during the month of May at the lower
Nepal. The rate of pasture infection was determined by
altitudes (26 weeks) and during April at the higher
grazing naïve (born and reared indoor) tracer lambs
altitudes (24 weeks).
with the flocks for successive months of the year and then
rearing them indoors before slaughter. It was recorded Joshi (unpublished) also studied the development
that the peak of pasture infection was during the wet of H. contortus derived from sheep and goats in
summer months (June–September), and that it gradually the corresponding and alternate host species. It was
declined during the drier winter months. The highest recorded that fecundity of an isolate of H. contortus
level of infection was acquired by the tracer lambs derived from goats was higher in both sheep and
during the month of June in both management systems. goats (Table 15.4). In particular, the percentage of
Thus infection of animals was closely related to the gravid female worms at 28 days post-infection was
development of larvae on the pasture and their intake higher with the goat strain in both sheep and goat
by grazing animals. The proportion of hypobiotic larvae species (68 and 90%). However, with the sheep strain,
in the lambs grazed with the sedentary flocks was low the percentage of gravid female worms was higher
(5% during January and February) but high in the lambs
in goats than sheep (82 and 36%, respectively).
grazed with migratory flocks (60 and 70% during
Internal parasites of small ruminants in Nepal

September and August).

In the same study, evaluation of the grazing pasture for Table 15.4 Mean faecal egg counts (eggs per
its infectivity showed that high altitude pastures were gram) at 28 days post-infection in
heavily contaminated with nematode larvae. Larvae
lambs and kids infected with sheep
were recovered up to 4170 m above sea level. There
and goat strains of H. contortus
were distinct trends according to the altitude range.
At the lower altitudes (below 2300 m), Trichostrongylus Strain Lambs Kids
spp., Ostertagia spp. and Haemonchus contortus were
Sheep 400 ± 200 700 ± 100
all present, at 2300–4000 m, Trichostrongylus spp. and
Goat 2166 ± 548 2000 ± 1250
Ostertagia spp., and above 4000 m, only Ostertagia
spp. (Joshi 1996).

252
Peri-parturient egg rise had different trends in sedentary
and migratory management systems (Joshi, unpublished).
Sedentary ewes had a steady rise in egg count two
weeks post parturition, whereas the peri-parturient egg
rise trend was erratic in the migratory ewes. There was
no peri-parturient egg rise in the sedentary nannies
(in fact a decline was observed) but an increase was
observed in the migratory nannies. These trends are
difficult to explain, but might have been influenced by
the grazing management. The other factor might be
that all lambing and kidding were during the winter
months when it was dry and cold with low or no
possibility of infection from the pastures. These studies Goat housing with good ventilation, shelter and space
indicated that peri-parturient egg rise might be of for manure collection can be made out of local material.
epidemiological significance in sheep kept under (G.D. Gray)
migratory management. normal farming management). No supplementation
Feeding of rice straw, which plays such an important was provided. Weight gain and faecal egg counts
role in the transmission of Fasciola to stall-fed buffaloes were monitored for six months (in sedentary animals)
(Joshi 1987), does not seem to have any role in the to one year (in migratory animals). The results of the
epidemiology of gastrointestinal nematode infection study show a significant effect of worms on the weight
of small ruminants. gain of the animals (Table 15.5).
The performance of migratory animals after a single
Controlling worms and drenching was studied by Joshi and Joshi (1999).
Weight gain was encouraging but the study was
improving productivity conducted for only a short period (up to May).
Shrestha et al. (1990) demonstrated significant
Commercial anthelmintic treatment
improvement in the growth rate of goats treated with
Joshi (1996a, 1996b, 1999) monitored the effect anthelmintics and supplemented with maize grain
of worms on small ruminant productivity managed (@10 g/kg body weight) over the untreated controls.
under sedentary and migratory management. A single anthelmintic treatment increased the daily weight
A group of animals was maintained worm free by gain from 28 g/day to 47 g/ day in the yearling male
regular anthelmintic treatment and managed together goats and was profitable, whereas supplementation
with untreated pair-matched control animals (under without anthelmintic was not economically profitable.

253
 Table 15.5 Weight gain responses of migratory and sedentary sheep and goats following worm
control using anthelmintics.
System Species Groups Total weight gain (kg) Weight gain/day (g)

Migratory Sheep Treated 11.0 30

Control 5.1 14
Goats Treated 9.1 25
Control 5.0 14
Sedentary Sheep
(during summer) Treated 3.5 19
Control 1.6 9
Sheep
(during winter) Treated 5.5 30
Control 3.4 19
Goats Treated 9.0 43
Control 3.7 18

This study, however, did not indicate the level ■ anthelmintic and concentrate fed, 37 g/day
of infection, management system or the time
■ anthelmintic plus concentrate and mineral
and duration of the study.
supplement, 43 g/day.
Internal parasites of small ruminants in Nepal

Nutrition It was interesting to note that, in addition to body

weight gain, the age of first kidding, kidding–conception
The effect of anthelmintic treatment during the summer interval, kidding interval and kidding percentage
monsoon months and/or nutrition was studied in village were also significantly reduced in the treated and
goat flocks (Kadariya and Joshi 1994). Anthelmintic supplemented groups. However, there was no effect
treatment and better nutrition significantly improved on twinning percentage. Among the untreated
mean weight gain per day as follows: animals about 10% mortality was attributed to
■ controls, 26 g/day parasitic gastroenteritis.

■ anthelmintic only, 30 g/day

254
In a similar study, Gurung et al. (1994) supplemented
feed with mustard cake and maize and compared the
weight gain of anthelmintic treated, and untreated,
castrated male goat kids. In the anthelmintic treated
goats, growth rate was 59% higher than in the untreated
groups. Mustard cake alone also significantly improved
growth: ‘Despite infection of gastrointestinal nematodes,
supplementation of mustard cake as a protein source
increased the growth rate of fattening goats in the
undrenched group’. There was no consideration of the
level of infection and its dynamics after the interventions.
McTaggart and Wilkinson (1981, 1982) studied the
growth response of terai goats with ad lib berseem
(leguminous forage) feeding and reported a daily
weight gain of 98 g. This dropped to 29 g/day
with grazing on natural pasture only. Anthelmintic
treatment contributed marginally to weight gain,
but it was also shown that berseem feeding resulted
in self-cure among untreated kids.
The effect of experimental infection with Fasciola Making compost from manure provides fertiliser and
gigantica and different levels of nutrition on Nepalese prevents contamination of pasture with worm eggs
hill goats was studied by Pakhrin et al. (2000). Although and larvae. (D. Pezo)
the recovery of flukes was higher (55 flukes) in the
concentrate-fed goats than those grazing on fodder Plants as anthelmintics
trees (1 fluke), the concentrate-fed ones had a higher
daily weight gain (61 g/day compared to 39 g/day) Some plant products have been evaluated for their
and the condition of the liver was normal. Thus, anthelmintic properties in Nepal, for example, Euphorbia
improved nutrition reduced the pathogenicity of the roulina has been tested against Ascaris suum of pigs
parasites. Though not conclusive, fodder trees appear and has been recorded to be very effective (Mahato and
to reduce fluke establishment in goats and it may be Rai 1988). Other plants (roots of Imparata cylindrica
possible that some tree fodder has similar effects on the and Morus indica roxburgii, bulb of Allium satirum, seeds
establishment of gastrointestinal nematodes. This needs of Litsea cubeba) were evaluated against buffalo
to be further investigated. ascariasis (Neoascaris vitulorum) and found to expel

255
 adult worms but were not comparable to commercial
anthelmintics (LAC Annual Report 1987/88). These
studies (and those mentioned at the end of the previous
section) indicate the potential of some plant products
to be used as anthelmintics but more detailed studies
are needed.
The only study on goat worms used a commercially
available Indian herbal product — Krimos Powder
(Bharatiya Booti Bhawan). This was found to be
ineffective compared with fenbendazole and
mebendazole (Thakuri et al. 1994). Farmers have
reported the use of various plants (bark of Melia Accurate weighing scales at markets ensures farmers
azedarach, buds of Dhurteli, buds of Ainselu and juice are rewarded for increased body size. (G.D. Gray)
of ginger) against worm infection of farm animals (Joshi
et al. 1997) but the anthelmintic efficacy of these plants
■ migratory Baruwal sheep and Sinhal goats
has not been scientifically evaluated.
in the eastern region of Nepal (Shrestha 1997)

Genetic resistance ■ migratory Sinhal goats in the Larnali region

(Upreti and Mahato 1995)
The resistance of three indigenous sheep breeds (Kage,
Baruwal and Lampuchhre) to artificial H. contortus ■ sedentary Chyangra goats at the Pakhribas
infection was evaluated by measuring faecal egg counts Agricultural Centre (Shrestha et al. 1992)
and recovering worms (Joshi 1995). Kage sheep were
Internal parasites of small ruminants in Nepal

■ Kage sheep and local goats at the Institute

most resistant to the challenge infection of H. contortus of Agricultural and Animal Science farm in
and Baruwal were most susceptible. Chitwan (Dhakal et al. 1985).

Production performance of different breeds When the performance of migratory Baruwal sheep was
compared with that of their crosses with Polwarth and
The performance of several indigenous sheep and Border Leicester it was found that most reproduction
goat breeds in different regions of Nepal has been parameters were comparable between the native
studied as follows: sheep and the exotic crossbreeds. However, wool
■ migratory Baruwal sheep in the Gandaki production in the crossbreeds was significantly higher
zone (Karki 1985) than in the native animals. Notably though, survival
of native sheep in the migratory management system

256
was considerably higher than for the cross-breeds,
probably because of the better flocking behaviour of
native sheep (Dhaubadel and Karki 1996, Rasali 1995).
When the performance of sedentary native Khari goats
was compared with that of their crosses with exotic
breeds Jamunapari, Beetal and Barbari in the eastern
region of the country, the native goats were found to
Grazing fallow rice paddies makes effective use of
be more profitable (Oli 1987). Later, at Bandipur goat
stubble and weeds and provides manure. (G.D. Gray)
farm, the performance of seven breeds — two native
(Sinhal and Khari), two exotic (Jamunapari and Barbari)
2) treating adult animals, especially lactating ewes,
and three crosses between local and exotic breeds
at the beginning of dry winter to avoid winter
(Khari x Jamunapari, Khari x Barbari and Khari x Kiko)
weight loss
— was compared (Upreti and Khanal 1997). Results
clearly showed that both native breeds were more 3) using anthelmintics in a feed-based formulation
profitable than the exotic breeds or their crosses. for sedentary sheep
4) treating goats, both young and adults,
Worm control strategy during wet summer months
5) studying and evaluating plant products with
The epidemiological studies in the mid-1990s were
helpful in designing control strategies for both sedentary anthelmintic properties and using them at the
and migratory systems of small ruminant management field level
in Nepal. Until then, methods of parasite control 6) stall feeding, particularly during the wet season
were based on anthelmintic drenching without any
consideration of season. Drenching was usually
conducted during the winter months or when the Conclusions
animals were clinically sick. Joshi (1995) recommended
This review will need to be updated as further
the strategic use of anthelmintics for better control of
information becomes available. Although it is difficult
endoparasites. Pasture management techniques for worm
to draw conclusions, the findings of many of the papers
control are not applicable under Nepalese conditions.
reviewed can be summarised as:
The strategy suggested required:
■ goat and sheep rearing is an important aspect
1) protecting vulnerable animals, particularly young of the Nepali farming system and provides an
animals, from heavy challenge during the peak important source of cash income for most
transmission period (wet monsoon months) households in Nepal

257
 ■ animals are reared under traditional management ■ the availability of chemical anthelmintics could
systems — sedentary or migratory —without many be a problem in remote areas
external inputs
■ no information on anthelmintic resistance
■ gastrointestinal nematodes are an important is available.
constraint to increased sheep and goat
productivity under both sedentary and
migratory management systems Acknowledgments
■ infection of small ruminants with worms I would like to express my gratitude to Dr G. Douglas
is confined to the wet summer months Gray who advised, suggested, and supported the
carrying out of this review and to the International
■ increased productivity response to anthelmintic Fund for Agricultural Development (IFAD) for funding
treatment is encouraging support. I am also thankful to Mr Milan Bijukchhe and
■ there is a considerable potential to improve Mr O.B. Gurung, who helped me to collect literature
animal productivity by improving management and photocopy it and library staff of various libraries
of health and nutrition for their help and support.

■ some plants have been shown to possess

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Appendix – list of authors

M. Adnan Binh Van Dinh

Veterinary Research Institute Goat and Rabbit Research Centre
Malaysia National Institute of Animal Husbandry
[email protected] Vietnam
[email protected]
A.M.P. Alo
PCARRD D. Gauchan
Philippines Outreach Research Division
[email protected] Nepal Agricultural Research Council (NARC)
Nepal
R.K. Bain [email protected]
Inverness
Scotland, UK G.D. Gray
[email protected] ILRI
Philippines
R.L. Baker [email protected]
ILRI
Kenya G.M. Hood
[email protected] ILRI
Philippines
P. Chandrawathani [email protected]
Veterinary Research Institute
Malaysia B.R. Joshi
[email protected] Animal Health Division
Nepal Agriculture Research Council (NARC)
T.S. Cheah Nepal.
Veterinary Research Institute [email protected]
Malaysia
[email protected]

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 S. Kochapakdee Sorn San
Faculty of Natural Resources National Animal Health and
Prince of Songkla University Production Investigation Centre
Thailand Ministry of Agriculture
[email protected] Cambodia
[email protected]
Nguyen Duy Ly
Goat and Rabbit Research Centre R.A. Sani
National institute of Animal Husbandry Faculty of Veterinary Medicine
Vietnam Universiti Putra Malaysia
[email protected] Malaysia
[email protected]
R.S. McLeod
eSYS Development T. Sartika
Australia Indonesian Research Institute of Animal Production
[email protected] Indonesia

P. Manueli Subandriyo
Secretariat of the Pacific Community Indonesian Research Institute of Animal Production
Fiji Indonesia
[email protected] [email protected]

V. Phimphachanhvongsod Suhardono
National Agriculture and Forestry Research Institute Research Institute for Veterinary Science
Lao PDR Indonesia
[email protected] [email protected]

A.R. Quartermain E.C. Villar

NARI PCARRD
Papua New Guinea Philippines
[email protected] [email protected]

S. Saithanoo C.A.T. Yee

ILRI ILRI
Philippines Philippines
[email protected] [email protected]

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 Worm Control for Small Ruminants in Tropical Asia

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Worm Control for Small Ruminants in Tropical Asia ACIAR