BENTHIC FORAMINIFERA

A. J. Gooday, Southampton Oceanography Centre, the-world expedition of 1872–76, still underpins our
Southampton, UK knowledge of the group. Later biological expeditions
Copyright & 2001 Elsevier Ltd. added to this knowledge. For much of the 1900s,
however, the study of deep-sea foraminifera was
This article is reproduced from the 1st edition of Encyclopedia of Ocean conducted largely by geologists, notably J.A. Cush-
Sciences, volume 1, pp 274–286, & 2001, Elsevier Ltd.
man, F.B. Phleger, and their students, who amassed
an extensive literature dealing with the taxonomy
Introduction and distribution of calcareous and other hard-shelled
taxa. In recent decades, the emphasis has shifted
Foraminifera are enormously successful organisms toward the use of benthic species in paleoceano-
and a dominant deep-sea life form. These amoeboid graphic reconstructions. Interest in deep-sea for-
protists are characterized by a netlike (granulor- aminifera has also increased among biologists since
eticulate) system of pseudopodia and a life cycle that the 1970s, stimulated in part by the description of
is often complex but typically involves an alternation the Komokiacea, a superfamily of delicate, soft-
of sexual and asexual generations. The most obvious shelled foraminifera, by O.S. Tendal and R.R.
characteristic of foraminifera is the presence of a Hessler. This exclusively deep-sea taxon is a domin-
shell or ‘test’ that largely encloses the cytoplasmic ant component of the macrofauna in some abyssal
body and is composed of one or more chambers. In regions.
some groups, the test is constructed from foreign
particles (e.g., mineral grains, sponge spicules, shells
of other foraminifera) stuck together (‘agglutinated’)
by an organic or calcareous/organic cement. In oth- Morphological and Taxonomic
ers, it is composed of calcium carbonate (usually Diversity
calcite, occasionally aragonite) or organic material
Foraminifera are relatively large protists. Their tests
secreted by the organism itself.
range from simple agglutinated spheres a few tens of
Although the test forms the basis of foraminiferal
micrometers in diameter to those of giant tubular
classification, and is the only structure to survive
species that reach lengths of 10 cm or more. How-
fossilization, the cell body is equally remarkable and
ever, most are a few hundred micrometers in size.
important. It gives rise to the complex, highly mo-
They exhibit an extraordinary range of morphologies
bile, and pervasive network of granuloreticulose
(Figures 1 and 2), including spheres, flasks, various
pseudopodia. These versatile organelles perform a
types of branched or unbranched tubes, and cham-
variety of functions (locomotion, food gathering, test
bers arranged in linear, biserial, triserial, or coiled
construction, and respiration) that are probably
(spiral) patterns. In most species, the test has an
fundamental to the ecological success of foraminifera
aperture that assumes a variety of forms and is
in marine environments.
sometimes associated with a toothlike structure. The
As well as being an important component of
komokiaceans display morphologies not tradition-
modern deep-sea communities, foraminifera have an
ally associated with the foraminifera. The test forms
outstandingly good fossil record and are studied
a treelike, bushlike, spherical, or lumpish body that
intensively by geologists. Much of their research uses
consists of a complex system of fine, branching
knowledge of modern faunas to interpret fossil
tubules (Figure 2A–C).
assemblages. The study of deep-sea benthic for-
The foraminifera (variously regarded as a sub-
aminifera, therefore, lies at the interface between
phylum, class, or order) are highly diverse with
biology and geology. This articles addresses both
around 900 living genera and an estimated 10 000
these facets.
described living species, in addition to large numbers
of fossil taxa. Foraminiferal taxonomy is based very
largely on test characteristics. Organic, agglutinated,
History of Study
and different kinds of calcareous wall structure serve
Benthic foraminifera attracted the attention of some to distinguish the main groupings (orders or sub-
pioneer deep-sea biologists in the late 1860s. The orders). At lower taxonomic levels, the nature and
monograph of H.B. Brady, published in 1884 and position of the aperture and the number, shape, and
based on material collected in the Challenger round- arrangement of the chambers are important.

336
 BENTHIC FORAMINIFERA 337

)A( (B)

(C) (D) (E)

(F) (G) (H)

Figure 1 Scanning electron micrographs of selected deep-sea foraminifera (maximum dimensions are given in parentheses).
(A) Epistominella exigua; 4850 m water depth, Porcupine Abyssal Plain, NE Atlantic (190 mm). (B) Nonionella iridea; 1345 m depth,
Porcupine Seabight, NE Atlantic (110 mm). (C) Nonionella stella; 550 m depth, Santa Barbara Basin, California Borderland (220 mm).
(D) Brizalina tumida; 550 m depth, Santa Barbara Basin, California Borderland (680 mm). (E) Melonis barleaanum; 1345 m depth,
Porcupine Seabight, NE Atlantic (450 mm). (F) Hormosina sp., 4495 m depth, Porcupine Abyssal Plain (1.5 mm). (G) Pyrgoella
sp.; 4550 m depth, foothills of Mid-Atlantic Ridge (620 mm). (H) Technitella legumen; 997–1037 m depth, NW African margin (8 mm).
(A)–(E) and (G) have calcareous tests, (F) and (H) have agglutinated tests. (C) and (D), photographs courtesy of Joan Bernhard.

Methodology use of coring devices. The two most popular corers

used in the deep sea are the box corer, which obtains
Qualitative deep-sea samples for foraminiferal stud- a large (e.g., 0.25 m2) sample, and the multiple corer,
ies are collected using nets (e.g., trawls) that are which collects simultaneously a battery of up to 12
dragged across the seafloor. Much of the Challenger smaller cores. The main advantage of the multiple
material studied by Brady was collected in this way. corer is that it obtains the sediment–water interface
Modern quantitative studies, however, require the in a virtually undisturbed condition.
338 BENTHIC FORAMINIFERA

)A( (B)

(C) (D) (E)

(F)

(H)

(G)

(I) (J)
(K)

Figure 2 Light micrographs of deep-sea foraminifera (maximum dimensions are given in parentheses). (A) Species of Lana in which
pad-like test consists of tightly meshed system of fine tubules; 5432 m water depth, Great Meteor East region, NE Atlantic (7.4 mm).
(B) Septuma sp.; same locality (2 mm). (C) Edgertonia mudball; same locality (3.8 mm). (D) Hormosina globulifera; 4004 m depth, NW
African margin (6.4 mm). (E) Rhabdammina parabyssorum; 3392 m depth, Oman margin, NW Arabian Sea (18 mm). (F) Leptohalysis
sp.; 3400 m depth, Oman margin, NW Arabian Sea (520 mm). (G) Minute species of Hyperammina; 3400 m depth, Oman margin, NW
Arabian Sea (400 mm). (H) Lenticularia sp.; 997–1037 m depth, NW African margin (2.5 mm). (I, J) Biloculinella sp.; 4004 m depth, NW
African margin (3 mm). (K) Spherical allogromiid; 3400 m depth, Oman margin, NW Arabian Sea (105 mm). Specimens illustrated in
(A)–(G) have agglutinated tests, in (H)–(J) calcareous tests and in (K) an organic test. (A)–(C) belong to the superfamily Komokiacea.

Foraminifera are extracted from sieved sediment rose Bengal solution. This colors the cytoplasm red
residues. Studies are often based on dried residues and is most obvious when residues are examined in
and concern ‘total’ assemblages (i.e. including both water. Stained assemblages provide a snapshot of the
live and dead individuals). To distinguish individuals foraminifera that were living when the samples were
that were living at the time of collection from dead collected. Since the live assemblage varies in both
tests, it is necessary to preserve sediment samples in time and space, it is also instructive to examine the
either alcohol or formalin and then stain them with dead assemblage that provides an averaged view of
 BENTHIC FORAMINIFERA 339

the foraminiferal fauna. Deep-sea foraminiferal In the central North Pacific, for example, for-
assemblages are typically very diverse and therefore aminifera (mainly komokiaceans) outnumber all
faunal data are often condensed mathematically by metazoans combined by at least an order of mag-
using multivariate approaches such as principal nitude. A few species are large enough to be easily
components or factor analysis. visible to the unaided eye and constitute part of the
The mesh size of the sieve strongly influences the megafauna. These include the tubular species
species composition of the foraminiferal assemblage Bathysiphon filiformis, which is sometimes abun-
retained. Most deep-sea studies have been based on dant on continental slopes (Figure 3). Some xeno-
>63 mm, 125 mm, 150 mm, 250 mm, or even 500 mm phyophores, agglutinated protists that are probably
meshes. In recent years, the use of a fine 63 mm mesh closely related to the foraminifera, are even larger
has become more prevalent with the realization that (up to 24 cm maximum dimension!). These giant
some small but important species are not adequately protists may dominate the megafauna in regions of
retained by coarser sieves. However, the additional sloped topography (e.g., seamounts) or high surface
information gained by examining fine fractions must productivity. In well-oxygenated areas of the deep-
be weighed against the considerable time and effort seafloor, foraminiferal assemblages are very species
required to sort foraminifera from them. rich, with well over 100 species occurring in rela-
tively small volumes of surface sediment (Figure 4).
Many are undescribed delicate, soft-shelled forms.
Ecology There is an urgent need to describe at least some of
these species as a step toward estimating global
Abundance and Diversity
levels of deep-sea species diversity. The common
Foraminifera typically make up >50% of the soft- species are often widely distributed, particularly at
bottom, deep-sea meiofauna (Table 1). They are abyssal depths, although endemic species un-
also often a major component of the macrofauna. doubtedly also occur.

Table 1 The percentage contribution of foraminifera to the deep-sea meiofauna at sites where bottom water is well oxygenated

Area Depth (m) Percentage of foraminifera Number of samples

NW Atlantic
Off North Carolina 500–2500 11.0–90.4 14
Off North Carolina 400–4000 7.6–85.9 28
Off Martha’s Vineyard 146–567 3.4–10.6 4
NE Atlantic
Porcupine Seabight 1345 47.0–59.2 8
Porcupine Abyssal Plaina 4850 61.8–76.3 3
Madeira Abyssal Plaina 4950 61.4–76.1 3
Cape Verde Abyssal Plaina 4550 70.2 1
Off Mauretania 250–4250 26
4–27
461N, 16–171W 4000–4800 0.5–8.3 9
Indian Ocean
NW Arabian Seab 3350 54.4 1
Pacific
Western Pacific 2000–6000 36.0–69.3 11
Central North Pacific 5821–5874 49.5 2
Arctic 1000–2600 14.5–84.1 74
Southern Ocean 1661–1680 2.2–23.7 2

a
Data from Gooday AJ (1996) Epifaunal and shallow infaunal foraminiferal communities at three abyssal NE Atlantic sites subject to
differing phytodetritus input regimes. Deep-Sea Research I 43: 1395–1421.
b
Data from Gooday AJ, Bernhard JM, Levin LA and Suhr SB (2000) Foraminifera in the Arabian Sea oxygen minimum zone and other
oxygen-deficient settings: taxonomic composition, diversity, and relation to metazoan faunas. Deep-Sea Research II 47: 25–54.
Based on Gooday AJ (1986) Meiofaunal foraminiferans from the bathyal Porcupine Seabight (northeast Atlantic): size structure,
standing stock, taxonomic composition, species diversity and vertical distribution in the sediment. Deep-Sea Research 35: 1345–
1373; with permission from Elsevier Science.
340 BENTHIC FORAMINIFERA

the sea floor for periods of months. They include

various undescribed matlike taxa and branched
tubular forms, as well as a variety of small coiled
agglutinated species (many in the superfamily Tro-
chamminacea), and calcareous forms.

Role in Benthic Communities

The abundance of foraminifera suggests that they play
an important ecological role in deep-sea communities,
although many aspects of this role remain poorly
understood. One of the defining features of these
protists, their highly mobile and pervasive pseudopo-
dial net, enables them to gather food particles very
efficiently. As a group, foraminifera exhibit a wide
variety of trophic mechanisms (e.g., suspension feed-
ing, deposit feeding, parasitism, symbiosis) and diets
(herbivory, carnivory, detritus feeding, use of dis-
solved organic matter). Many deep-sea species appear
to feed at a low trophic level on organic detritus,
sediment particles, and bacteria. Foraminifera are
prey, in turn, for specialist deep-sea predators (sca-
phopod mollusks and certain asellote isopods), and
also ingested (probably incidentally) in large numbers
by surface deposit feeders such as holothurians. They
may therefore provide a link between lower and
higher levels of deep-sea food webs.
Figure 3 Bathysiphon filiformis, a large tubular agglutinated Some deep-sea foraminifera exhibit opportunistic
foraminifer, photographed from the Johnson Sealink submersible
characteristics – rapid reproduction and population
on the North Carolina continental slope (850 m water depth). The
tubes reach a maximum length of about 10 cm. (Photograph growth responses to episodic food inputs. Well-
courtesy of Lisa Levin.) known examples are Epistominella exigua, Alaba-
minella weddellensis and Eponides pusillus. These
small (generally o200 mm), calcareous species feed
120 on fresh algal detritus (‘phytodetritus’) that sinks
100 through the water column to the deep-ocean floor
Numbers per 25 cm 2

after the spring bloom (a seasonal burst of phyto-

80 plankton primary production that occurs most
60 strongly in temperate latitudes). Utilizing energy
from this labile food source, they reproduce rapidly
40 to build up large populations that then decline when
20 their ephemeral food source has been consumed.
Moreover, certain large foraminifera can reduce
0 their metabolism or consume cytoplasmic reserves
Species ordered by rank
when food is scarce, and then rapidly increase their
Figure 4 Deep-sea foraminiferal diversity: all species from a metabolic rate when food again becomes available.
single multiple corer sample collected at the Porcupine Abyssal These characteristics, together with the sheer abun-
Plain, NE Atlantic (4850 m water depth), ranked by abundance. dance of foraminifera, suggest that their role in the
Each bar represents one ‘live’ (rose Bengal-stained) species. The
sample was 25.5 cm2 surface area, 0–1 cm depth, and sieved on cycling of organic carbon on the deep-seafloor is very
a 63 mm mesh sieve. It contained 705 ‘live’ specimens and 130 significant.
species. The tests of large foraminifera are an important
source of environmental heterogeneity in the deep
Foraminifera are also a dominant constituent of sea, providing habitats and attachment substrates for
deep-sea hard-substrate communities. Dense popu- other foraminifera and metazoans. Mobile infaunal
lations encrust the surfaces of manganese nodules as species bioturbate the sediment as they move through
well as experimental settlement plates deployed on it. Conversely, the pseudopodial systems of
 BENTHIC FORAMINIFERA 341

foraminifera may help to bind together and stabilize down to 10 cm or more (Figure 6). A few deep-water
deep-sea sediments, although this has not yet been foraminifera, including the well-known calcareous
clearly demonstrated. species Cibicidoides wuellerstorfi, occur on hard
substrates (e.g., stones) that are raised above the
sediment–water interface (elevated epifaunal micro-
Microhabitats and Temporal Variability
habitat). There is a general relation between test
Like many smaller organisms, foraminifera reside morphotypes and microhabitat preferences. Epifaunal
above, on and within deep-sea sediments. Various and shallow infaunal species are often trochospiral
factors influence their overall distribution pattern with large pores opening on the spiral side of the test;
within the sediment profile, but food availability and infaunal species tend to be planispiral, spherical, or
geochemical (redox) gradients are probably the most ovate with small, evenly distributed pores. It is im-
important. In oligotrophic regions, the flux of organic portant to appreciate that foraminiferal microhabitats
matter (food) to the seafloor is low and most for- are by no means fixed. They may vary between sites
aminifera live on or near the sediment surface where and over time and are modified by the burrowing
food is concentrated. At the other extreme, in eu- activities of macrofauna. Foraminiferal microhabitats
trophic regions, the high organic-matter flux causes should therefore be regarded as dynamic rather than
pore water oxygen concentrations to decrease rapidly static. This tendency is most pronounced in shallow-
with depth into the sediment, restricting access to the water settings where environmental conditions are
deeper layers to those species that can tolerate low more changeable and macrofaunal activity is more
oxygen levels. Foraminifera penetrate most deeply intense than in the deep sea.
into the sediment where organic inputs are of inter- The microhabitats occupied by species reflect the
mediate intensity and the availability of food and same factors that constrain the overall distribution
oxygen within the sediment is well balanced. patterns of foraminifera within the sediment. Epi-
Underlying these patterns are the distributions of faunal and shallow infaunal species cannot tolerate
individual species. Foraminifera occupy more or less low oxygen concentrations and also require a diet of
distinct zones or microenvironments (‘microhabitats’). relatively fresh organic matter. Deep infaunal for-
For descriptive purposes, it is useful to recognize a aminifera are less opportunistic but are more tolerant
number of different microhabitats: epifaunal and of oxygen depletion than are species living close to
shallow infaunal for species living close to the sedi- the sediment–water interface (Figure 6). It has been
ment surface (upper 2 cm); intermediate infaunal for suggested that species of genera such as Globobuli-
species living between about 1 cm and 4 cm (Figure 5); mina may consume either sulfate-reducing bacteria
and deep infaunal for species that occur at depths or labile organic matter released by the metabolic

Number of specimens
0 20 40 0 20 0 10
0
1
2
3
Depth in sediment (cm)

4
(A) (B) (C)
5

0 5 0 5 10 5
0
1
2
3
4
5 (D) (E) (F)

Figure 5 Vertical distribution patterns within the top 5 cm of sediment of common foraminiferal species (‘live’, rose Bengal-stained
specimens) in the Porcupine Seabight, NW Atlantic (511360 N, 131000 W; 1345 m water depth). Based on 463 mm sieve fraction. (A)
Ovammina sp. (mean of 20 samples). (B) Nonionella iridea (20 samples). (C) Leptohalysis aff. catenata (7 samples). (D) Melonis
barleeanum (9 samples). (E) Haplophragmoides bradyi (19 samples). (F) ‘Turritellella’ laevigata (21 samples). (Amended and
reprinted from Gooday AJ (1986) Meiofaunal foraminiferans from the bathyal Porcupine Seabight (northeast Atlantic): size structure,
standing stock, taxonomic composition, species diversity and vertical distribution in the sediment. Deep-Sea Research 35: 1345–
1373; permission from Elsevier Science.)
342 BENTHIC FORAMINIFERA

_1
Oxygen (µmol l )
0 100 200 300 400 500 0 50 100 150 200 250
0 0 0 10 20 30 40 50
1 0.25
1

Depth in sediment (cm)

2 2 1.25
2.25
3 3
4 3.25
4
4.25
5 5
6 5.25
6
6.25
7 7
7.25
8 8
9 _1 8.25
9
Nitrate (µmol l )
10 9.25
10
Number of stained 0 20 40 60 80100120140160 Intermediate and
(A) foraminifera (B) (C) deep infauna, number of specimens

Figure 6 Vertical distribution of (A) total ‘live’ (rose Bengal-stained) foraminifera), (B) pore water oxygen and nitrate concentrations,
and (C) intermediate and deep infaunal foraminiferal species within the top 10 cm of sediment on the north-west African margin
(21128.80 N, 17157.20 W, 1195 m). All foraminiferal counts based on 4150 mm sieve fraction, standardized to a 34 cm3 volume. Species
are indicated as follows: Pullenia salisburyi (black), Melonis barleeanum (crossed pattern), Chilostomella oolina (honeycomb pattern),
Fursenkoina mexicana (grey), Globobulimina pyrula (diagonal lines), Bulimina marginata (large dotted pattern). (Adopted and
reprinted from Jorissen FJ, Wittling I, Peypouquet JP, Rabouille C and Relexans JC (1998) Live benthic foraminiferal faunas off Cape
Blanc, northwest Africa: community structure and microhabitats. Deep-Sea Research I 45: 2157–2158; with permission from Elsevier
Science.)

activities of these bacteria. These species move closer prevented the development of ideas. It is likely that
to the sediment surface as redox zones shift upward foraminiferal distribution patterns reflect a combin-
in the sediment under conditions of extreme oxygen ation of influences. The most important first-order
depletion. Although deep-infaunal foraminifera must factor is calcium carbonate dissolution. Above the
endure a harsh microenvironment, they are exposed carbonate compensation depth (CCD), faunas in-
to less pressure from predators and competitors than clude calcareous, agglutinated, and allogromiid taxa.
those occupying the more densely populated surface Below the CCD, calcareous species are almost en-
sediments. tirely absent. At oceanwide or basinwide scales, the
Deep-sea foraminifera may undergo temporal organic carbon flux to the seafloor (and its season-
fluctuations that reflect cycles of food and oxygen ality) and bottom-water hydrography appear to be
availability. Changes over seasonal timescales in the particularly important, both above and below the
abundance of species and entire assemblages have CCD.
been described in continental slope settings (Fig- Studies conducted in the 1950s and 1960s em-
ure 7). These changes are related to fluctuations in phasized bathymetry (water depth) as an important
pore water oxygen concentrations resulting from controlling factor. However, it soon became apparent
episodic (seasonal) organic matter inputs to the sea- that the bathymetric distribution of foraminiferal
floor. In some cases, the foraminifera migrate up and species beyond the shelf break is not consistent
down in the sediment, tracking critical oxygen levels geographically. Analyses of modern assemblages in
or redox fronts. Population fluctuations also occur in the North Atlantic, carried out in the 1970s, revealed
abyssal settings where food is a limiting ecological a much closer correlation between the distribution of
factor. In these cases, foraminiferal population dy- foraminiferal species and bottom-water masses. For
namics reflect the seasonal availability of phytode- example, Cibicidoides wuellerstorfi was linked to
tritus (‘food’). As a result of these temporal North Atlantic Deep Water (NADW) and Nuttallides
processes, living foraminifera sampled during one umbonifera to Antarctic Bottom Water (AABW). At
season often provide an incomplete view of the live this time, it was difficult to explain how slight
fauna as a whole. physical and chemical differences between water
masses could influence foraminiferal distributions.
However, recent work in the south-east Atlantic,
Environmental Controls on Foraminiferal
where hydrographic contrasts are strongly de-
Distributions
veloped, suggests that the distributions of certain
Our understanding of the factors that control the foraminiferal species are controlled in part by the
distribution of foraminifera on the deep-ocean floor lateral advection of water masses. In the case of
is very incomplete, yet lack of knowledge has not N. umboniferus there is good evidence that the main
 BENTHIC FORAMINIFERA 343

Oxygenated layer (cm)

0.5
1.0
1.5
2.0

living benthic foraminifera (per 10 cm )

2
2.5
(A)
3.0
3000 3.5
Total numbers of

2000

1000
(B)
0
34 5 8 1112 2 3 5 7 9 11 4 6 12 5 9 12
1991 1992 1993 1994

(C)

Others Bolivina spissa

Fursenkoina sp.1 Bulimina aculeata
Bolivina pacifica Globobulimina spp.
Textularia kattegatensis Chilostomella ovoidea
Uvigerina spp.

Figure 7 Seasonal changes over a 4-year period (March 1991 to December 1994) in (A) the thickness of the oxygenated layer, (B)
the total population density of live benthic foraminifera, and (C) the abundances of the most common species at a 1450 m deep site in
Sagami Bay, Japan. (Reprinted from Ohga T and Kitazato H (1997) Seasonal changes in bathyal foraminiferal populations in response
to the flux of organic matter (Sagami Bay, Japan). Terra Nova 9: 33–37; with permission from Blackwell Science Ltd.)

factor is the degree of undersaturation of the bottom Chilostomella ovoidea and Globobulimina affinis,
water in calcium carbonate. This abyssal species is predominate in organically enriched areas, e.g. be-
found typically in the carbonate-corrosive (and neath upwelling zones. Epifaunal species such as
highly oligotrophic) environment between the calcite Cibicidoides wuellerstorfi and Nuttallides umboni-
lysocline and the CCD, a zone that may coincide fera are common in oligotrophic areas, e.g. the cen-
approximately with AABW. Where water masses are tral oceanic abyss. In addition to flux intensity, the
more poorly delineated, as in the Indian and Pacific degree of seasonality of the food supply (i.e., whether
Oceans, links with faunal distributions are less clear. it is pulsed or continuous) is a significant factor.
During the past 15 years, attention has focused on Epistominella exigua, one of the opportunists that
the impact on foraminiferal ecology of organic exploit phytodetritus, occurs in relatively oligo-
matter fluxes to the seafloor. The abundance of dead trophic areas where phytodetritus is deposited
foraminiferal shells 4150 mm in size correlates well seasonally.
with flux values. There is also compelling evidence Recent analysis of a large dataset relating the
that the distributions of species and species associ- relative abundance of ‘live’ (stained) foraminiferal
ations are linked to flux intensity. Infaunal species, assemblages in the north-east Atlantic and Arctic
such as Melonis barleeanum, Uvigerina peregrina, Oceans to flux rates to the seafloor has provided a
344 BENTHIC FORAMINIFERA

quantitative framework for these observations. Al- the degradation of organic matter, concentrations of
though species are associated with a wide flux range, oxygen in bottom water and sediment pore water are
this range diminishes as a species become relatively inversely related to the organic flux derived from
more abundant and conditions become increasingly surface production. In the deep sea, persistent oxy-
optimum for it. When dominant occurrences (i.e., gen depletion (O2o1 ml l1) occurs at bathyal depths
where species represent a high percentages of the (o1000 m) in basins (e.g., on the California Bor-
fauna) are plotted against flux and water depth, derland) where circulation is restricted by a sill and
species fall into fields bounded by particular flux and in areas where high primary productivity resulting
depth values (Figure 8). Despite a good deal of from the upwelling of nutrient-rich water leads to the
overlap, it is possible to distinguish a series of development of an oxygen minimum zone (OMZ;
dominant species that succeed each other bath- e.g., north-west Arabian Sea and the Peru margin).
ymetrically on relatively eutrophic continental slopes Subsurface sediments also represent an oxygen-lim-
and other species that dominate on the more oligo- ited setting, although oxygen penetration is generally
trophic abyssal plains. greater in oligotrophic deep-sea sediments than in
Other environmental attributes undoubtedly fine-grained sediments on continental shelves.
modify the species composition of foraminiferal On the whole, foraminifera exhibit greater toler-
assemblages in the deep sea. Agglutinated species ance of oxygen deficiency than most metazoan taxa,
with tubular or spherical tests are found in areas although the degree of tolerance varies among species.
where the seafloor is periodically disturbed by strong Oxygen probably only becomes an important limiting
currents capable of eroding sediments. Forms pro- factor for foraminifera at concentrations well below
jecting into the water column may be abundant 1 ml l1. Some species are abundant at levels of 0.1 ml
where steady flow rates convey a continuous supply l1 or less. A few apparently live in permanently an-
of suspended food particles. Other species associ- oxic sediments, although anoxia sooner or later re-
ations may be linked to sedimentary characteristics. sults in death when accompanied by high
concentrations of hydrogen sulfide. Oxygen-deficient
areas are characterized by high foraminiferal densities
Low-Oxygen Environments
but low, sometimes very low (o10), species numbers.
Oxygen availability is a particularly important eco- This assemblage structure (high dominance, low spe-
logical parameter. Since oxygen is consumed during cies richness) arises because (i) low oxygen

20 0
0
10

30

30
1 Tetragonostomia rhombiformis
10

2 Nonion asterizans 1
3 Trifarina fornasinii
4 Rupertina stabilis
5 Bolivina albatrossi 2
100
Water depth (m)

4 5
1000 6
7 6 Sphaeroidina bulloides
7 Hoeglundina elegans
8 8 Pyrgo murrhina
9 Eponides tumidulus and
9
Stetsonia arctica
0.1 1 10 100
_ _
Flux of organic carbon (g m 2 y 1)

Figure 8 Dominant ‘live’ (rose Bengal-stained) occurrences of foraminiferal species in relation to water depth and flux or organic
carbon to seafloor in the North Atlantic from the Guinea Basin to the Arctic Ocean. Each open circle corresponds to a data point. The
polygonal areas indicate the combination of water depth and flux conditions under which nine different species are a dominant faunal
component. The diagonal lines indicate levels of primary production (10, 30, 100, 300 g m2 y1) that result in observed flux rates.
Based on 4250 mm sieve fraction plus 63–250 mm fraction from Guinea Basin and Arctic Ocean. (Reprinted from Altenbach AV,
Pflaumann U, Schiebel R et al. (1999) Scaling percentages and distribution patterns of benthic foraminifera with flux rates of organic
carbon. Journal of Foraminiferal Research 29: 173–185; with permission from The Cushman Foundation.)
 BENTHIC FORAMINIFERA 345

concentration acts as a filter that excludes non-toler- Textularia, Trochammina (both multilocular), Bath-
ant species and (ii) the tolerant species that do survive ysiphon, and Psammosphaera (both unilocular), are
are able to flourish because food is abundant and also abundant. However, miliolids, allogromiids, and
predation is reduced. Utrastructural studies of some other soft-shelled foraminifera are generally rare in
species have revealed features, e.g., bacterial sym- low-oxygen environments. It is important to note
bionts and unusually high abundances of peroxi- that no foraminiferal taxon is currently known to be
somes, that may be adaptations to extreme oxygen confined entirely to oxygen-depleted environments.
depletion. In addition, mitachondria-laden pseudo-
podia have the potential to extend into overlying
sediment layers where some oxygen may be present. Deep-Sea Foraminifera in
Many low-oxygen-tolerant foraminifera belong to
Paleo-Oceanography
the Orders Rotaliida and Buliminida. They often
have thin-walled, calcareous tests with either flat- Geologists require proxy indicators of important
tened, elongate biserial or triserial morphologies environmental variables in order to reconstruct an-
(e.g., Bolivina, Bulimina, Globobulimina, Fursen- cient oceans. Benthic foraminifera provide good
koina, Loxotomum, Uvigerina) or planispiral/len- proxies for seafloor parameters because they are
ticular morphologies (e.g., Cassidulina, widely distributed, highly sensitive to environmental
Chilostomella, Epistominella, Loxotomum, Nonion, conditions, and abundant in Cenozoic and Cret-
Nonionella). Some agglutinated foraminifera, e.g., aceous deep-sea sediments (note that deep-sea

Table 2 Benthic foraminiferal proxies or indicators (both faunal and chemical) useful in paleo-oceanographic reconstruction

Environmental parameter/property Proxy or indicator Remarks

Water depth Bathymetric ranges of abundant Depth zonation largely local although
species in modern oceans broad distinction between shelf,
slope and abyssal depth zones
possible
Distribution of bottom water masses Characteristic associations of epifaunal Relations between species and water
species masses may reflect lateral advection
Carbonate corrosiveness of bottom Abundance of Nuttallides umbonifera Corrosive bottom water often broadly
water corresponds to Antarctic Bottom
Water
Deep-ocean thermohaline circulation Cd/Ca ratios and d13C values for Proxies reflect ‘age’ of bottom
calcareous tests watermasses; i.e., period of time
elapsed since formation at ocean
surface
Oxygen-deficient bottom-water and Characteristic species associations; Species not consistently associated
pore water high-dominance, low-diversity with particular range of oxygen
assemblages concentrations and also found in
high-productivity areas
Primary productivity Abundance of foraminiferal tests Transfer function links productivity to
4150 mm test abundance (corrected for
differences in sedimentation rates
between sites) in oxygenated
sediments
Organic matter flux to seafloor (i) Assemblages of high productivity Assemblages indicate high organic
taxa (e.g. Globobulimina, Melonis matter flux to seafloor, with or without
barleeanum) corresponding decrease in oxygen
concentrations
(ii) Ratio between infaunal and epifaunal
morphotypes
(iii) Ratio between planktonic and
benthic tests
Seasonality in organic matter flux Relative abundance of ‘phytodetritus Reflects seasonally pulsed inputs of
species’ labile organic matter to seafloor
Methane release Large decrease (2–3%) in d13C values Inferred sudden release of 12C enriched
of benthic and planktonic tests methane from clathrate deposits
following temperature rise
346 BENTHIC FORAMINIFERA

sediments older than the middle Jurassic age have The cadmium/calcium ratio is a proxy for the nutrient
been destroyed by subduction, except where pre- (phosphate) content of sea water that reflects abyssal
served in ophiolite complexes). circulation patterns. Carbon isotope ratios also reflect
Foraminiferal faunas, and the chemical tracers deep-ocean circulation and the strength of organic
preserved in the tests of calcitic species, can be used matter fluxes to the seafloor.
to reconstruct a variety of paleoenvironmental par- It is important to appreciate that the accuracy with
ameters and attributes. The main emphasis has been which fossil foraminifera can be used to reconstruct
on organic matter fluxes and bottom-water/pore ancient deep-sea environments is often limited. These
water oxygen concentrations (inversely related par- limitations reflect the complexities of deep-sea for-
ameters), the distribution of bottom-water masses, aminiferal biology, many aspects of which remain
and the development of thermohaline circulation poorly understood. Moreover, simple relationships
(Table 2). Modern deep-sea faunas became estab- between the composition of foraminiferal assemblages
lished during the Middle Miocene (10–15 million and environmental variables are elusive, and it is often
years ago), and these assemblages can often be in- difficult to identify faunal characteristics that can be
terpreted in terms of modern analogues. This ap- used as precise proxies for paleo-oceanographic par-
proach is difficult or impossible to apply to sediments ameters. For example, geologists often wish to es-
from the Cretaceous and earlier Cenozoic, which tablish paleobathymetry. However, the bathymetric
contain many foraminiferal species that are now ex- distributions of foraminiferal species are inconsistent
tinct. In these cases, it can be useful to work with test and depend largely on the organic flux to the seafloor,
morphotypes (e.g., trochospiral, cylindrical, biserial/ which decreases with increasing depth (Figure 8) and
triserial) rather than species. The relative abundance is strongly influenced by surface productivity. Thus,
of infaunal morphotypes, for example, has been used foraminifera can be used only to discriminate in a
as an index of bottom-water oxygenation or relative general way between shelf, slope, and abyssal faunas,
intensities of organic matter inputs. The trace element but not to estimate precise paleodepths. Oxygen
(e.g., cadmium) content and stable isotope (d13C; i.e., concentrations and organic matter inputs are par-
the deviation from a standard 12C : 12C ratio) ticularly problematic. Certain species and morpho-
chemistry of the calcium carbonate shells of benthic types dominate in low-oxygen habitats that also are
foraminifera provide powerful tools for making usually characterized by high organic loadings.
paleo-oceanographic reconstructions, particularly However, the same foraminifera may occur in or-
during the climatically unstable Quaternary period. ganically enriched settings where oxygen levels are

0 3000 6000 9000 0 25 50 75 100

0 0

5 000 5 000
10 000 YD 10 000 YD
15 000 15 000
H1
20 000 20 000

25 000 25 000 H2

30 000 30 000
H3
35 000 35 000
40 000 40 000
H4
45 000 45 000
Phytodetritus species, Phytodetritus species,
Number per gram Relative abundance

Figure 9 (A) Absolute (specimens per gram of dry sediment) and (B) relative (percentage) abundances of Alabaminella
weddellensis and Epistominella exigua (463 mm fraction) in a long-sediment core from the North Atlantic (50141.30 N, 21151.90 W,
3547 m water depth). In modern oceans, these two species respond to pulsed inputs of organic matter (‘phytodetritus’) derived from
surface primary production. Note that they increased in abundance around 15 000 years ago, corresponding to the main Northern
Hemisphere deglaciation and the retreat of the Polar Front. Short period climatic fluctuations (YD ¼ Younger Dryas; H1–4 ¼ Heinrich
events, periods of very high meltwater production) are also evident in the record of these two species. (Reprinted from Thomas E,
Booth L, Maslin M and Shackleton NJ (1995). Northeast Atlantic benthic foraminifera during the last 45 000 years: change in
productivity seen from the bottom up. Paleoceanography: 10: 545–562; with permission from the American Geophysical Union.)
 BENTHIC FORAMINIFERA 347

not severely depressed, making it difficult for paleo- enormously diverse in terms of species numbers and
oceanographers to disentangle the influence of these test morphology. These testate (shell-bearing) protists
two variables. Finally, biological factors such as are also the most abundant benthic organisms pre-
microhabitat preferences and the exploitation of served in the deep-sea fossil record and provide
phytodetrital aggregates (‘floc’) influence the stable powerful tools for making paleo-oceanographic re-
isotope chemistry of foraminiferal tests. constructions. Our understanding of their biology has
There are many examples of the use of benthic advanced considerably during the last two decades,
foraminiferal faunas to interpret the geological his- although much remains to be learnt.
tory of the oceans. Only one is given here. Cores
collected at 501410 N, 211520 W (3547 m water depth)
and 581370 N, 191260 W (1756 m water depth) were
See also
used by E. Thomas and colleagues to study changes Abrupt Climate Change. Anthropogenic Trace
in the North Atlantic over the past 45 000 years. The Elements in the Ocean. Benthic Organisms
cores yielded fossil specimens of two foraminiferal Overview. Cenozoic Oceans – Carbon Cycle
species, Epistominella exigua and Alabaminella Models. Deep-Sea Fauna. Floc Layers.
weddellensis, both of which are associated with Macrobenthos. Meiobenthos. Microphytobenthos.
seasonal inputs of organic matter (phytodetritus) in Ocean Carbon System, Modeling of. Phytoplankton
modern oceans. In the core from 511N, these ‘phy- Blooms. Primary Production Processes.
Radiocarbon. Stable Carbon Isotope Variations in
todetritus species’ were uncommon during the last
the Ocean. Tracers of Ocean Productivity.
glacial maximum but increased sharply in absolute
and relative abundance during the period of degla-
ciation 15 000–16 000 years ago (Figure 9). At the
Further Reading
same time there was a decrease in the abundance of
Neogloboquadrina pachyderma, a planktonic fora- Fischer G and Wefer G (1999) Use of Proxies in
minifer found in polar regions, and an increase in the Paleoceanography: Examples from the South Atlantic.
abundance of Globigerina bulloides, a planktonic Berlin: Springer-Verlag.
species characteristic of warmer water. These chan- Gooday AJ, Levin LA, Linke P, and Heeger T (1992) The
ges were interpreted as follows. Surface primary role of benthic foraminifera in deep-sea food webs and
productivity was low at high latitudes in the glacial carbon cycling. In: Rowe GT and Pariente V (eds.)
North Atlantic, but was much higher to the south of Deep-Sea Food Chains and the Global Carbon Cycle,
pp. 63--91. Dordrecht: Kluwer Academic.
the Polar Front. At the end of the glacial period, the
Jones RW (1994) The Challenger Foraminifera. Oxford:
ice sheet shrank and the Polar Front retreated Oxford University Press.
northwards. The 511N site was now overlain by Loeblich AR and Tappan H (1987) Foraminiferal Genera
more productive surface water characterized by a and their Classification, vols 1, 2. New York: Van
strong spring bloom and a seasonal flux of phyto- Nostrand Reinhold.
detritus to the seafloor. This episodic food source Murray JW (1991) Ecology and Palaeoecology of Benthic
favored opportunistic species, particularly E. exigua Foraminifera. New York: Wiley; Harlow: Longman
and A. weddellensis, which became much more Scientific and Technical.
abundant both in absolute terms and as a proportion SenGupta BK (ed.) (1999) Modern Foraminifera.
of the entire foraminiferal assemblage. Dordrecht: Kluwer Academic.
Tendal OS and Hessler RR (1977) An introduction to the
biology and systematics of Komokiacea. Galathea
Conclusions Report 14: 165--194, plates 9–26.
Van der Zwan GJ, Duijnstee IAP, den Dulk M, et al. (1999)
Benthic foraminifera are a major component of deep- Benthic foraminifers:: proxies or problems? A review of
sea communities, play an important role in ecosystem paleoecological concepts. Earth Sciences Reviews 46:
functioning and biogeochemical cycling, and are 213--236.