These data were collected during the mesocosm experiment described in "Keystone nonconsumpti... more These data were collected during the mesocosm experiment described in "Keystone nonconsumptive effects within a diverse predator community" by Meadows et al. 2017. A description of each column follows: 1- Source: treatment groups; 2- Exposure: C=caged mosquito larvae, NC= exposed mosquito larvae; 3- Sex: sex could only be determined for (most) adult mosquitoes; 4-Tp: days to pupation i.e. larval development period; 5- Longevity: adult mosquito longevity (eclosion-death, in days); 6- Density: total number of predators in mesocosm; 7- Aquarius: number of Aquarius in mesocosm; 8- Beetle: number of Agabus + Tropisternus beetles in mesocosm; 9- Notonecta: number of Notonecta in mesocosm; 10- Aeshna: was Aeshna present in the community? Yes or No for predator treatments, Control if no predator (or Aeshna, by extension); 11-H: Shannon's H calculation for predator community evenness (99 entered for control to easily subset predator only treatments); 12- Cslong: sex-standardized adult longevity (see Meadows et al. Supp Info for calculation); 13- Winglength: adult winglength (in mm
Targeted management strategies to control mosquitoes and birds in orchards and vineyards could ... more Targeted management strategies to control mosquitoes and birds in orchards and vineyards could help curb the spread of WNV Fig 5. WNV incidence in (A) horses and (B) mosquitoes increases with increasing acreage of orchards and vineyards. (A) The number of WNV cases in horses from 2007-2010 in each county where WNV was confirmed present (shaded gray) is shown. (B) Each circle represents a unique sampling location, with the shade of the circle indicating the proportion of mosquito pools at that location that tested positive for WNV. In both panels, the area devoted to orchard and vineyard production is shaded green.
Experimental demonstration of a parasite-induced immune response in wild birds: Darwin’s finches ... more Experimental demonstration of a parasite-induced immune response in wild birds: Darwin’s finches and introduced
<jats:title>Abstract</jats:title> <jats:p>Birds increase crop yields via consum... more <jats:title>Abstract</jats:title> <jats:p>Birds increase crop yields via consumption of pests in some contexts but disrupt pest control via intraguild predation in others. Landscape complexity acts as an inconsistent mediator, sometimes increasing, decreasing, or not impacting pest control. Here, we examined how landscape context and seasonal variation mediate the impact of birds on arthropod pests and natural enemies, leaf damage, and yields of broccoli (Brassica oleracea) on highly diversified farms that spanned the USA west coast. Our study had two complementary components: a bird exclusion experiment and molecular diet analysis of 357 fecal samples collected from the most commonly captured bird species that also foraged in Brassica fields—American Goldfinch (Spinus tristis), American Robin (Turdus migratorius), Savannah Sparrow (Passerculus sandwichensis), Song Sparrow (Melospiza melodia), and White-crowned Sparrow (Zonotrichia leucophrys). Bird access yielded higher, rather than lower, numbers of pest aphids and increased their parasitism, while no other arthropods examined were consistently impacted. Independent of bird presence, percent natural cover in the landscape sometimes increased and sometimes decreased densities of arthropods in the mid-growth period, with diminishing impacts in the late-growth period. Herbivore feeding damage to broccoli leaves decreased with increasing amounts of natural land cover and in the late-growth period. Molecular diet analysis revealed that Brassica pests and predatory arthropods were relatively uncommon prey for birds. Landscape context did not alter the prey items found in bird diets. Altogether, our bird-exclusion experiment and molecular diet analysis suggested that birds have relatively modest impacts on the arthropods associated with broccoli plantings. More broadly, the limited support in our study for net natural pest control services suggests that financial incentives may be required to encourage the adoption of bird-friendly farming practices in certain cropping systems.</jats:p>
Recent foodborne illness outbreaks have heightened pressures on growers to deter wildlife from fa... more Recent foodborne illness outbreaks have heightened pressures on growers to deter wildlife from farms, jeopardizing conservation efforts. However, it remains unclear which species, particularly birds, pose the greatest risk to food safety. Using >11,000 pathogen tests and 1565 bird surveys covering 139 bird species from across the western United States, we examined the importance of 11 traits in mediating wild bird risk to food safety. We tested whether traits associated with pathogen exposure (e.g., habitat associations, movement, and foraging strategy) and pace-of-life (clutch size and generation length) mediated foodborne pathogen prevalence and proclivities to enter farm fields and defecate on crops. Campylobacter spp. were the most prevalent enteric pathogen (8.0%), while Salmonella and Shiga-toxin producing Escherichia coli (STEC) were rare (0.46% and 0.22% prevalence, respectively). We found that several traits related to pathogen exposure predicted pathogen prevalence. Specifically, Campylobacter and STEC-associated virulence genes were more often detected in species associated with cattle feedlots and bird feeders, respectively. Campylobacter was also more prevalent in species that consumed plants and had longer generation lengths. We found that species associated with feedlots were more likely to enter fields and defecate on crops. Our results indicated that canopy-foraging insectivores were less likely to deposit foodborne pathogens on crops, suggesting growers may be able to promote pest-eating birds and birds of conservation concern (e.g., via nest boxes) without necessarily compromising food safety. As such, promoting insectivorous birds may represent a win-win-win for bird conservation, crop production, and food safety. Collectively, our results suggest that separating crop production from livestock farming may be the best way to lower food safety risks from birds. More broadly, our trait-based framework suggests a path forward for co-managing wildlife conservation and food safety risks in farmlands by providing a strategy for holistically evaluating the food safety risks of wild animals, including under-studied species.
1. Birds play many roles within agroecosystems including as consumers of crops and pests, carrier... more 1. Birds play many roles within agroecosystems including as consumers of crops and pests, carriers of pathogens, and beloved icons. Birds are also rapidly declining across North America, in part due to agricultural intensification. Thus, it is imperative to identify how to manage agroecosystems to best support birds for multi-functional outcomes (e.g., crop production and conservation). Both the average amounts of services/disservices provided and their temporal stability are important for effective farm planning. 2. Here, we conducted point-count surveys for four years across 106 locations on 27 diversified farms in Washington and Oregon, USA. We classified birds as ecosystem service or disservice providers using indices spanning supporting, regulating, provisioning, and cultural services/disservices. We then examined service/disservice index pairwise correlations and assessed the relative importance of local, farm, and landscape complexity on the average and temporal stability of ...
Growing demand for poultry meat and eggs labeled as organic, cage free, or pasture raised has inc... more Growing demand for poultry meat and eggs labeled as organic, cage free, or pasture raised has increased the number of producers that manage chickens outdoors. In these open environments, there are likely diverse enteric parasites sustained by fecal-oral transmission or passage through intermediate invertebrate hosts (e.g., worms and insects) that chickens consume. Enteric parasites can reduce chicken health and productivity, but there are few published data describing the identities or prevalence of these parasites on farms that use open environments in the United States. We surveyed 27 poultry farms with open environments that were situated across a wide geographic range, including California, Oregon, Idaho, and Washington. These farms did not use anticoccidial drugs, coccidia vaccines, or parasiticides. Flock size, enclosure area, flock density, flock rotation frequency, and average flock age were highly correlated for all the farms in this study. We analyzed how enclosure size and flock rotations per year (which represented two axes of variation in management) correlated with prevalence of five observed parasite taxa at the farm level. Across all flocks, we detected by fecal flotation Eimeria spp. (95% flocks), Ascaridia galli (69%), Heterakis gallinarum (52%), Capillaria spp. (39%), Strongyloides avium (13%), tapeworm species (29%), Cryptosporidium spp. (3%), and Dispharynx nasuta (1%). Eighty-five percent of samples were coinfected with two or more parasite taxa. Sixty-seven percent of farms raised only layer chicken breeds, 4% raised only broiler breeds, and 30% raised both layer and broiler breeds. The average age of the broiler flocks was 11.0 wk (±1.1 SE), and flocks were moved 54.7 (±17.9) times annually to new locations in pastures (hereafter, "rotation"). Layer flocks averaged 84.9 (±7.67) wk of age and were moved less often on farms being rotated 20.0 (±6.05) times per year. Generalized linear mixed models indicated that for every 1 m2 increase in enclosure size, the odds of detecting Eimeria spp. increased by 0.03%. Furthermore, for every additional rotation per year, the odds of detecting A. galli decreased by 1.3%. For every additional rotation per year, the odds of detecting tapeworm species increased by 2.2%. We found no evidence that flock spatial management affected prevalence of the other parasites observed on the farms. Farming practices and parasite responses in these systems are highly varied, which makes it difficult to identify potential management interventions for reducing these infections.
Agricultural intensification is a leading threat to bird conservation. Highly diversified farming... more Agricultural intensification is a leading threat to bird conservation. Highly diversified farming systems that integrate livestock and crop production might promote a diversity of habitats useful to native birds foraging across otherwise-simplified landscapes. At the same time, these features might be attractive to non-native birds linked to a broad range of disservices to both crop and livestock production. We evaluated the influence of crop-livestock integration on wild bird richness and density along a north-south transect spanning the U.S. west coast. We surveyed birds on 52 farms that grew primarily mixed vegetables and fruits alone or integrated livestock into production. Crop-livestock systems harbored higher native bird density and richness relative to crop only farms, a benefit more pronounced on farms embedded in non-natural landscapes. Crop-livestock systems bolstered native insectivores linked to the suppression of agricultural pest insects but did not bolster native gra...
Abstract Growers may be more likely to adopt wildlife-friendly practices if they perceive that be... more Abstract Growers may be more likely to adopt wildlife-friendly practices if they perceive that beneficial species are present and conservation actions are successful. At the same time, a farm's landscape and regional context may influence whether biodiversity, including wild birds, are likely to provide ecosystem services or disservices. Here, across two Bird Conservation Regions in the western USA, we assessed a feedback loop that links growers' attitudes towards birds, farming practices, and bird assemblages' hypothesized impacts. To do so, we paired a grower questionnaire survey, bird point count surveys, and farm management and landscape classifications. We found that growers generally exhibited more positive attitudes towards raptors than songbirds and allies (e.g., flycatchers, woodpeckers, hummingbirds). Attitudes towards raptors were more positive when farms were embedded in more natural landscapes and had greater proportions of nonnative birds. Growers held more positive attitudes towards songbirds and allies related to production (yields, crop quality, insect control) when their farms were in the Northern Pacific Rainforest region and were embedded in more natural landscapes. Growers' attitudes towards songbirds and allies related to disease/infrastructure (food safety, animal disease, building/machinery damage, vertebrate control) were more positive in the Northern Pacific Rainforest region as landscapes became more natural, but these relationships did not hold for Coastal California. However, growers' attitudes towards birds were mostly unrelated to the practices used on the farm. Understanding these feedback loops is crucial to increasing uptake of and retention in conservation programs for rapidly declining farmland bird communities.
Enteric illnesses remain the second largest source of communicable diseases worldwide, and wild b... more Enteric illnesses remain the second largest source of communicable diseases worldwide, and wild birds are suspected sources for human infection. This has led to efforts to reduce pathogen spillover through deterrence of wildlife and removal of wildlife habitat, particularly within farming systems, which can compromise conservation efforts and the ecosystem services wild birds provide. Further, Salmonella spp. are a significant cause of avian mortality, leading to additional conservation concerns. Despite numerous studies of enteric bacteria in wild birds and policies to discourage birds from food systems, we lack a comprehensive understanding of wild bird involvement in transmission of enteric bacteria to humans. Here, we propose a framework for understanding spillover of enteric pathogens from wild birds to humans, which includes pathogen acquisition, reservoir competence and bacterial shedding, contact with people and food, and pathogen survival in the environment. We place the literature into this framework to identify important knowledge gaps. Second, we conduct a meta-analysis of prevalence data for three human enteric pathogens, Campylobacter spp., E. coli, and Salmonella spp., in 431 North American breeding bird species. Our literature review revealed that only 3% of studies addressed the complete system of pathogen transmission. In our meta-analysis, we found a Campylobacter spp. prevalence of 27% across wild birds, while prevalence estimates of pathogenic E. coli (20%) and Salmonella spp. (6.4%) were lower. There was significant bias in which bird species have been tested, with most studies focusing on a small number of taxa that are common near people (e.g. European starlings Sturnus vulgaris and rock pigeons Columba livia) or commonly in contact with human waste (e.g. gulls). No pathogen prevalence data were available for 65% of North American breeding bird species, including many commonly in contact with humans (e.g. black-billed magpie Pica hudsonia and great blue heron Ardea herodias), and our metadata suggest that some under-studied species, taxonomic groups, and guilds may represent equivalent or greater risk to human infection than heavily studied species. We conclude that current data do not provide sufficient information to determine the likelihood of enteric pathogen spillover from wild birds to humans and thus preclude management solutions. The primary focus in the literature on pathogen prevalence likely overestimates the probability of enteric pathogen spillover from wild birds to humans because a pathogen must survive long enough at an infectious dose and be a strain that is able to colonize humans to cause infection. We propose that future research should focus on the large number of under-studied species commonly in contact with people and food production and demonstrate shedding of bacterial strains pathogenic to humans into the environment where people may contact them. Finally, studies assessing the duration and intensity of bacterial shedding and survival of bacteria in the environment in bird faeces will help provide crucial missing information necessary to calculate spillover probability. Addressing these essential knowledge gaps will support policy to reduce enteric pathogen spillover to humans and enhance bird conservation efforts that are currently undermined by unsupported fears of pathogen spillover from wild birds.
ABSTRACT Background/Question/Methods The vertebrate immune system utilizes physiological resource... more ABSTRACT Background/Question/Methods The vertebrate immune system utilizes physiological resources to produce the diverse cells and proteins that provide defense against infectious organisms (parasites). Hypothetically, the resources allocated to the immune system must be traded against other physiological demands (e.g. growth). These internal trade-offs are believed to drive the variation in immune function often observed among individuals. These resource constraints begin with the diet itself, since nutrients and calories vary with food quantity and quality. Here we ask if diet manipulation affects immune function of a deer mouse (Peromyscus maniculatus) through its ability to gain resistance to an ectoparasite, the Rocky Mountain wood tick (Dermacentor andersoni). Four distinct diet groups were created using mixtures of arthropods and seeds. The range of diets included ratios of seeds versus arthropods at the limits of mouse homeostasis (i.e. further dietary skew produced rapid weight loss and mortality). Mice were fed the controlled diets before and during 2 tick infestation periods where each mouse was inoculated with 50 wood tick larvae. Engorged ticks were recovered and counted from each mouse during both infestations to determine the relative susceptibility/resistance to ticks among the mouse diet groups. Results/Conclusions Mouse body weight was affected by diet and parasitism. In general mice lost weight during periods of infestation and regained weight during the time between infestations. Mice fed a diet skewed toward arthropods lost weight more rapidly during infestations than mice fed a diet skewed toward seeds. Within an infestation period the number of ticks that successfully obtained blood meals was unaffected by the variation in host diet. Significantly fewer ticks fed on mice during the second infestation compared to the first infestation, which indicated that mice acquired resistance to tick blood feeding during the initial exposure. This observation mirrors results of other experiments demonstrating deer mice will develop resistance to Rocky Mountain wood ticks. These results suggest diet affects body mass during parasitism, but immune defense remains intact regardless of dietary differences. This has implications for the interactions between host ecology and infectious disease. Though host condition (body weight) may be influenced by the interaction between food resources and infection, immune defense may remain intact even when dietary resources change over space and time. Ongoing work is also examining the effect of diet on immune function relative to parasitism by wood ticks through manipulation of food abundance.
Commercial vaccines based on the tick gut protein Bm86 have been successful in controlling the on... more Commercial vaccines based on the tick gut protein Bm86 have been successful in controlling the onehost tick Rhipicephalus (Boophilus) microplus and provide heterologous protection against certain other non-target ixodid tick species. This cross protection, however, does not extend to the three-host tick R. appendiculatus, the vector of the protozoan parasite Theileria parva. When transmitted to cattle, T. parva causes the often fatal disease East Coast fever. Here, we used insect cell-expressed recombinant versions of the R. appendiculatus homologs of Bm86, named Ra86, to vaccinate cattle. We measured multiple fitness characteristics for ticks that were fed on cattle Ra86-vaccinated or unvaccinated. The Ra86 vaccination of cattle significantly decreased the molting success of nymphal ticks to the adult stage. Modeling simulations based on our empirical data suggest that repeated vaccinations using Ra86 could reduce tick populations over successive generations. Vaccination with Ra86 could thus form a component of integrated control strategies for R. appendiculatus leading to a reduction in use of environmentally damaging acaricides.
Background: Maternal antibodies are believed to play an integral role in protecting immunological... more Background: Maternal antibodies are believed to play an integral role in protecting immunologically immature wildpasserines from environmental antigens. This study comprehensively examines the early development of the adaptive immune system in an altricial-developing wild passerine species, the house sparrow (Passer domestics), by characterizing the half-life of maternal antibodies in nestling plasma, the onset of de novo synthesis of endogenous antibodies by nestlings, and the timing of immunological independence, where nestlings rely entirely on their own antibodies for immunologic protection. Methodology/Principal Findings: In an aviary study we vaccinated females against a novel antigen that these birds would not otherwise encounter in their natural environment, and measured both antigen-specific and total antibody concentration in the plasma of females, yolks, and nestlings. We traced the transfer of maternal antibodies from females to nestlings through the yolk and measured catabolisation of maternal antigen-specific antibodies in nestlings during early development. By utilizing measurements of non-specific and specific antibody levels in nestling plasma we were able to calculate the half-life of maternal antibodies in nestling plasma and the time point at which nestling were capable of synthesizing antibodies themselves. Based on the short half-life of maternal antibodies, the rapid production of endogenous antibodies by nestlings and the relatively low transfer of maternal antibodies to nestlings, our findings suggest that altricialdeveloping sparrows achieve immunologic independence much earlier than precocial birds. Conclusions/Significance: To our knowledge, this is the first in depth analyses performed on the adaptive immune system of a wild-passerine species. Our results suggest that maternal antibodies may not confer the immunologic protection or immune priming previously proposed in other passerine studies. Further research needs to be conducted on other altricial passerines to determine if the results of our study are a species-specific phenomenon or if they apply to all altricialdeveloping birds.
Arthropod-borne viruses (arboviruses) threaten the health of humans, livestock, and wildlife. Wes... more Arthropod-borne viruses (arboviruses) threaten the health of humans, livestock, and wildlife. West Nile virus (WNV), the world's most widespread arbovirus, invaded the United States in 1999 and rapidly spread across the county. Although the ecology of vectors and hosts are key determinants of WNV prevalence across landscapes, the factors shaping local vector and host populations remain unclear. Here, we used spatially-explicit models to evaluate how three land-use types (orchards, vegetable/forage crops, natural) and two climatic variables (temperature, precipitation) influence the prevalence of WNV infections and vector/host distributions at landscape and local spatial scales. Across landscapes, we show that orchard habitats were associated with greater prevalence of WNV infections in reservoirs (birds) and incidental hosts (horses), while increased precipitation was associated with fewer infections. At local scales, orchard habitats increased the prevalence of WNV infections in vectors (mosquitoes) and the abundance of mosquitoes and two key reservoir species, the American robin and the house sparrow. Thus, orchard habitats benefitted WNV vectors and reservoir hosts locally, creating focal points for the transmission of WNV at landscape scales in the presence of suitable climatic conditions.
Background: Ectoparasites rely on blood-feeding to sustain activity, support development and prod... more Background: Ectoparasites rely on blood-feeding to sustain activity, support development and produce offspring. Blood-feeding is also a route for transmission of diverse vector-borne pathogens. The likelihood of successfully feeding is thus an important aspect of ectoparasite population dynamics and pathogen transmission. Factors that affect blood-feeding include ectoparasite density, host defenses, and ages of the host and ectoparasite. How these factors interact to affect feeding success is not well understood. Methods: We monitored blood-feeding success of larval Rocky Mountain wood ticks (RMWTs; Dermacentor andersoni) on deer mice (Peromyscus maniculatus) in several experiments to determine how tick density, host defense, and ages of mice and ticks interact to influence feeding success. In the first experiment, tick-naive deer mice were infested with one of several densities of RMWT larvae, while a second cohort of mice were infested with 50 larvae each. Two weeks after ticks dropped off, mice in the first cohort were re-exposed to 50 larvae each and mice in the second cohort were re-exposed to varying densities of larvae. In the second experiment mice of different ages (45-374 days old) were exposed to 50 larvae each. Two weeks later mice were re-exposed to 50 larvae each. We combined data from these and several similar experiments to test the generality of the patterns we observed. Lastly, we tested whether tick feeding success was consistent on individual mice that were challenged on four occasions. Results: Mice acquired resistance such that feeding success declined dramatically from the first to the second infestation. Feeding success also declined with tick density and tick age. Mice, however, became more permissive with age. The sizes of these effects were similar and additive. Surprisingly, over successive infestations the relative resistance among mice changed among hosts within a cohort. Conclusions: We predict that larval blood-feeding success, and thus development to the nymph stage, will change due to variation in tick age and density, as well as the age and history of the host. Incorporating these biotic factors into modeling of tick population dynamics may improve predictions of tick-borne pathogen transmission.
1. Farmland diversification practices are increasingly adopted to help reverse biodiversity decli... more 1. Farmland diversification practices are increasingly adopted to help reverse biodiversity declines in agroecosystems. However, evidence for the effectiveness of this approach often comes from documenting the species attracted to particular farming systems or landscapes, rather than their underlying physiological states that ultimately determine population growth or decline over the longer term. 2. Across 38 organic, mixed-produce farms spanning the U.S. west coast, we quantified three physiological biomarkers that are widely used to capture variation in short and long-term stress responses for nine bird species with diverse life-history traits. While controlling for other potentially confounding variables, we used multilevel models to examine the association between bird physiological conditions, landscape context and local farm management practices, including the integration of livestock, and cropland composition and configuration. 3. Birds generally had lower stress responses on more-locally-diverse farms and in landscapes with higher amounts of seminatural cover. However, interactions between farm diversity and landscape context suggested birds were less stressed on more diverse farms in simpler landscapes, but more stressed and in poorer condition on more diverse farms embedded within complex landscapes. 4. We found no differences in stress responses among birds in relation to their degree of human association (synanthropy), which suggests generality in our findings. 5. Synthesis and application. Birds were often less stressed on more diverse farms. However, these patterns were mediated by landscape context: birds were less stressed on more diverse farms in simplified landscapes, but more stressed on more diverse farms within complex landscapes. This means land managers might not see uniform effects of local diversification schemes across different landscape contexts. Our results underscore the need to consider responses related to physiological health status, in addition to species richness and abundance, [...]
These data were collected during the mesocosm experiment described in "Keystone nonconsumpti... more These data were collected during the mesocosm experiment described in "Keystone nonconsumptive effects within a diverse predator community" by Meadows et al. 2017. A description of each column follows: 1- Source: treatment groups; 2- Exposure: C=caged mosquito larvae, NC= exposed mosquito larvae; 3- Sex: sex could only be determined for (most) adult mosquitoes; 4-Tp: days to pupation i.e. larval development period; 5- Longevity: adult mosquito longevity (eclosion-death, in days); 6- Density: total number of predators in mesocosm; 7- Aquarius: number of Aquarius in mesocosm; 8- Beetle: number of Agabus + Tropisternus beetles in mesocosm; 9- Notonecta: number of Notonecta in mesocosm; 10- Aeshna: was Aeshna present in the community? Yes or No for predator treatments, Control if no predator (or Aeshna, by extension); 11-H: Shannon's H calculation for predator community evenness (99 entered for control to easily subset predator only treatments); 12- Cslong: sex-standardized adult longevity (see Meadows et al. Supp Info for calculation); 13- Winglength: adult winglength (in mm
Targeted management strategies to control mosquitoes and birds in orchards and vineyards could ... more Targeted management strategies to control mosquitoes and birds in orchards and vineyards could help curb the spread of WNV Fig 5. WNV incidence in (A) horses and (B) mosquitoes increases with increasing acreage of orchards and vineyards. (A) The number of WNV cases in horses from 2007-2010 in each county where WNV was confirmed present (shaded gray) is shown. (B) Each circle represents a unique sampling location, with the shade of the circle indicating the proportion of mosquito pools at that location that tested positive for WNV. In both panels, the area devoted to orchard and vineyard production is shaded green.
Experimental demonstration of a parasite-induced immune response in wild birds: Darwin’s finches ... more Experimental demonstration of a parasite-induced immune response in wild birds: Darwin’s finches and introduced
<jats:title>Abstract</jats:title> <jats:p>Birds increase crop yields via consum... more <jats:title>Abstract</jats:title> <jats:p>Birds increase crop yields via consumption of pests in some contexts but disrupt pest control via intraguild predation in others. Landscape complexity acts as an inconsistent mediator, sometimes increasing, decreasing, or not impacting pest control. Here, we examined how landscape context and seasonal variation mediate the impact of birds on arthropod pests and natural enemies, leaf damage, and yields of broccoli (Brassica oleracea) on highly diversified farms that spanned the USA west coast. Our study had two complementary components: a bird exclusion experiment and molecular diet analysis of 357 fecal samples collected from the most commonly captured bird species that also foraged in Brassica fields—American Goldfinch (Spinus tristis), American Robin (Turdus migratorius), Savannah Sparrow (Passerculus sandwichensis), Song Sparrow (Melospiza melodia), and White-crowned Sparrow (Zonotrichia leucophrys). Bird access yielded higher, rather than lower, numbers of pest aphids and increased their parasitism, while no other arthropods examined were consistently impacted. Independent of bird presence, percent natural cover in the landscape sometimes increased and sometimes decreased densities of arthropods in the mid-growth period, with diminishing impacts in the late-growth period. Herbivore feeding damage to broccoli leaves decreased with increasing amounts of natural land cover and in the late-growth period. Molecular diet analysis revealed that Brassica pests and predatory arthropods were relatively uncommon prey for birds. Landscape context did not alter the prey items found in bird diets. Altogether, our bird-exclusion experiment and molecular diet analysis suggested that birds have relatively modest impacts on the arthropods associated with broccoli plantings. More broadly, the limited support in our study for net natural pest control services suggests that financial incentives may be required to encourage the adoption of bird-friendly farming practices in certain cropping systems.</jats:p>
Recent foodborne illness outbreaks have heightened pressures on growers to deter wildlife from fa... more Recent foodborne illness outbreaks have heightened pressures on growers to deter wildlife from farms, jeopardizing conservation efforts. However, it remains unclear which species, particularly birds, pose the greatest risk to food safety. Using >11,000 pathogen tests and 1565 bird surveys covering 139 bird species from across the western United States, we examined the importance of 11 traits in mediating wild bird risk to food safety. We tested whether traits associated with pathogen exposure (e.g., habitat associations, movement, and foraging strategy) and pace-of-life (clutch size and generation length) mediated foodborne pathogen prevalence and proclivities to enter farm fields and defecate on crops. Campylobacter spp. were the most prevalent enteric pathogen (8.0%), while Salmonella and Shiga-toxin producing Escherichia coli (STEC) were rare (0.46% and 0.22% prevalence, respectively). We found that several traits related to pathogen exposure predicted pathogen prevalence. Specifically, Campylobacter and STEC-associated virulence genes were more often detected in species associated with cattle feedlots and bird feeders, respectively. Campylobacter was also more prevalent in species that consumed plants and had longer generation lengths. We found that species associated with feedlots were more likely to enter fields and defecate on crops. Our results indicated that canopy-foraging insectivores were less likely to deposit foodborne pathogens on crops, suggesting growers may be able to promote pest-eating birds and birds of conservation concern (e.g., via nest boxes) without necessarily compromising food safety. As such, promoting insectivorous birds may represent a win-win-win for bird conservation, crop production, and food safety. Collectively, our results suggest that separating crop production from livestock farming may be the best way to lower food safety risks from birds. More broadly, our trait-based framework suggests a path forward for co-managing wildlife conservation and food safety risks in farmlands by providing a strategy for holistically evaluating the food safety risks of wild animals, including under-studied species.
1. Birds play many roles within agroecosystems including as consumers of crops and pests, carrier... more 1. Birds play many roles within agroecosystems including as consumers of crops and pests, carriers of pathogens, and beloved icons. Birds are also rapidly declining across North America, in part due to agricultural intensification. Thus, it is imperative to identify how to manage agroecosystems to best support birds for multi-functional outcomes (e.g., crop production and conservation). Both the average amounts of services/disservices provided and their temporal stability are important for effective farm planning. 2. Here, we conducted point-count surveys for four years across 106 locations on 27 diversified farms in Washington and Oregon, USA. We classified birds as ecosystem service or disservice providers using indices spanning supporting, regulating, provisioning, and cultural services/disservices. We then examined service/disservice index pairwise correlations and assessed the relative importance of local, farm, and landscape complexity on the average and temporal stability of ...
Growing demand for poultry meat and eggs labeled as organic, cage free, or pasture raised has inc... more Growing demand for poultry meat and eggs labeled as organic, cage free, or pasture raised has increased the number of producers that manage chickens outdoors. In these open environments, there are likely diverse enteric parasites sustained by fecal-oral transmission or passage through intermediate invertebrate hosts (e.g., worms and insects) that chickens consume. Enteric parasites can reduce chicken health and productivity, but there are few published data describing the identities or prevalence of these parasites on farms that use open environments in the United States. We surveyed 27 poultry farms with open environments that were situated across a wide geographic range, including California, Oregon, Idaho, and Washington. These farms did not use anticoccidial drugs, coccidia vaccines, or parasiticides. Flock size, enclosure area, flock density, flock rotation frequency, and average flock age were highly correlated for all the farms in this study. We analyzed how enclosure size and flock rotations per year (which represented two axes of variation in management) correlated with prevalence of five observed parasite taxa at the farm level. Across all flocks, we detected by fecal flotation Eimeria spp. (95% flocks), Ascaridia galli (69%), Heterakis gallinarum (52%), Capillaria spp. (39%), Strongyloides avium (13%), tapeworm species (29%), Cryptosporidium spp. (3%), and Dispharynx nasuta (1%). Eighty-five percent of samples were coinfected with two or more parasite taxa. Sixty-seven percent of farms raised only layer chicken breeds, 4% raised only broiler breeds, and 30% raised both layer and broiler breeds. The average age of the broiler flocks was 11.0 wk (±1.1 SE), and flocks were moved 54.7 (±17.9) times annually to new locations in pastures (hereafter, "rotation"). Layer flocks averaged 84.9 (±7.67) wk of age and were moved less often on farms being rotated 20.0 (±6.05) times per year. Generalized linear mixed models indicated that for every 1 m2 increase in enclosure size, the odds of detecting Eimeria spp. increased by 0.03%. Furthermore, for every additional rotation per year, the odds of detecting A. galli decreased by 1.3%. For every additional rotation per year, the odds of detecting tapeworm species increased by 2.2%. We found no evidence that flock spatial management affected prevalence of the other parasites observed on the farms. Farming practices and parasite responses in these systems are highly varied, which makes it difficult to identify potential management interventions for reducing these infections.
Agricultural intensification is a leading threat to bird conservation. Highly diversified farming... more Agricultural intensification is a leading threat to bird conservation. Highly diversified farming systems that integrate livestock and crop production might promote a diversity of habitats useful to native birds foraging across otherwise-simplified landscapes. At the same time, these features might be attractive to non-native birds linked to a broad range of disservices to both crop and livestock production. We evaluated the influence of crop-livestock integration on wild bird richness and density along a north-south transect spanning the U.S. west coast. We surveyed birds on 52 farms that grew primarily mixed vegetables and fruits alone or integrated livestock into production. Crop-livestock systems harbored higher native bird density and richness relative to crop only farms, a benefit more pronounced on farms embedded in non-natural landscapes. Crop-livestock systems bolstered native insectivores linked to the suppression of agricultural pest insects but did not bolster native gra...
Abstract Growers may be more likely to adopt wildlife-friendly practices if they perceive that be... more Abstract Growers may be more likely to adopt wildlife-friendly practices if they perceive that beneficial species are present and conservation actions are successful. At the same time, a farm's landscape and regional context may influence whether biodiversity, including wild birds, are likely to provide ecosystem services or disservices. Here, across two Bird Conservation Regions in the western USA, we assessed a feedback loop that links growers' attitudes towards birds, farming practices, and bird assemblages' hypothesized impacts. To do so, we paired a grower questionnaire survey, bird point count surveys, and farm management and landscape classifications. We found that growers generally exhibited more positive attitudes towards raptors than songbirds and allies (e.g., flycatchers, woodpeckers, hummingbirds). Attitudes towards raptors were more positive when farms were embedded in more natural landscapes and had greater proportions of nonnative birds. Growers held more positive attitudes towards songbirds and allies related to production (yields, crop quality, insect control) when their farms were in the Northern Pacific Rainforest region and were embedded in more natural landscapes. Growers' attitudes towards songbirds and allies related to disease/infrastructure (food safety, animal disease, building/machinery damage, vertebrate control) were more positive in the Northern Pacific Rainforest region as landscapes became more natural, but these relationships did not hold for Coastal California. However, growers' attitudes towards birds were mostly unrelated to the practices used on the farm. Understanding these feedback loops is crucial to increasing uptake of and retention in conservation programs for rapidly declining farmland bird communities.
Enteric illnesses remain the second largest source of communicable diseases worldwide, and wild b... more Enteric illnesses remain the second largest source of communicable diseases worldwide, and wild birds are suspected sources for human infection. This has led to efforts to reduce pathogen spillover through deterrence of wildlife and removal of wildlife habitat, particularly within farming systems, which can compromise conservation efforts and the ecosystem services wild birds provide. Further, Salmonella spp. are a significant cause of avian mortality, leading to additional conservation concerns. Despite numerous studies of enteric bacteria in wild birds and policies to discourage birds from food systems, we lack a comprehensive understanding of wild bird involvement in transmission of enteric bacteria to humans. Here, we propose a framework for understanding spillover of enteric pathogens from wild birds to humans, which includes pathogen acquisition, reservoir competence and bacterial shedding, contact with people and food, and pathogen survival in the environment. We place the literature into this framework to identify important knowledge gaps. Second, we conduct a meta-analysis of prevalence data for three human enteric pathogens, Campylobacter spp., E. coli, and Salmonella spp., in 431 North American breeding bird species. Our literature review revealed that only 3% of studies addressed the complete system of pathogen transmission. In our meta-analysis, we found a Campylobacter spp. prevalence of 27% across wild birds, while prevalence estimates of pathogenic E. coli (20%) and Salmonella spp. (6.4%) were lower. There was significant bias in which bird species have been tested, with most studies focusing on a small number of taxa that are common near people (e.g. European starlings Sturnus vulgaris and rock pigeons Columba livia) or commonly in contact with human waste (e.g. gulls). No pathogen prevalence data were available for 65% of North American breeding bird species, including many commonly in contact with humans (e.g. black-billed magpie Pica hudsonia and great blue heron Ardea herodias), and our metadata suggest that some under-studied species, taxonomic groups, and guilds may represent equivalent or greater risk to human infection than heavily studied species. We conclude that current data do not provide sufficient information to determine the likelihood of enteric pathogen spillover from wild birds to humans and thus preclude management solutions. The primary focus in the literature on pathogen prevalence likely overestimates the probability of enteric pathogen spillover from wild birds to humans because a pathogen must survive long enough at an infectious dose and be a strain that is able to colonize humans to cause infection. We propose that future research should focus on the large number of under-studied species commonly in contact with people and food production and demonstrate shedding of bacterial strains pathogenic to humans into the environment where people may contact them. Finally, studies assessing the duration and intensity of bacterial shedding and survival of bacteria in the environment in bird faeces will help provide crucial missing information necessary to calculate spillover probability. Addressing these essential knowledge gaps will support policy to reduce enteric pathogen spillover to humans and enhance bird conservation efforts that are currently undermined by unsupported fears of pathogen spillover from wild birds.
ABSTRACT Background/Question/Methods The vertebrate immune system utilizes physiological resource... more ABSTRACT Background/Question/Methods The vertebrate immune system utilizes physiological resources to produce the diverse cells and proteins that provide defense against infectious organisms (parasites). Hypothetically, the resources allocated to the immune system must be traded against other physiological demands (e.g. growth). These internal trade-offs are believed to drive the variation in immune function often observed among individuals. These resource constraints begin with the diet itself, since nutrients and calories vary with food quantity and quality. Here we ask if diet manipulation affects immune function of a deer mouse (Peromyscus maniculatus) through its ability to gain resistance to an ectoparasite, the Rocky Mountain wood tick (Dermacentor andersoni). Four distinct diet groups were created using mixtures of arthropods and seeds. The range of diets included ratios of seeds versus arthropods at the limits of mouse homeostasis (i.e. further dietary skew produced rapid weight loss and mortality). Mice were fed the controlled diets before and during 2 tick infestation periods where each mouse was inoculated with 50 wood tick larvae. Engorged ticks were recovered and counted from each mouse during both infestations to determine the relative susceptibility/resistance to ticks among the mouse diet groups. Results/Conclusions Mouse body weight was affected by diet and parasitism. In general mice lost weight during periods of infestation and regained weight during the time between infestations. Mice fed a diet skewed toward arthropods lost weight more rapidly during infestations than mice fed a diet skewed toward seeds. Within an infestation period the number of ticks that successfully obtained blood meals was unaffected by the variation in host diet. Significantly fewer ticks fed on mice during the second infestation compared to the first infestation, which indicated that mice acquired resistance to tick blood feeding during the initial exposure. This observation mirrors results of other experiments demonstrating deer mice will develop resistance to Rocky Mountain wood ticks. These results suggest diet affects body mass during parasitism, but immune defense remains intact regardless of dietary differences. This has implications for the interactions between host ecology and infectious disease. Though host condition (body weight) may be influenced by the interaction between food resources and infection, immune defense may remain intact even when dietary resources change over space and time. Ongoing work is also examining the effect of diet on immune function relative to parasitism by wood ticks through manipulation of food abundance.
Commercial vaccines based on the tick gut protein Bm86 have been successful in controlling the on... more Commercial vaccines based on the tick gut protein Bm86 have been successful in controlling the onehost tick Rhipicephalus (Boophilus) microplus and provide heterologous protection against certain other non-target ixodid tick species. This cross protection, however, does not extend to the three-host tick R. appendiculatus, the vector of the protozoan parasite Theileria parva. When transmitted to cattle, T. parva causes the often fatal disease East Coast fever. Here, we used insect cell-expressed recombinant versions of the R. appendiculatus homologs of Bm86, named Ra86, to vaccinate cattle. We measured multiple fitness characteristics for ticks that were fed on cattle Ra86-vaccinated or unvaccinated. The Ra86 vaccination of cattle significantly decreased the molting success of nymphal ticks to the adult stage. Modeling simulations based on our empirical data suggest that repeated vaccinations using Ra86 could reduce tick populations over successive generations. Vaccination with Ra86 could thus form a component of integrated control strategies for R. appendiculatus leading to a reduction in use of environmentally damaging acaricides.
Background: Maternal antibodies are believed to play an integral role in protecting immunological... more Background: Maternal antibodies are believed to play an integral role in protecting immunologically immature wildpasserines from environmental antigens. This study comprehensively examines the early development of the adaptive immune system in an altricial-developing wild passerine species, the house sparrow (Passer domestics), by characterizing the half-life of maternal antibodies in nestling plasma, the onset of de novo synthesis of endogenous antibodies by nestlings, and the timing of immunological independence, where nestlings rely entirely on their own antibodies for immunologic protection. Methodology/Principal Findings: In an aviary study we vaccinated females against a novel antigen that these birds would not otherwise encounter in their natural environment, and measured both antigen-specific and total antibody concentration in the plasma of females, yolks, and nestlings. We traced the transfer of maternal antibodies from females to nestlings through the yolk and measured catabolisation of maternal antigen-specific antibodies in nestlings during early development. By utilizing measurements of non-specific and specific antibody levels in nestling plasma we were able to calculate the half-life of maternal antibodies in nestling plasma and the time point at which nestling were capable of synthesizing antibodies themselves. Based on the short half-life of maternal antibodies, the rapid production of endogenous antibodies by nestlings and the relatively low transfer of maternal antibodies to nestlings, our findings suggest that altricialdeveloping sparrows achieve immunologic independence much earlier than precocial birds. Conclusions/Significance: To our knowledge, this is the first in depth analyses performed on the adaptive immune system of a wild-passerine species. Our results suggest that maternal antibodies may not confer the immunologic protection or immune priming previously proposed in other passerine studies. Further research needs to be conducted on other altricial passerines to determine if the results of our study are a species-specific phenomenon or if they apply to all altricialdeveloping birds.
Arthropod-borne viruses (arboviruses) threaten the health of humans, livestock, and wildlife. Wes... more Arthropod-borne viruses (arboviruses) threaten the health of humans, livestock, and wildlife. West Nile virus (WNV), the world's most widespread arbovirus, invaded the United States in 1999 and rapidly spread across the county. Although the ecology of vectors and hosts are key determinants of WNV prevalence across landscapes, the factors shaping local vector and host populations remain unclear. Here, we used spatially-explicit models to evaluate how three land-use types (orchards, vegetable/forage crops, natural) and two climatic variables (temperature, precipitation) influence the prevalence of WNV infections and vector/host distributions at landscape and local spatial scales. Across landscapes, we show that orchard habitats were associated with greater prevalence of WNV infections in reservoirs (birds) and incidental hosts (horses), while increased precipitation was associated with fewer infections. At local scales, orchard habitats increased the prevalence of WNV infections in vectors (mosquitoes) and the abundance of mosquitoes and two key reservoir species, the American robin and the house sparrow. Thus, orchard habitats benefitted WNV vectors and reservoir hosts locally, creating focal points for the transmission of WNV at landscape scales in the presence of suitable climatic conditions.
Background: Ectoparasites rely on blood-feeding to sustain activity, support development and prod... more Background: Ectoparasites rely on blood-feeding to sustain activity, support development and produce offspring. Blood-feeding is also a route for transmission of diverse vector-borne pathogens. The likelihood of successfully feeding is thus an important aspect of ectoparasite population dynamics and pathogen transmission. Factors that affect blood-feeding include ectoparasite density, host defenses, and ages of the host and ectoparasite. How these factors interact to affect feeding success is not well understood. Methods: We monitored blood-feeding success of larval Rocky Mountain wood ticks (RMWTs; Dermacentor andersoni) on deer mice (Peromyscus maniculatus) in several experiments to determine how tick density, host defense, and ages of mice and ticks interact to influence feeding success. In the first experiment, tick-naive deer mice were infested with one of several densities of RMWT larvae, while a second cohort of mice were infested with 50 larvae each. Two weeks after ticks dropped off, mice in the first cohort were re-exposed to 50 larvae each and mice in the second cohort were re-exposed to varying densities of larvae. In the second experiment mice of different ages (45-374 days old) were exposed to 50 larvae each. Two weeks later mice were re-exposed to 50 larvae each. We combined data from these and several similar experiments to test the generality of the patterns we observed. Lastly, we tested whether tick feeding success was consistent on individual mice that were challenged on four occasions. Results: Mice acquired resistance such that feeding success declined dramatically from the first to the second infestation. Feeding success also declined with tick density and tick age. Mice, however, became more permissive with age. The sizes of these effects were similar and additive. Surprisingly, over successive infestations the relative resistance among mice changed among hosts within a cohort. Conclusions: We predict that larval blood-feeding success, and thus development to the nymph stage, will change due to variation in tick age and density, as well as the age and history of the host. Incorporating these biotic factors into modeling of tick population dynamics may improve predictions of tick-borne pathogen transmission.
1. Farmland diversification practices are increasingly adopted to help reverse biodiversity decli... more 1. Farmland diversification practices are increasingly adopted to help reverse biodiversity declines in agroecosystems. However, evidence for the effectiveness of this approach often comes from documenting the species attracted to particular farming systems or landscapes, rather than their underlying physiological states that ultimately determine population growth or decline over the longer term. 2. Across 38 organic, mixed-produce farms spanning the U.S. west coast, we quantified three physiological biomarkers that are widely used to capture variation in short and long-term stress responses for nine bird species with diverse life-history traits. While controlling for other potentially confounding variables, we used multilevel models to examine the association between bird physiological conditions, landscape context and local farm management practices, including the integration of livestock, and cropland composition and configuration. 3. Birds generally had lower stress responses on more-locally-diverse farms and in landscapes with higher amounts of seminatural cover. However, interactions between farm diversity and landscape context suggested birds were less stressed on more diverse farms in simpler landscapes, but more stressed and in poorer condition on more diverse farms embedded within complex landscapes. 4. We found no differences in stress responses among birds in relation to their degree of human association (synanthropy), which suggests generality in our findings. 5. Synthesis and application. Birds were often less stressed on more diverse farms. However, these patterns were mediated by landscape context: birds were less stressed on more diverse farms in simplified landscapes, but more stressed on more diverse farms within complex landscapes. This means land managers might not see uniform effects of local diversification schemes across different landscape contexts. Our results underscore the need to consider responses related to physiological health status, in addition to species richness and abundance, [...]
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Papers by Jeb Owen