Extreme heat reduces host and parasite performance in a butterfly-parasite interaction.

Environmental temperature fundamentally shapes insect physiology, fitness and interactions with parasites. Differential climate warming effects on host versus parasite biology could exacerbate or inhibit parasite transmission, with far-reaching implications for pollination services, biocontrol and human health. Here, we experimentally test how controlled temperatures influence multiple components of host and parasite fitness in monarch butterflies (Danaus plexippus) and their protozoan parasites Ophryocystis elektroscirrha. Using five constant-temperature treatments spanning 18-34°C, we measured monarch development, survival, size, immune function and parasite infection status and intensity. Monarch size and survival declined sharply at the hottest temperature (34°C), as did infection probability, suggesting that extreme heat decreases both host and parasite performance. The lack of infection at 34°C was not due to greater host immunity or faster host development but could instead reflect the thermal limits of parasite invasion and within-host replication. In the context of ongoing climate change, temperature increases above current thermal maxima could reduce the fitness of both monarchs and their parasites, with lower infection rates potentially balancing negative impacts of extreme heat on future monarch abundance and distribution.

Interactions between parasitism and migration in monarch butterflies.

In many species, migration can increase parasite burdens or diversity as hosts move between diverse habitats with different parasite assemblages. On the other hand, migration can reduce parasite prevalence by letting animals escape infested habitats, or by exacerbating the costs of parasitism, leading to culling or dropout. How the balance between these negative and positive interactions is maintained or how they will change under anthropogenic pressure remains poorly understood. Here, we summarize the relationship between migration and infectious disease in monarch butterflies, finding that migration can reduce parasite prevalence through a combination of migratory culling and dropout. Because parasite prevalence has risen in recent decades, these processes are now resulting in the loss of tens of millions of monarchs. We highlight the remaining questions, asking how migration influences population genetics and virulence, how the establishment of resident populations interferes with migration, and whether infection can interfere with migratory cognition.

Land use, season, and parasitism predict metal concentrations in Australian flying fox fur.

Urban-living wildlife can be exposed to metal contaminants dispersed into the environment through industrial, residential, and agricultural applications. Metal exposure carries lethal and sublethal consequences for animals; in particular, heavy metals (e.g. arsenic, lead, mercury) can damage organs and act as carcinogens. Many bat species reside and forage in human-modified habitats and could be exposed to contaminants in air, water, and food. We quantified metal concentrations in fur samples from three flying fox species (Pteropus fruit bats) captured at eight sites in eastern Australia. For subsets of bats, we assessed ectoparasite burden, haemoparasite infection, and viral infection, and performed white blood cell differential counts. We examined relationships among metal concentrations, environmental predictors (season, land use surrounding capture site), and individual predictors (species, sex, age, body condition, parasitism, neutrophil:lymphocyte ratio). As expected, bats captured at sites with greater human impact had higher metal loads. At one site with seasonal sampling, bats had higher metal concentrations in winter than in summer, possibly owing to changes in food availability and foraging. Relationships between ectoparasites and metal concentrations were mixed, suggesting multiple causal mechanisms. There was no association between overall metal load and neutrophil:lymphocyte ratio, but mercury concentrations were positively correlated with this ratio, which is associated with stress in other vertebrate taxa. Comparison of our findings to those of previous flying fox studies revealed potentially harmful levels of several metals; in particular, endangered spectacled flying foxes (P. conspicillatus) exhibited high concentrations of cadmium and lead. Because some bats harbor pathogens transmissible to humans and animals, future research should explore interactions between metal exposure, immunity, and infection to assess consequences for bat and human health.

Parasite dynamics in North American monarchs predicted by host density and seasonal migratory culling.

Insect-pathogen dynamics can show seasonal and inter-annual variations that covary with fluctuations in insect abundance and climate. Long-term analyses are especially needed to track parasite dynamics in migratory insects, in part because their vast habitat ranges and high mobility might dampen local effects of density and climate on infection prevalence. Monarch butterflies Danaus plexippus are commonly infected with the protozoan Ophryocystis elektroscirrha (OE). Because this parasite lowers monarch survival and flight performance, and because migratory monarchs have experienced declines in recent decades, it is important to understand the patterns and drivers of infection. Here we compiled data on OE infection spanning 50 years, from wild monarchs sampled in the United States, Canada and Mexico during summer breeding, fall migrating and overwintering periods. We examined eastern versus western North American monarchs separately, to ask how abundance estimates, resource availability, climate and breeding season length impact infection trends. We further assessed the intensity of migratory culling, which occurs when infected individuals are removed from the population during migration. Average infection prevalence was four times higher in western compared to eastern subpopulations. In eastern North America, the proportion of infected monarchs increased threefold since the mid-2000s. In the western region, the proportion of infected monarchs declined sharply from 2000 to 2015, and increased thereafter. For both eastern and western subpopulations, years with greater summer adult abundance predicted greater infection prevalence, indicating that transmission increases with host breeding density. Environmental variables (temperature and NDVI) were not associated with changes in the proportion of infected adults. We found evidence for migratory culling of infected butterflies, based on declines in parasitism during fall migration. We estimated that tens of millions fewer monarchs reach overwintering sites in Mexico as a result of OE, highlighting the need to consider the parasite as a potential threat to the monarch population. Increases in infection among eastern North American monarchs post-2002 suggest that changes to the host's ecology or environment have intensified parasite transmission. Further work is needed to examine the degree to which human practices, such as mass caterpillar rearing and the widespread planting of exotic milkweed, have contributed to this trend.

Habitat Specialization by Wildlife Reduces Pathogen Spread in Urbanizing Landscapes.

AbstractUrban areas are expanding globally with far-reaching ecological consequences, including for wildlife-pathogen interactions. Wildlife show tremendous variation in their responses to urbanization; even within a single population, some individuals can specialize on urban or natural habitat types. This specialization could alter pathogen impacts on host populations via changes to wildlife movement and aggregation. Here, we build a mechanistic model to explore how habitat specialization in urban landscapes affects interactions between a mobile host population and a density-dependent specialist pathogen that confers no immunity. We model movement on a network of resource-stable urban sites and resource-fluctuating natural sites, where hosts are urban specialists, natural specialists, or generalists that use both patch types. We find that for generalists, natural and partially urban landscapes produce the highest infection prevalence and mortality, driven by high movement rates at natural sites and high densities at urban sites. However, habitat specialization protects hosts from these negative effects of partially urban landscapes by limiting movement between patch types. These findings suggest that habitat specialization can benefit populations by reducing infectious disease transmission, but by reducing movement between habitat types it could also carry the cost of reducing other movement-related ecosystem functions, such as seed dispersal and pollination.

Host Plant Species Mediates Impact of Neonicotinoid Exposure to Monarch Butterflies.

Neonicotinoids are the most widely used insecticides in North America. Numerous studies document the negative effects of neonicotinoids on bees, and it remains crucial to demonstrate if neonicotinoids affect other non-target insects, such as butterflies. Here we examine how two neonicotinoids (imidacloprid and clothianidin) affect the development, survival, and flight of monarch butterflies, and how these chemicals interact with the monarch's milkweed host plant. We first fed caterpillars field-relevant low doses (0.075 and 0.225 ng/g) of neonicotinoids applied to milkweed leaves (Asclepias incarnata), and found no significant reductions in larval development rate, pre-adult survival, or adult flight performance. We next fed larvae higher neonicotinoid doses (4-70 ng/g) and reared them on milkweed species known to produce low, moderate, or high levels of secondary toxins (cardenolides). Monarchs exposed to the highest dose of clothianidin (51-70 ng/g) experienced pupal deformity, low survival to eclosion, smaller body size, and weaker adult grip strength. This effect was most evident for monarchs reared on the lowest cardenolide milkweed (A. incarnata), whereas monarchs reared on the high-cardenolide A. curassavica showed no significant reductions in any variable measured. Our results indicate that monarchs are tolerant to low doses of neonicotinoid, and that negative impacts of neonicotinoids depend on host plant type. Plant toxins may confer protective effects or leaf physical properties may affect chemical retention. Although neonicotinoid residues are ubiquitous on milkweeds in agricultural and ornamental settings, commonly encountered doses below 50 ng/g are unlikely to cause substantial declines in monarch survival or migratory performance.

Thermal tolerance and environmental persistence of a protozoan parasite in monarch butterflies.

Many parasites have external transmission stages that persist in the environment prior to infecting a new host. Understanding how long these stages can persist, and how abiotic conditions such as temperature affect parasite persistence, is important for predicting infection dynamics and parasite responses to future environmental change. In this study, we explored environmental persistence and thermal tolerance of a debilitating protozoan parasite that infects monarch butterflies. Parasite transmission occurs when dormant spores, shed by adult butterflies onto host plants and other surfaces, are later consumed by caterpillars. We exposed parasite spores to a gradient of ecologically-relevant temperatures for 2, 35, or 93 weeks. We tested spore viability by feeding controlled spore doses to susceptible monarch larvae, and examined relationships between temperature, time, and resulting infection metrics. We also examined whether distinct parasite genotypes derived from replicate migratory and resident monarch populations differed in their thermal tolerance. Finally, we examined evidence for a trade-off between short-term within-host replication and long-term persistence ability. Parasite viability decreased in response to warmer temperatures over moderate-to-long time scales. Individual parasite genotypes showed high heterogeneity in viability, but differences did not cluster by migratory vs. resident monarch populations. We found no support for a negative relationship between environmental persistence and within-host replication, as might be expected if parasites invest in short-term reproduction at the cost of longer-term survival. Findings here indicate that dormant spores can survive for many months under cooler conditions, and that heat dramatically shortens the window of transmission for this widespread and virulent butterfly parasite.

Urban specialization reduces habitat connectivity by a highly mobile wading bird.

BACKGROUND: Mobile animals transport nutrients and propagules across habitats, and are crucial for the functioning of food webs and for ecosystem services. Human activities such as urbanization can alter animal movement behavior, including site fidelity and resource use. Because many urban areas are adjacent to natural sites, mobile animals might connect natural and urban habitats. More generally, understanding animal movement patterns in urban areas can help predict how urban expansion will affect the roles of highly mobile animals in ecological processes. METHODS: Here, we examined movements by a seasonally nomadic wading bird, the American white ibis (Eudocimus albus), in South Florida, USA. White ibis are colonial wading birds that forage on aquatic prey; in recent years, some ibis have shifted their behavior to forage in urban parks, where they are fed by people. We used a spatial network approach to investigate how individual movement patterns influence connectivity between urban and non-urban sites. We built a network of habitat connectivity using GPS tracking data from ibis during their non-breeding season and compared this network to simulated networks that assumed individuals moved indiscriminately with respect to habitat type. RESULTS: We found that the observed network was less connected than the simulated networks, that urban-urban and natural-natural connections were strong, and that individuals using urban sites had the least-variable habitat use. Importantly, the few ibis that used both urban and natural habitats contributed the most to connectivity. CONCLUSIONS: Habitat specialization in urban-acclimated wildlife could reduce the exchange of propagules and nutrients between urban and natural areas, which has consequences both for beneficial effects of connectivity such as gene flow and for detrimental effects such as the spread of contaminants or pathogens.

Landscape-level toxicant exposure mediates infection impacts on wildlife populations.

Anthropogenic landscape modification such as urbanization can expose wildlife to toxicants, with profound behavioural and health effects. Toxicant exposure can alter the local transmission of wildlife diseases by reducing survival or altering immune defence. However, predicting the impacts of pathogens on wildlife across their ranges is complicated by heterogeneity in toxicant exposure across the landscape, especially if toxicants alter wildlife movement from toxicant-contaminated to uncontaminated habitats. We developed a mechanistic model to explore how toxicant effects on host health and movement propensity influence range-wide pathogen transmission, and zoonotic exposure risk, as an increasing fraction of the landscape is toxicant-contaminated. When toxicant-contaminated habitat is scarce on the landscape, costs to movement and survival from toxicant exposure can trap infected animals in contaminated habitat and reduce landscape-level transmission. Increasing the proportion of contaminated habitat causes host population declines from combined effects of toxicants and infection. The onset of host declines precedes an increase in the density of infected hosts in contaminated habitat and thus may serve as an early warning of increasing potential for zoonotic spillover in urbanizing landscapes. These results highlight how sublethal effects of toxicants can determine pathogen impacts on wildlife populations that may not manifest until landscape contamination is widespread.

Movement rules determine nomadic species' responses to resource supplementation and degradation.

In environments that vary unpredictably, many animals are nomadic, moving in an irregular pattern that differs from year to year. Exploring the mechanisms of nomadic movement is needed to understand how animals survive in highly variable environments, and to predict behavioural and population responses to environmental change. We developed a network model to identify plausible mechanisms of nomadic animal movement by comparing the performance of multiple movement rules along a continuum from nomadism to residency. Using simulations and analytical results, we explored how different types of habitat modifications (that augment or decrease resource availability) might affect the abundance and movement rates of animals following each of these rules. Movement rules for which departure from patches depended on resource availability and/or competition performed almost equally well and better than residency or uninformed movement under most conditions, even though animals using each rule moved at substantially different rates. Habitat modifications that stabilized resources, either by resource supplementation or degradation, eroded the benefits of informed nomadic movements, particularly for movements based on resource availability alone. These results suggest that simple movement rules can explain nomadic animal movements and determine species' responses to environmental change. In particular, landscape stabilization and supplementation might be useful strategies for promoting populations of resident animals, but would be less beneficial for managing highly mobile species, many of which are threatened by habitat disruption and changes in climate.

Ecological and evolutionary drivers of haemoplasma infection and bacterial genotype sharing in a Neotropical bat community.

Most emerging pathogens can infect multiple species, underlining the importance of understanding the ecological and evolutionary factors that allow some hosts to harbour greater infection prevalence and share pathogens with other species. However, our understanding of pathogen jumps is based primarily around viruses, despite bacteria accounting for the greatest proportion of zoonoses. Because bacterial pathogens in bats (order Chiroptera) can have conservation and human health consequences, studies that examine the ecological and evolutionary drivers of bacterial prevalence and barriers to pathogen sharing are crucially needed. Here were studied haemotropic Mycoplasma spp. (i.e., haemoplasmas) across a species-rich bat community in Belize over two years. Across 469 bats spanning 33 species, half of individuals and two-thirds of species were haemoplasma positive. Infection prevalence was higher for males and for species with larger body mass and colony sizes. Haemoplasmas displayed high genetic diversity (21 novel genotypes) and strong host specificity. Evolutionary patterns supported codivergence of bats and bacterial genotypes alongside phylogenetically constrained host shifts. Bat species centrality to the network of shared haemoplasma genotypes was phylogenetically clustered and unrelated to prevalence, further suggesting rare-but detectable-bacterial sharing between species. Our study highlights the importance of using fine phylogenetic scales when assessing host specificity and suggests phylogenetic similarity may play a key role in host shifts not only for viruses but also for bacteria. Such work more broadly contributes to increasing efforts to understand cross-species transmission and the epidemiological consequences of bacterial pathogens.

Planting gardens to support insect pollinators.

Global insect pollinator declines have prompted habitat restoration efforts, including pollinator-friendly gardening. Gardens can provide nectar and pollen for adult insects and offer reproductive resources, such as nesting sites and caterpillar host plants. We conducted a review and meta-analysis to examine how decisions made by gardeners on plant selection and garden maintenance influence pollinator survival, abundance, and diversity. We also considered characteristics of surrounding landscapes and the impacts of pollinator natural enemies. Our results indicated that pollinators responded positively to high plant species diversity, woody vegetation, garden size, and sun exposure and negatively to the separation of garden habitats from natural sites. Within-garden features more strongly influenced pollinators than surrounding landscape factors. Growing interest in gardening for pollinators highlights the need to better understand how gardens contribute to pollinator conservation and how some garden characteristics can enhance the attractiveness and usefulness of gardens to pollinators. Further studies examining pollinator reproduction, resource acquisition, and natural enemies in gardens and comparing gardens with other restoration efforts and to natural habitats are needed to increase the value of human-made habitats for pollinators.

Siembra jardines para dar soporte a los insectos polinizadores Resumen La declinación mundial de insectos polinizadores ha dado pie a esfuerzos de restauración, incluyendo la jardinería amigable con los polinizadores. Los jardines pueden proporcionar néctar y polen para los insectos adultos y también pueden ofrecer recursos reproductivos, como sitios de anidación y plantas hospederas para las orugas. Realizamos una revisión y un meta-análisis para examinar cómo las decisiones que toman los jardineros relacionadas a la selección de plantas y el mantenimiento del jardín influyen se la supervivencia, abundancia y diversidad de los polinizadores. También consideramos las características de los paisajes vecinos y los impactos de los enemigos naturales de los polinizadores. Nuestros resultados indicaron que los polinizadores respondieron positivamente a la alta diversidad de especies de plantas, la vegetación leñosa, el tamaño del jardín y la exposición al sol, mientras que respondieron negativamente a la separación entre los jardines y los sitios naturales. Las características intrínsecas de los jardines tuvieron una mayor influencia sobre los polinizadores que los factores del paisaje vecino. El creciente interés por la jardinería para polinizadores resalta la necesidad de entender como los jardines contribuyen a la conservación y como algunas características de los jardines pueden incrementar lo útil y atractivo de los jardines para los polinizadores. Se requieren estudios más profundos que examinen la reproducción de los polinizadores, la adquisición de recursos y los enemigos naturales en los jardines, y también que comparen a los jardines con otros esfuerzos de restauración y con los hábitats naturales para incrementar el valor de los hábitats para polinizadores creados por humanos.

Multiple transmission routes sustain high prevalence of a virulent parasite in a butterfly host.

Understanding factors that allow highly virulent parasites to reach high infection prevalence in host populations is important for managing infection risks to human and wildlife health. Multiple transmission routes have been proposed as one mechanism by which virulent pathogens can achieve high prevalence, underscoring the need to investigate this hypothesis through an integrated modelling-empirical framework. Here, we examine a harmful specialist protozoan infecting monarch butterflies that commonly reaches high prevalence (50-100%) in resident populations. We integrate field and modelling work to show that a combination of three empirically-supported transmission routes (vertical, adult transfer and environmental transmission) can produce and sustain high infection prevalence in this system. Although horizontal transmission is necessary for parasite invasion, most new infections post-establishment arise from vertical transmission. Our study predicts that multiple transmission routes, coupled with high parasite virulence, can reduce resident host abundance by up to 50%, suggesting that the protozoan could contribute to declines of North American monarchs.

Exposure to Non-Native Tropical Milkweed Promotes Reproductive Development in Migratory Monarch Butterflies.

BACKGROUND: North American monarchs (Danaus plexippus) are well-known for their long-distance migrations; however, some monarchs within the migratory range have adopted a resident lifestyle and breed year-round at sites where tropical milkweed (Asclepias curassavica) is planted in the southern coastal United States. An important question is whether exposure to exotic milkweed alters monarch migratory physiology, particularly the ability to enter and remain in the hormonally-induced state of reproductive diapause, whereby adults delay reproductive maturity. Cued by cooler temperatures and shorter photoperiods, diapause is a component of the monarch's migratory syndrome that includes directional flight behavior, lipid accumulation, and the exceptional longevity of the migratory generation. METHODS: Here, we experimentally test how exposure to tropical milkweed during the larval and adult stages influences monarch reproductive status during fall migration. Caterpillars reared under fall-like conditions were fed tropical versus native milkweed diets, and wild adult migrants were placed in outdoor flight cages with tropical milkweed, native milkweed, or no milkweed. RESULTS: We found that monarchs exposed to tropical milkweed as larvae were more likely to be reproductively active (exhibit mating behavior in males and develop mature eggs in females) compared to monarchs exposed to native milkweed. Among wild-caught fall migrants, females exposed to tropical milkweed showed greater egg development than females exposed to native or no milkweed, although a similar response was not observed for males. CONCLUSIONS: Our study provides evidence that exposure to tropical milkweed can increase monarch reproductive activity, which could promote continued residency at year-round breeding sites and decrease monarch migratory propensity.

The changing ecology of primate parasites: Insights from wild-captive comparisons.

Host movements, including migrations or range expansions, are known to influence parasite communities. Transitions to captivity-a rarely studied yet widespread human-driven host movement-can also change parasite communities, in some cases leading to pathogen spillover among wildlife species, or between wildlife and human hosts. We compared parasite species richness between wild and captive populations of 22 primate species, including macro- (helminths and arthropods) and micro-parasites (viruses, protozoa, bacteria, and fungi). We predicted that captive primates would have only a subset of their native parasite community, and would possess fewer parasites with complex life cycles requiring intermediate hosts or vectors. We further predicted that captive primates would have parasites transmitted by close contact and environmentally-including those shared with humans and other animals, such as commensals and pests. We found that the composition of primate parasite communities shifted in captive populations, especially because of turnover (parasites detected in captivity but not reported in the wild), but with some evidence of nestedness (holdovers from the wild). Because of the high degree of turnover, we found no significant difference in overall parasite richness between captive and wild primates. Vector-borne parasites were less likely to be found in captivity, whereas parasites transmitted through either close or non-close contact, including through fecal-oral transmission, were more likely to be newly detected in captivity. These findings identify parasites that require monitoring in captivity and raise concerns about the introduction of novel parasites to potentially susceptible wildlife populations during reintroduction programs.

Leukocyte Profiles Reflect Geographic Range Limits in a Widespread Neotropical Bat.

Quantifying how the environment shapes host immune defense is important for understanding which wild populations may be more susceptible or resistant to pathogens. Spatial variation in parasite risk, food and predator abundance, and abiotic conditions can each affect immunity, and these factors can also manifest at both local and biogeographic scales. Yet identifying predictors and the spatial scale of their effects is limited by the rarity of studies that measure immunity across many populations of broadly distributed species. We analyzed leukocyte profiles from 39 wild populations of the common vampire bat (Desmodus rotundus) across its wide geographic range throughout the Neotropics. White blood cell differentials varied spatially, with proportions of neutrophils and lymphocytes varying up to six-fold across sites. Leukocyte profiles were spatially autocorrelated at small and very large distances, suggesting that local environment and large-scale biogeographic factors influence cellular immunity. Generalized additive models showed that bat populations closer to the northern and southern limits of the species range had more neutrophils, monocytes, and basophils, but fewer lymphocytes and eosinophils, than bats sampled at the core of their distribution. Habitats with access to more livestock also showed similar patterns in leukocyte profiles, but large-scale patterns were partly confounded by time between capture and sampling across sites. Our findings suggest that populations at the edge of their range experience physiologically limiting conditions that predict higher chronic stress and greater investment in cellular innate immunity. High food abundance in livestock-dense habitats may exacerbate such conditions by increasing bat density or diet homogenization, although future spatially and temporally coordinated field studies with common protocols are needed to limit sampling artifacts. Systematically assessing immune function and response over space will elucidate how environmental conditions influence traits relevant to epidemiology and help predict disease risks with anthropogenic disturbance, land conversion, and climate change.

Parasite sharing in wild ungulates and their predators: Effects of phylogeny, range overlap, and trophic links.

Understanding factors that facilitate interspecific pathogen transmission is a central issue for conservation, agriculture, and human health. Past work showed that host phylogenetic relatedness and geographical proximity can increase cross-species transmission, but further work is needed to examine the importance of host traits, and species interactions such as predation, in determining the degree to which parasites are shared between hosts. Here we consider the factors that predict patterns of parasite sharing across a diverse assemblage of 116 wild ungulates (i.e., hoofed mammals in the Artiodactyla and Perissodactyla) and nearly 900 species of micro- and macroparasites, controlling for differences in total parasite richness and host sampling effort. We also consider the effects of trophic links on parasite sharing between ungulates and carnivores. We tested for the relative influence of range overlap, phylogenetic distance, body mass, and ecological dissimilarity (i.e., the distance separating species in a Euclidean distance matrix based on standardized traits) on parasite sharing. We also tested for the effects of variation in study effort as a potential source of bias in our data, and tested whether carnivores reported to feed on ungulates have more ungulate parasites than those that use other resources. As in other groups, geographical range overlap and phylogenetic similarity predicted greater parasite community similarity in ungulates. Ecological dissimilarity showed a weak negative relationship with parasite sharing. Counter to our expectations, differences, not similarity, in host body mass predicted greater parasite sharing between pairs of ungulate hosts. Pairs of well-studied host species showed higher overlap than poorly studied species, although including sampling effort did not reduce the importance of biological traits in our models. Finally, carnivores that feed on ungulates harboured a greater richness of ungulate helminths. Overall, we show that the factors that predict parasite sharing in wild ungulates are similar to those known for other mammal groups, and demonstrate the importance of controlling for heterogeneity in host sampling effort in future analyses of parasite sharing. We also show that ecological interactions, in this case trophic links via predation, can allow sharing of some parasite species among distantly related host species.

On the relationship between body condition and parasite infection in wildlife: a review and meta-analysis.

Body condition metrics are widely used to infer animal health and to assess costs of parasite infection. Since parasites harm their hosts, ecologists might expect negative relationships between infection and condition in wildlife, but this assumption is challenged by studies showing positive or null condition-infection relationships. Here, we outline common condition metrics used by ecologists in studies of parasitism, and consider mechanisms that cause negative, positive, and null condition-infection relationships in wildlife systems. We then perform a meta-analysis of 553 condition-infection relationships from 187 peer-reviewed studies of animal hosts, analysing observational and experimental records separately, and noting whether authors measured binary infection status or intensity. Our analysis finds substantial heterogeneity in the strength and direction of condition-infection relationships, a small, negative average effect size that is stronger in experimental studies, and evidence for publication bias towards negative relationships. The strongest predictors of variation in study outcomes are host thermoregulation and the methods used to evaluate body condition. We recommend that studies aiming to assess parasite impacts on body condition should consider host-parasite biology, choose condition measures that can change during the course of infection, and employ longitudinal surveys or manipulate infection status when feasible.

Genetic diversity, infection prevalence, and possible transmission routes of Bartonella spp. in vampire bats.

Bartonella spp. are globally distributed bacteria that cause endocarditis in humans and domestic animals. Recent work has suggested bats as zoonotic reservoirs of some human Bartonella infections; however, the ecological and spatiotemporal patterns of infection in bats remain largely unknown. Here we studied the genetic diversity, prevalence of infection across seasons and years, individual risk factors, and possible transmission routes of Bartonella in populations of common vampire bats (Desmodus rotundus) in Peru and Belize, for which high infection prevalence has previously been reported. Phylogenetic analysis of the gltA gene for a subset of PCR-positive blood samples revealed sequences that were related to Bartonella described from vampire bats from Mexico, other Neotropical bat species, and streblid bat flies. Sequences associated with vampire bats clustered significantly by country but commonly spanned Central and South America, implying limited spatial structure. Stable and nonzero Bartonella prevalence between years supported endemic transmission in all sites. The odds of Bartonella infection for individual bats was unrelated to the intensity of bat flies ectoparasitism, but nearly all infected bats were infested, which precluded conclusive assessment of support for vector-borne transmission. While metagenomic sequencing found no strong evidence of Bartonella DNA in pooled bat saliva and fecal samples, we detected PCR positivity in individual saliva and feces, suggesting the potential for bacterial transmission through both direct contact (i.e., biting) and environmental (i.e., fecal) exposures. Further investigating the relative contributions of direct contact, environmental, and vector-borne transmission for bat Bartonella is an important next step to predict infection dynamics within bats and the risks of human and livestock exposures.

Host Dispersal Responses to Resource Supplementation Determine Pathogen Spread in Wildlife Metapopulations.

Many wildlife species occupy landscapes that vary in the distribution, abundance, and quality of food resources. Increasingly, urbanized and agricultural habitats provide supplemental food resources that can have profound consequences for host distributions, movement patterns, and pathogen exposure. Understanding how host and pathogen dispersal across landscapes is affected by the spatial extent of food-supplemented habitats is therefore important for predicting the consequences for pathogen spread and impacts on host occupancy. Here we develop a generalizable metapopulation model to understand how the relative abundance of provisioned habitats across the landscape and how the host dispersal responses to provisioning and infection influence patch occupancy by hosts and their pathogens. We find that pathogen invasion and landscape-level infection prevalence are greatest when provisioning increases patch attractiveness and disperser production and when infection has minimal costs on dispersal success. Alternatively, if provisioning promotes site fidelity or reduces disperser production, increasing the fraction of food-supplemented habitats can reduce landscape-scale infection prevalence and minimize disease-induced declines in host occupancy. This work highlights the importance of considering how resources and infection jointly influence host dispersal for predicting how changing resource distributions influence the spread of infectious diseases.