Multi-host Communities Research Articles

Dose relationships can exacerbate, mute, or reverse the impact of heterospecific host density on infection prevalence.

The likelihood an individual becomes infected depends on the community in which it is embedded. For environmentally transmitted parasites, host community composition can alter host density, the density of parasites that hosts encounter in the environment, and the dose to which hosts are subsequently exposed. While some multi-host theory incorporates some of these factors (e.g., competition among hosts), it does not currently consider the nonlinear relationships between parasite exposure dose and per-propagule infectivity (dose-infectivity relationships), between exposure dose and infected host mortality (dose-mortality relationships), and between exposure dose and parasite propagule excretion (dose-excretion relationships). This makes it difficult to predict the impact of host species on one another's likelihood of infection. To understand the implications of these nonlinear dose relationships for multi-host communities, we first performed a meta-analysis on published dose-infectivity experiments to quantify the proportion of accelerating, linear, or decelerating dose-infectivity relationships; we found that most experiments demonstrated decelerating dose-infectivity relationships. We then explored how dose-infectivity, dose-mortality, and dose-excretion relationships might alter the impact of heterospecific host density on infectious propagule density, infection prevalence, and density of a focal host using two-host, one-parasite models. We found that dose relationships either decreased the magnitude of the impact of heterospecific host density on propagule density and infection prevalence via negative feedback loops (decelerating dose-infectivity relationships, positive dose-mortality relationships, and negative dose-excretion relationships), or increased the magnitude of the impact of heterospecific host density on infection prevalence via positive feedback loops (accelerating dose-infectivity relationships and positive dose-excretion relationships). Further, positive dose-mortality relationships resulted in hosts that traditionally decrease disease (e.g., low competence, strong competitors) increasing infection prevalence, and vice versa. Finally, we found that dose relationships can create positive feedback loops that facilitate friendly competition (i.e., increased heterospecific density has a positive effect on focal host density because the reduction in disease outweighs the negative effects of interspecific competition). This suggests that without taking dose relationships into account, we may incorrectly predict the effect of heterospecific host interactions, and thus host community composition, on environmentally transmitted parasites.

Using sensitivity analysis to identify factors promoting higher versus lower infection prevalence in multi-host communities

Relationships between host species richness and levels of disease in a focal host are likely to be context-dependent, depending on the characteristics of which particular host species are present in a community. I use a multi-host epidemiological model with environmental transmission to explore how the characteristics of the host species (e.g., competence and competitive ability), host density, and the pathogen transmission mechanism affect the proportion of infected individuals (i.e., infection prevalence) in a focal host. My sensitivity-based approach identifies the indirect pathways through which specific ecological and epidemiological processes affect focal host infection prevalence. This in turn yields predictions about the context-dependent rules governing whether increased host species richness increases (amplifies) or decreases (dilutes) infection prevalence in a focal host. For example, in many cases, amplification and dilution are predicted to occur when added host species are sources or sinks of infectious propagules, respectively. However, if the added host species have strong and asymmetric competitive effects on resident host species, then amplification and dilution are predicted to occur when the added host species have stronger competitive effects on resident host species that are sources or sinks of infectious propagules, respectively. My results also predict that greater dilution and less amplification is more likely to occur under frequency-dependent direct transmission than density-dependent direct transmission when (i) the added hosts have lower competence than resident host species and (ii) interspecific competition between the added host species and resident host species is lower; the opposite conditions promote greater amplification and less dilution under frequency-dependent direct transmission. This work helps identify and explain the mechanisms shaping the context-dependent relationships between host species richness and disease in multi-host communities.

Host phylogeny matters: Examining sources of variation in infection risk by blood parasites across a tropical montane bird community in India

BackgroundIdentifying patterns and drivers of infection risk among host communities is crucial to elucidate disease dynamics and predict infectious disease risk in wildlife populations. Blood parasites of the genera Plasmodium and Haemoproteus are a diverse group of vector-borne protozoan parasites that affect bird populations globally. Despite their widespread distribution and exceptional diversity, factors underlying haemosporidian infection risk in wild bird communities remain poorly understood. While some studies have examined variation in avian haemosporidian risk, researchers have primarily focused on host ecological traits without considering host phylogenetic relationships. In this study, we employ a phylogenetically informed approach to examine the association between host ecological traits and haemosporidian infection risk in endemic bird communities in the Western Ghats Sky Islands.MethodsWe used parasite sequence data based on partial mitochondrial cytochrome b gene, that was amplified from genomic DNA extracted from 1177 birds (28 species) across the Western Ghats to assess infection of birds with haemosporidian parasites. We employed a Bayesian phylogenetic mixed effect modelling approach to test whether haemosporidian infection risk was affected by seven species-specific and four individual-level ecological predictors. We also examined the effect of host phylogenetic relationships on the observed patterns of variation in haemosporidian infection risk by estimating phylogenetic signal.ResultsOur study shows that host ecological traits and host phylogeny differentially influence infection risk by Plasmodium (generalist parasite) and Haemoproteus (specialist parasite). For Plasmodium, we found that sociality, sexual dimorphism and foraging strata were important ecological predictors. For Haemoproteus, patterns of infection risk among host species were associated with sociality, species elevation and individual body condition. Interestingly, variance in infection risk explained by host phylogeny was higher for Haemoproteus parasites compared to Plasmodium.ConclusionsOur study highlights that while host ecological traits promoting parasite exposure and host susceptibility are important determinants of infection risk, host phylogeny also contributes substantially to predicting patterns of haemosporidian infection risk in multi-host communities. Importantly, infection risk is driven by joint contributions of host ecology and host phylogeny and studying these effects together could increase our ability to better understand the drivers of infection risk and predict future disease threats.Graphical abstract

Mycobacterium bovis Infection in Red Foxes in Four Animal Tuberculosis Endemic Areas in France.

In France, animal tuberculosis (TB) due to Mycobacterium bovis (M. bovis) affects a multi-host community that include cattle and wildlife species such as wild boars (Sus scrofa), badgers (Meles meles), or wild deer (Cervus elaphus, Capreolus capreolus). The involvement of foxes in the epidemiology of TB is fairly described in countries facing multispecies concerns. After the discovery of grouped cases of TB in foxes in a French TB endemic region, a study was implemented in the core of four TB endemic areas in Dordogne, Charente, Landes (departments of Nouvelle-Aquitaine region), and Côte-d’Or (Burgundy-Franche-Comté region). No infected fox was found in Côte-d’Or (n = 146), where in parallel TB in cattle and other wild species became sparse in the last years. In contrast, in Dordogne, Charente, and Landes, 13 (n = 184), 9 (n = 98) and 7 (n = 140) foxes were found infected by M. bovis, respectively, corresponding to 7.1% (CI95% 3.8–11.8%), 9.2% (4.3–16.7%) and 5.0% (CI95% 2.0–10.0%) prevalence rates, respectively. These infection rates are comparable with those observed in badgers and wild boar in these same three areas (ranging from 9 to 13.2% and 4.3 to 17.9%, respectively), where the number of cattle outbreaks has increased in the last 10-15 years. In each area, the genotypes of foxes’ M. bovis isolates were the same as those in local cattle and other wildlife species. None of the infected foxes presented TB-like gross lesions. M. bovis was found in the mesenteric lymph nodes of 28 foxes (68%). For the 12 foxes where retropharyngeal and respiratory lymph nodes were analyzed separately, M. bovis was present in the respiratory lymph nodes of eight individuals. With regard to excretion, appropriate samples were available for 12 infected foxes from Dordogne. M. bovis DNA was detected in the feces of five of these animals, four of which were infected in the mesenteric lymph nodes. Combined with the knowledge on the biology and ecology of foxes, the results of this study suggest that in areas where infection in cattle is still active in France, foxes might play a role of spillover host in the epidemiology of M. bovis.

Quantification of the Animal Tuberculosis Multi-Host Community Offers Insights for Control.

Animal tuberculosis (TB) is a multi-host zoonotic disease whose prevalence in cattle herds in Europe has been increasing, despite a huge investment in eradication. The composition of the host community is a fundamental driver of pathogen transmission, and yet this has not been formally quantified for animal TB in Europe. We quantified multi-host communities of animal TB, using stochastic models to estimate the number of infected domestic and wild hosts in three regions: officially TB-free Central–Western Europe, and two largely TB-endemic regions, the Iberian Peninsula and Britain and Ireland. We show that the estimated number of infected animals in the three regions was 290,059–1,605,612 and the numbers of infected non-bovine domestic and wild hosts always exceeded those of infected cattle, with ratios ranging from 3.3 (1.3–19.6):1 in Britain and Ireland to 84.3 (20.5–864):1 in the Iberian Peninsula. Our results illustrate for the first time the extent to which animal TB systems in some regions of Europe are dominated by non-bovine domestic and wild species. These findings highlight the need to adapt current strategies for effective future control of the disease.

Infectious hematopoietic necrosis virus specialization in a multihost salmonid system.

Many pathogens interact and evolve in communities where more than one host species is present, yet our understanding of host–pathogen specialization is mostly informed by laboratory studies with single species. Managing diseases in the wild, however, requires understanding how host–pathogen specialization affects hosts in diverse communities. Juvenile salmonid mortality in hatcheries caused by infectious hematopoietic necrosis virus (IHNV) has important implications for salmonid conservation programs. Here, we evaluate evidence for IHNV specialization on three salmonid hosts and assess how this influences intra‐ and interspecific transmission in hatchery‐reared salmonids. We expect that while more generalist viral lineages should pose an equal risk of infection across host types, viral specialization will increase intraspecific transmission. We used Bayesian models and data from 24 hatcheries in the Columbia River Basin to reconstruct the exposure history of hatcheries with two IHNV lineages, MD and UC, allowing us to estimate the probability of juvenile infection with these lineages in three salmonid host types. Our results show that lineage MD is specialized on steelhead trout and perhaps rainbow trout (both Oncorhynchus mykiss), whereas lineage UC displayed a generalist phenotype across steelhead trout, rainbow trout, and Chinook salmon. Furthermore, our results suggest the presence of specialist–generalist trade‐offs because, while lineage UC had moderate probabilities of infection across host types, lineage MD had a small probability of infection in its nonadapted host type, Chinook salmon. Thus, in addition to quantifying probabilities of infection of socially and economically important salmonid hosts with different IHNV lineages, our results provide insights into the trade‐offs that viral lineages incur in multihost communities. Our results suggest that knowledge of the specialist/generalist strategies of circulating viral lineages could be useful in salmonid conservation programs to control disease.

How intraguild predation affects the host diversity-disease relationship in a multihost community

Broad evidence has shown that host diversity can impede disease invasion and reduce the eventual prevalence, but little is known on how species interactions play in shaping this host diversity-disease relationship. Previous work has illustrated that intraguild predation (IGP), combined with parasite-mediated indirect effects, can have strong influences on parasitic infection. Following this line of thinking, we here examine the role of predatory interactions in the disease transmission within a multihost community. Through varying fractions of IGP in a competitive community, we show that, dependent on the fraction of predatory interactions, species richness can switch from enhancing to inhibiting disease establishment/prevalence. Without IGP interactions, high host species richness can likely weaken the ‘dilution effect’ and in some cases even enhance the disease establishment (and/or prevalence) due to the existence of alternative sources for infection, whereas IGP can generally heighten the negative diversity-disease relationship due to the reduction of encounter rate between prospective hosts and parasites. Although trait-mediated interactions (captured as the infection-induced changes in predation rate) only weakly affect disease prevalence, density-mediated interactions (captured as the additional infection-induced mortality) can pose a relatively strong influence on disease transmission. Our results thus underline the importance of considering species interactions when investigating the host diversity-disease relationship.

Trypanosoma cruzi transmission dynamics in a synanthropic and domesticated host community.

Trypanosoma cruzi is the causative agent of Chagas disease, a Neglected Tropical Disease affecting 8 million people in the Americas. Triatomine hematophagous vectors feed on a high diversity of vertebrate species that can be reservoirs or dead-end hosts, such as avian species refractory to T. cruzi. To understand its transmission dynamics in synanthropic and domesticated species living within villages is essential to quantify disease risk and assess the potential of zooprophylaxis. We developed a SI model of T. cruzi transmission in a multi-host community where vector reproduction and parasite transmission depend on a triatomine blood-feeding rate accounting for vector host preferences and interference while feeding. The model was parameterized to describe T. cruzi transmission in villages of the Yucatan peninsula, Mexico, using the information about Triatoma dimidiata vectors and host populations accumulated over the past 15 years. Extensive analyses of the model showed that dogs are key reservoirs and contributors to human infection, as compared to synanthropic rodents and cats, while chickens or other domesticated avian hosts dilute T. cruzi transmission despite increasing vector abundance. In this context, reducing the number of dogs or increasing avian hosts abundance decreases incidence in humans by up to 56% and 39%, respectively, while combining such changes reduces incidence by 71%. Although such effects are only reached over >10-years periods, they represent important considerations to be included in the design of cost-effective Integrated Vector Management. The concomitant reduction in T. cruzi vector prevalence estimated by simulating these zooprophylactic interventions could indeed complement the removal of colonies from the peridomiciles or the use of insect screens that lower vector indoor abundance by ~60% and ~80%. These new findings reinforce the idea that education and community empowerment to reduce basic risk factors is a cornerstone to reach and sustain the key objective of interrupting Chagas disease intra-domiciliary transmission.

Parasite richness and network architecture jointly affect multihost community composition

Broad evidence has shown that network structure can play an important role in food-web persistence, but little is known on how the structure of parasitic links affects the multihost community. Following a previous model of parasitic infection in host food-web, we have explored the effects of parasite richness and architecture of parasitic links on species persistence and topological properties within the merged network including predatory and parasitic sub-webs. Results have shown that the effect of parasitic links on community structure depends on both the level of parasite richness and network architecture. Particularly for architecture network generated by inverse niche model, the standard deviation of vulnerability with low connectance of parasitic links amazingly reaches a hollow at moderate parasite richness, but high for the extreme richness (weak or strong). Although network architecture can strongly affect topological properties of multihost community, it can only weakly influence the ability of species to coexist. The results emphasize that addition of parasites in the ecosystem could be an important process for species diversity and topological structure of ecological network.

Using contact networks and next-generation sequencing for wildlife epidemiology

Horizontal transmission of infectious diseases is strongly determined by the contact network between hosts [1] . Environmental and ecological variables that define the probability of contacts between individuals, such as food resource quality and quantity, have been largely neglected in models studying the dynamics and epidemiology of wildlife diseases. In this work, we used pollinators and their pathogens to study the role of contact networks in a natural multi-host pathogen community. In agricultural landscapes, wild flowers are the most important food resources of insect pollinators such as bees and flies. To boost yields of agricultural crops and ensure pollinator conservation, the UK Environmental Stewardship scheme prompted farmers to grow pollinator-friendly wild flower margins along their fields ( Fig. 1 ). Wild flower margins ( Fig. 1 ) have proven to be efficient to increase both density and diversity of bees in agricultural areas, and to increase pollination success of surrounding crops. As the rate of disease transmission should increase with host density, we hypothesize that the success of wild flower margins may generate hubs for pathogen exchange within the bee community. Several recent studies have illustrated the frequent transmission of infectious diseases between managed and wild bees, potentially via the shared use of flowers [2] . However, the environmental and ecological drivers of disease dynamics between pollinators remain uncharacterised [3] . To understand the role of flower density and diversity for bee disease transmission, we reconstructed high-resolution plant–insect visitor networks from flower visitation data collected in ten farms in Southern England (five farms participating in the scheme vs. five control farms), as well as a record of bee pollen collection to describe the resource bees were exploiting (pollen vs. nectar). When analysing the plant–pollinator networks, we found that flower density and diversity strongly define pollinator density and foraging behaviour, and influence the structure of indirect ‘contact networks’ among pollinators (via the use of flower species). Particularly, we found flower diversity to be positively correlated with the reduction of niche overlap between insect species. This response of insect pollinators suggest that wild flower margins with high plant species richness may reduce insect competition for resources, and potentially reduce the risk of inter-specific disease transmission by supporting diverse diet for insects exploiting different flowers. To test the effect of plant diversity on pathogen dynamics in bees, we sampled pollinators on these farms and characterized their virome by deep transcriptome sequencing. We are now combining these environmental data to virus discovery in order to reveal the impact of the agri-environmental scheme on viral dynamics. Ultimately, we aim to identify environmental (flower density, agricultural practices) and ecological factors (plant taxa, insect community assemblage) that significantly enhance the transmission of plant and pollinator viral diseases within our model to eventually improve agricultural practises and wildlife management.

Host traits and competitive ability jointly structure disease dynamics and community assembly

Parasitism and competition are both ubiquitous interactions in ecological communities. The ability of host species to interact directly via competition and indirectly through shared parasites suggests that host traits related to competition and parasitism are likely important in structuring communities and disease dynamics. Specifically, those host traits affecting competition and those mediating parasitism are often correlated either because of trade-offs (in resource acquisition or resource allocation) or condition dependence, yet the consequences of these trait relationships for community and epidemiological dynamics are poorly understood. We conducted a literature review of parasite-related host traits-competitive ability relationships. We found that transmission-competitive ability relationships were most often reported, and that superior competitors exhibited elevated transmission relative to their less-competitive counterparts in nearly 80% of the cases. We also found a significant number of virulence-competitive ability and parasite shedding-competitive ability relationships. We investigated these links by altering the relationship between host competitive ability and three parasite-related traits (transmission, virulence and parasite shedding rates) in a simple model, incorporating competitive asymmetries in a multi-host community. We show that these relationships can lead to a range of different communities. For example, depending on the strength and direction of these distinct trait relationships, we observed communities with anywhere from high parasite prevalence to complete parasite extinction, and either one, two or the maximum of three host species coexisting. Our results suggest that parasite-competitive ability relationships may be common in nature, that further integration of these relationships can produce novel and unexpected community and disease dynamics, and that generalizations may allow for the prediction of how parasitism and competition jointly structure disease and diversity in natural communities.

Chance or choice? Understanding parasite selection and infection in multi-host communities

Ongoing debate over the relationship between biodiversity and disease risk underscores the need to develop a more mechanistic understanding of how changes in host community composition influence parasite transmission, particularly in complex communities with multiple hosts. A key challenge involves determining how motile parasites select among potential hosts and the degree to which this process shifts with community composition. Focusing on interactions between larval amphibians and the pathogenic trematode Ribeiroia ondatrae, we designed a novel, large-volume set of choice chambers to assess how the selectivity of free-swimming infectious parasites varied among five host species and in response to changes in assemblage composition (four different permutations). In a second set of trials, cercariae were allowed to contact and infect hosts, allowing comparison of host-parasite encounter rates (parasite choice) with infection outcomes (successful infections). Cercariae exhibited consistent preferences for specific host species that were independent of the community context; large-bodied amphibians, such as larval bullfrogs (Rana catesbeiana), exhibited the highest level of parasite attraction. However, because host attractiveness was decoupled from susceptibility to infection, assemblage composition sharply affected both per-host infection as well as total infection (summed among co-occurring hosts). Species such as the non-native R. catesbeiana functioned as epidemiological ‘sinks’ or dilution hosts, attracting a disproportionate fraction of parasites relative to the number that established successfully, whereas Taricha granulosa and especially Pseudacris regilla supported comparatively more metacercariae relative to cercariae selection. These findings provide a framework for integrating information on parasite preference in combination with more traditional factors such as host competence and density to forecast how changes within complex communities will affect parasite transmission.

A possible reservoir of Batrachochytrium dendrobatidis in Australia

A possible reservoir of <i>Batrachochytrium dendrobatidis</i> in Australia

Exploring vector-borne infection ecology in multi-host communities: A case study of West Nile virus

In this study, we develop a model to investigate how ecological factors might affect the dynamics of a vector-borne pathogen in a population composed by different hosts which interact with each other. Specifically, we consider the case when different host species compete with each other, as they share the same habitat, and the vector might have different feeding preference, which can also be time dependent. As a prototypical example, we apply our model to study the invasion and spread, during a typical season, of West Nile virus in an ecosystem composed of two competent avian host species and possibly of dead-end host species. We found that competition and vector feeding preferences can profoundly influence pathogen invasion, influencing its probability to start an epidemic, and influencing transmission rates. Finally, when considering time-dependent feeding preferences, as observed in the field, we noted that the virus circulation could be amplified and that the timing of epidemic peaks could be changed. Our work highlights that ecological interactions between hosts can have a profound influence on the dynamics of the pathogen and that, when modeling vector-borne infections, vector feeding behavior should, for this reason, be carefully evaluated.

Climate forcing of an emerging pathogenic fungus across a montane multi-host community.

Changes in the timings of seasonality as a result of anthropogenic climate change are predicted to occur over the coming decades. While this is expected to have widespread impacts on the dynamics of infectious disease through environmental forcing, empirical data are lacking. Here, we investigated whether seasonality, specifically the timing of spring ice-thaw, affected susceptibility to infection by the emerging pathogenic fungus Batrachochytrium dendrobatidis (Bd) across a montane community of amphibians that are suffering declines and extirpations as a consequence of this infection. We found a robust temporal association between the timing of the spring thaw and Bd infection in two host species, where we show that an early onset of spring forced high prevalences of infection. A third highly susceptible species (the midwife toad, Alytes obstetricans) maintained a high prevalence of infection independent of time of spring thaw. Our data show that perennially overwintering midwife toad larvae may act as a year-round reservoir of infection with variation in time of spring thaw determining the extent to which infection spills over into sympatric species. We used future temperature projections based on global climate models to demonstrate that the timing of spring thaw in this region will advance markedly by the 2050s, indicating that climate change will further force the severity of infection. Our findings on the effect of annual variability on multi-host infection dynamics show that the community-level impact of fungal infectious disease on biodiversity will need to be re-evaluated in the face of climate change.This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.

Are All Hosts Created Equal? Partitioning Host Species Contributions to Parasite Persistence in Multihost Communities.

Many parasites circulate endemically within communities of multiple host species. To understand disease persistence within these communities, it is essential to know the contribution each host species makes to parasite transmission and maintenance. However, quantifying those contributions is challenging. We present a conceptual framework for classifying multihost sharing, based on key thresholds for parasite persistence. We then develop a generalized technique to quantify each species' contribution to parasite persistence, allowing natural systems to be located within the framework. We illustrate this approach using data on gastrointestinal parasites circulating within rodent communities and show that, although many parasites infect several host species, parasite persistence is often driven by just one host species. In some cases, however, parasites require multiple host species for maintenance. Our approach provides a quantitative method for differentiating these cases using minimal reliance on system-specific parameters, enabling informed decisions about parasite management within poorly understood multihost communities.

A Combination of Species Evenness and Functional Diversity Is the Best Predictor of Disease Risk in Multihost Communities.

Although accumulated evidence has shown that biodiversity can play an important role in disease transmission and prevalence, it remains unclear how different measures of diversity based on taxonomy or function perform in predicting disease risk. In this article, we assess the relative ability of species richness, Shannon's evenness index, single functional traits, and several functional diversity metrics and their interactions to predict disease risk in both nonequilibrium and equilibrium communities simulated by a multihost epidemiological model. On the basis of generalized linear models and Akaike's information criterion, we found that Shannon's evenness index outperforms species richness as a single variable in explaining variation in disease risk, while the best combination consists of Shannon's evenness index and functional diversity. This study is, to our knowledge, the first to demonstrate the important role played by species evenness and functional diversity in accounting for variation in disease risk in multihost communities.

Interspecific Contact and Competition May Affect the Strength and Direction of Disease-Diversity Relationships for Directly Transmitted Microparasites.

The frequency of opportunities for transmission is key to the severity of directly transmitted disease outbreaks in multihost communities. Transmission opportunities for generalist microparasites often arise from competitive and trophic interactions. Additionally, contact heterogeneities within and between species either hinder or promote transmission. General theory incorporating competition and contact heterogeneities for disease-diversity relationships is underdeveloped. Here, we present a formal framework to explore disease-diversity relationships for directly transmitted parasites that infect multiple host species, including influenza viruses, rabies virus, distemper viruses, and hantaviruses. We explicitly include host regulation via intra- and interspecific competition, where the latter can be dependent on or independent of interspecific contact rates (covering resource utilization overlap, habitat selection preferences, and temporal niche partitioning). We examine how these factors interact with frequency- and density-dependent transmission along with traits of the hosts in the assemblage, culminating in the derivation of a relationship describing the propensity for parasite fitness to decrease in species assemblages relative to that in single-host species. This relationship reveals that increases in biodiversity do not necessarily suppress frequency-dependent parasite transmission and that regulation of hosts via interspecific competition does not always lead to a reduction in parasite fitness. Our approach explicitly shows that species identity and ecological interactions between hosts together determine microparasite transmission outcomes in multispecies communities.

Host species composition influences infection severity among amphibians in the absence of spillover transmission

Wildlife epidemiological outcomes can depend strongly on the composition of an ecological community, particularly when multiple host species are affected by the same pathogen. However, the relationship between host species richness and disease risk can vary with community context and with the degree of spillover transmission that occurs among co-occurring host species. We examined the degree to which host species composition influences infection by Batrachochytrium dendrobatidis (Bd), a widespread fungal pathogen associated with amphibian population declines around the world, and whether transmission occurs from one highly susceptible host species to other co-occurring host species. By manipulating larval assemblages of three sympatric amphibian species in the laboratory, we characterized the relationship between host species richness and infection severity, whether infection mediates growth and survivorship differently across various combinations of host species, and whether Bd is transmitted from experimentally inoculated tadpoles to uninfected tadpoles. We found evidence of a dilution effect where Bd infection severity was dramatically reduced in the most susceptible of the three host species (Anaxyrus boreas). Infection also mediated survival and growth of all three host species such that the presence of multiple host species had both positive (e.g., infection reduction) and negative (e.g., mortality) effects on focal species. However, we found no evidence that Bd infection is transmitted by this species. While these results demonstrate that host species richness as well as species identity underpin infection dynamics in this system, dilution is not the product of reduced transmission via fewer infectious individuals of a susceptible host species. We discuss various mechanisms, including encounter reduction and antagonistic interactions such as competition and opportunistic cannibalism that may act in concert to mediate patterns of infection severity, growth, and mortality observed in multihost communities.

Co-infection and cross-species transmission of divergent Hepatocystis lineages in a wild African primate community

Hemoparasites of the apicomplexan family Plasmodiidae include the etiological agents of malaria, as well as a suite of non-human primate parasites from which the human malaria agents evolved. Despite the significance of these parasites for global health, little information is available about their ecology in multi-host communities. Primates were investigated in Kibale National Park, Uganda, where ecological relationships among host species are well characterized. Blood samples were examined for parasites of the genera Plasmodium and Hepatocystis using microscopy and PCR targeting the parasite mitochondrial cytochrome b gene, followed by Sanger sequencing. To assess co-infection, “deep sequencing” of a variable region within cytochrome b was performed. Out of nine black-and-white colobus (Colobus guereza), one blue guenon (Cercopithecus mitis), five grey-cheeked mangabeys (Lophocebus albigena), 23 olive baboons (Papio anubis), 52 red colobus (Procolobus rufomitratus) and 12 red-tailed guenons (Cercopithecus ascanius), 79 infections (77.5%) were found, all of which were Hepatocystis spp. Sanger sequencing revealed 25 different parasite haplotypes that sorted phylogenetically into six species-specific but morphologically similar lineages. “Deep sequencing” revealed mixed-lineage co-infections in baboons and red colobus (41.7% and 64.7% of individuals, respectively) but not in other host species. One lineage infecting red colobus also infected baboons, but always as the minor variant, suggesting directional cross-species transmission. Hepatocystis parasites in this primate community are a diverse assemblage of cryptic lineages, some of which co-infect hosts and at least one of which can cross primate species barriers.