A power-efficiency trade-off in resource use alters epidemiological relationships

Trade-offs play pivotal roles in the ecology and evolution of natural populations. However, trade-offs are probably not static, invariant relationships. Instead, ecological factors can shift, alter, or reverse the relationships underlying trade-offs and create critical genotype x environment (G x E) interactions. But which ecological factors alter trade-offs or create G x E interactions, and why (mechanistically) do they do this? We tackle these questions using resource quality as the central ecological factor and a case study of disease in the plankton. We show that clonal genotypes of a zooplankton host (Daphnia dentifera) exhibit a "power-efficiency" trade-off in resource use, where powerful (fast-feeding) host clones perform well on richer algal resources, but more efficient (slow-feeding) clones perform relatively well on poorer resources. This resource-based trade-off then influences epidemiological relationships due to fundamental connections between resources and fecundity, transmission rate (an index of resistance), and replication of a virulent fungal parasite (Metschnikowia bicuspidata) within hosts. For instance, using experiments and dynamic energy budget models, we show that the power-efficiency trade-off overturned a previously detected trade-off between fecundity and transmission risk of hosts to this parasite. When poorer resources were eaten, transmission risk and fecundity were negatively, not positively, correlated. Additionally, poor resource quality changed positive relationships between yield of infectious stages (spores) and host fecundity: those fecundity-spore relationships with poor food became negative or nonsignificant. Finally, the power-efficiency trade-off set up an interaction between host clone and resource quality for yield of fungal spores: powerful clones yielded relatively more spores on the better resource, while efficient clones yielded relatively more on the poorer resource. Thus, the physiological ecology of resource use can offer potent, mechanistic insight linking environmental factors to epidemiological relationships.     

Genetic relatedness and eusociality: parasite-mediated selection on the genetic composition of groups

Summary Contrary to the expectations of kin selection theory, intracolony relatedness in eusocial insects is often low. We examined the idea that associations of low relatedness (high genetic variability) may be advantageous because of negative frequency-dependent selection on common host phenotypes by rapidly evolving parasites and pathogens. Using the natural host-parasite system of the bumble bee Bombus terrestris and its intestinal trypanosome Crithidia bombi, we investigated the transmission properties of parasites in host groups. Within naturally infested nests and in artificially constructed groups of workers, prevalence of infestation increased with time of exposure (Table 1). The susceptibility of isolated groups of workers to the parasites to which they were exposed differed with identity and natural infestation of their nest of origin (Table 2). In addition, those workers that were related to the individual introducing an infection to their group were more likely to become infested than were unrelated workers (Table 3). Although the bumble bee workers in experimental boxes appeared to differ in behavior toward kin and non-kin, making more physical contacts with kin, we found no discernible relationship between number of physical contacts and prevalence of infestation in a group. Therefore, we conclude that differences in parasite transmission reflected interactions among different host and parasite phenotypes. This system thus demonstrates the factors necessary for negative frequency-dependent selection by parasites on common host phenotypes - variability for susceptibility and infectiousness in host and parasite populations and similarity for these traits among related individuals. If, as we show here, high genetic relatedness within groups enhances parasite transmission, kin directed altruism may increase the risk of contracting parasites and infectious diseases. Therefore, parasites and pathogens may be an important force moderating the genetic structure of social groups. Offprint requests to: J.A. Shykoff at the present address     

Parasite transmission in a migratory multiple host system

A transmission model was devised for trichostrongyloid nematodes of saiga antelopes and domestic sheep in Kazakhstan. The framework extends previous models by including seasonal migration of saigas, contact with separate populations of sheep, and climate-driven stochasticity in herbage biomass and in the development, survival and migration onto herbage of free-living larvae. The model was parameterised for the contrasting life histories of Marshallagia, Haemonchus and Nematodirus, three important parasites of saigas and sheep in the region, and was successful at predicting broad qualitative patterns of infection dynamics in sheep and saigas. Parasite transmission between saigas and sheep was predicted to be most important for Marshallagia (from sheep to saigas in the south in winter, and onward transmission to sheep in the north in summer) and Haemonchus (from sheep in the north in summer via saigas to sheep further south in autumn). Model predictions for winter transmission of Marshallagia infection in saigas were consistent with field data, which showed that saigas culled before they have grazed the winter range carry lower burdens of this parasite than older animals. The model provides a mechanistic explanation for its predictions, which will assist hypothesis formation, and further the epidemiological basis of efforts to control parasite transmission between wildlife and livestock in both directions. A similar modelling approach could prove useful in other situations where detailed mechanistic models of parasite transmission are inappropriate in the face of parameter uncertainty and spatio-temporal variation in climate and host density. This is likely to include the majority of wildlife-parasite systems.     

Exposing males to female scent increases the cost of controlling <Emphasis Type="Italic">Salmonella</Emphasis> infection in wild house mice

Secondary sexual characters often provide indicators of a male’s resistance to infectious diseases to rivals and potential mates, but it is unclear why. It is often suggested that males honestly signal their health due to energetic and other physiological trade-offs between investing into secondary sexual traits vs resistance to infectious diseases. Our aim was to determine whether such a trade-off exists using wild-derived male house mice (Mus domesticus). We exposed male mice to female scent, a manipulation that induces elevations in testosterone concentration and the expression of a variety of testosterone-mediated secondary sexual traits, and tested whether this sexual stimulation impaired the males’ ability to resolve or cope with an experimental infection (Salmonella enterica). We kept the males on a controlled diet to prevent them from compensating by eating more food. We found that sexually stimulated males were able to control bacterial growth as effectively as sham-stimulated controls; however, to do so, they lost more body mass during infection compared to the controls. In contrast, we found no evidence that sexual stimulation reduced the body mass of uninfected male mice. These results indicate that males’ responses to female odor are not immunosuppressive per se, yet they increase the energetic costs of controlling infection. Our findings support the idea that there is a physiological trade-off between secondary sexual signaling vs resistance to infectious diseases and suggest that studies using only immunocompetence assays might fail to detect such energetic trade-offs. We dedicate this paper to the late Professor Chris Barnard who conducted pioneering research on this topic.     

Local adaptation of immunity against a trematode parasite in marine amphipod populations

Resources allocated to defence against parasites are not available for investment in other functions such as growth or reproduction, resulting in trade-offs between different components of an organism’s fitness. In balancing the cost of infection and the cost of immunity, selection should only favour individuals that allocate more energy to resistance and immune responses in populations regularly exposed to debilitating parasites. Here, we compare the ability of amphipods, Paracalliope novizealandiae, to (1) avoid becoming infected and (2) to respond to infection by encapsulating and melanizing parasites, between two natural populations exposed to different risk of parasitism. One population faces high levels of infection by the debilitating trematode parasite Maritrema novaezealandensis, whereas the other population is not parasitised by this trematode nor by any other parasite. Under controlled experimental conditions, with exposure to a standardized dose of parasites, amphipods from the parasite-free population acquired significantly more parasites than those from the population regularly experiencing infection. Furthermore, a lower frequency of amphipods from the parasite-free population succeeded at melanizing (and thus killing) parasites, and they melanized a lower percentage of parasites on average, than amphipods from the parasitised population. These differences persist when individual factors, such as amphipod sex or body length, are taken into account as potential confounding variables. These results support the existence of local adaptation against parasites: an amphipod population that never experiences trematode infections is less capable of resisting infection, both in terms of its first line of defence (avoiding infection) and a later line of defence (fighting parasites following infection), than a population regularly exposed to infection.     

Parasite transmission in complex communities: predators and alternative hosts alter pathogenic infections in amphibians

While often studied in isolation, host-parasite interactions are typically embedded within complex communities. Other community members, including predators and alternative hosts, can therefore alter parasite transmission (e.g., the dilution effect), yet few studies have experimentally evaluated more than one such mechanism. Here, we used data from natural wetlands to design experiments investigating how alternative hosts and predators of parasites mediate trematode (Ribeiroia ondatrae) infection in a focal amphibian host (Pseudacris regilla). In short-term predation bioassays involving mollusks, zooplankton, fish, larval insects, or newts, four of seven tested species removed 62-93% of infectious stages. In transmission experiments, damselfly nymphs (predators) and newt larvae (alternative hosts) reduced infection in P. regilla tadpoles by -50%, whereas mosquitofish (potential predators and alternative hosts) did not significantly influence transmission. Additional bioassays indicated that predators consumed parasites even in the presence of alternative prey. In natural wetlands, newts had similar infection intensities as P. regilla, suggesting that they commonly function as alternative hosts despite their unpalatability to downstream hosts, whereas mosquitofish had substantially lower infection intensities and are unlikely to function as hosts. These results underscore the importance of studying host-parasite interactions in complex communities and of broadly linking research on predation, biodiversity loss, and infectious diseases.     

Parasite competition hidden by correlated coinfection: using surveys and experiments to understand parasite interactions

Within most free-living species exists a cryptic community of interacting parasites. By combining multiscale field data with manipulative experiments, we evaluated patterns of parasite coinfection in amphibian hosts and their underlying mechanisms. Surveys of 86 wetlands and 1273 hosts revealed positive correlations between two pathogenic trematodes (Ribeiroia ondatrae and Echinostoma trivolvis) both between wetlands and within individual hosts. In infection and coinfection experiments, Ribeiroia caused greater pathology than Echinostoma, including high host mortality (24%) and severe limb malformations (75%). No interactive effects were noted for host pathology, but both parasites decreased the per capita persistence of one another by 17-36%. Thus, in spite of consistently positive associations from field data, these parasites negatively affected the persistence of one another, likely via cross immunity (apparent competition). These findings underscore the danger of inferring parasite interactions from coinfection patterns and emphasize the potential disconnect between within-host processes (e.g., competition) and between-host processes (e.g., exposure and transmission). Here, correlated coinfections likely resulted from similarities in the parasites' host requirements and heterogeneity in host susceptibility or exposure. Understanding complex interactions among parasites depends critically on the scale under consideration, highlighting the importance of combining coinfection field studies with mechanistic experiments.     

Infection dynamics of an oyster parasite in its newly expanded range

Over a 2-year period in 1990 and 1991, coincident with a pronounced warming episode, Dermo disease outbreaks in the oyster, Crassostrea virginica, caused by the parasite Perkinsus marinus, occurred over a 500-km range from Delaware Bay to Cape Cod, in the northeastern United States. The parasite had not previously been recorded or known to cause mortalities in this region. To document infection patterns and levels in this region several years after the initial outbreaks, and to compare them with those in the parasite’s historic southern range, we deployed and sampled oysters from 1996 to 1998 at multiple sites spanning the expanded range. During this 2-year period, the parasite was documented to occur in oysters at high prevalences throughout the new range, in sites varying from small, enclosed embayments to large estuaries, and in both cultured and wild-set oysters. Infection and mortality patterns, and levels were similar to those in southern locations where the parasite has been enzootic for at least decades. The persistence of high P. marinus infection levels in the new range after the initial expansion is probably due to several factors: (1) winter temperatures continued to increase during the 1990s and early 2000s, albeit at a slower rate than in 1990–1991, facilitating overwinter survival of the parasite; (2) many oyster-growing sites in the northeast are in relatively shallow water in which summer temperatures offer ample time for the parasite to proliferate and spread; and (3) the combination of high parasite burdens and high host densities in oyster farms results in an abundance of parasites and high transmission rates. Colder winters and high rainfall after 2002 reduced prevalences in some regions, but P. marinus can survive low temperatures and low salinities, and epizootic conditions are likely to return if temperatures rise again, as predicted by climate-change models.     

Female choice for parasite-free male satin bowerbirds and the evolution of bright male plumage

Summary Hamilton and Zuk proposed that bright male plumage may have evolved in males of polygynous species as a result of female preferences for males that are able to demonstrate their resistance to disease. They predicted an inverse correlation between female mating preferences and the level of parasitic infection of males. We found such a correlation between the level of infection by a common ectoparasite (Myrsidea ptilonorhynchi: Menoponidae) and mating success of male satin bowerbirds (Ptilonorhynchus violaceus). In addition, we tested and were able to confirm three other predictions derived from their model: that (1) older males had fewer parasites than their younger counterparts, (2) levels of individual parasitic infection are highly correlated between years, and (3) that individuals resighted in successive years are less parasitized than those that fail to return. These results support the bright male model, but they are also consistent with two other hypotheses that may explain plumage dimorphism based on the level of parasitic infection. The correlated infection model suggests that females choose males with few ectoparasites because of a correlation between the level of ectoparasitic infection and heritable resistance to internal infections. In the parasite avoidance model, females favor parasitefree males because it lowers their own prospects for parasitic infection. Our data did not show the predicted relationship between parasite numbers with plumage quality that is needed to support the bright male hypothesis, nor did it show the inverse correlation between male condition and parasite numbers that is predicted by both the bright male and correlated infection hypotheses. Our results are most consistent with the parasite avoidance hypothesis.     

The effects of parasites on male ornaments and female choice in the lek-breeding black grouse (Tetrao tetrix)

Summary We describe the results of two studies of parasitic infection in the black grouse (Tetrao tetrix). The first deals with our own observations of lekking black grouse in which the parasite levels of two blood parasites, the protozoan Leucocytozoon lovati and microfilaria, probably produced by a nematode worm Splendidofilaria tuvensis, were scored. We also obtained measures of age, survival, number of copulations, body mass and length of the ornamental tail feathers (the lyre) of the lekking males. The second study analysed the data from Lund (1954) which involved eight gut parasites obtained from birds which were killed. In the first study we found higher levels of infection of Leucocytozoon in adults relative to young birds. Parasites had no effect on male survival and there was no correlation in infection between the two types of parasites. Birds infected with microfilaria had shorter tail ornaments. There was no relationship between parasitic infection and mating success. However, the data indicated that such a trend indeed may exist for Leucocytozoon and the most successful males on the leks were less often infected by Leucocytozoon than other males. Results of the second study showed a negative relationship between parasite load (a combined measure of all parasites) and both ornamental tail feather length and body mass. These observations are compatible with, but not conclusive evidence for, the hypothesis of Hamilton and Zuk (1982) on the evolution of secondary sexual characters, where females choose to mate with genetically resistant males which show their resistance by expressing larger and more showy secondary sexual characters. Alternative explanations for the observed patterns are: females avoid infected males for some immediate benefit; and/or parasite loads are indicators of general stress rather than genetical resistance. Under the latter hypothesis females could mate with more vigorous males for reasons unrelated to parasite resistance.     

Personality and parasites: sex-dependent associations between avian malaria infection and multiple behavioural traits

The evolution and ecology of consistent behavioural variation, or personality, is currently the focus of much attention in natural populations. Associations between personality traits and parasite infections are increasingly being reported, but the extent to which multiple behavioural traits might be associated with parasitism at the same time is largely unknown. Here, we use a population of great tits, Parus major, to examine whether infection by avian malaria (Plasmodium and Leucocytozoon) is associated with three behavioural traits assayed under standardized conditions. All of these traits are of broad ecological significance and two of them are repeatable or heritable in our population. Here, we show weak correlations between some but not all of these behavioural traits, and sex-dependent associations between all three behavioural traits and parasite infection. Infected males showed increased problem-solving performance whereas infected females showed reduced performance; furthermore, uninfected females were four times more likely to solve problems than uninfected males. Infected females were more exploratory than uninfected females, but infection had no effect on males. Finally, infected males were more risk-averse than uninfected males but females were unaffected. Our results demonstrate the potential for complex interactions between consistent personality variation and parasite infection, though we discuss the difficulty of attributing causality in these associations. Accounting for complex parasite-behaviour associations may prove essential in understanding the evolutionary ecology of behavioural variation and the dynamics of host–parasite interactions.     

Effect of acanthocephalan parasites on the behaviour and coloration of the mud crab Macrophthalmus hirtipes (Brachyura: Ocypodidae)

In the field, the numbers of cystacanths of the parasitic acanthocephalan Profilicollis spp. harboured by crabs are relatively high and correlate with carapace width. In a field experiment, the responses of crabs to the simulated approach of a bird predator (the parasite's definitive host) was not influenced by the number of acanthocephalans they harboured. Crabs that were exposed at the surface of the sediments during receding high tide, however, tended to harbour more parasites than nearby crabs hidden in burrows. An analysis of colour patterns on the carapace of crabs showed that infection levels did not influence carapace pigmentation, and thus did not affect the conspicuousness of a crab relative to the background environment. However, the likelihood of a male crab winning a ritualized fight against a conspecific in the field was associated with its infection level, but in a way that suggests that this finding is a consequence of pathology rather than an adaptation of the parasite to increase its transmission rate. Although only weak evidence was found indicating that Profilicollis manipulates the behaviour or colour of its host to its own benefit, the high infection levels observed suggest that the crab population acts as a major reservoir for larval stages of this parasite that are infective to birds.     

Network structure and prevalence of Cryptosporidium in Belding’s ground squirrels

Although pathogen transmission dynamics are profoundly affected by population social and spatial structure, few studies have empirically demonstrated the population-level implications of such structure in wildlife. In particular, epidemiological models predict that the extent to which contact patterns are clustered decreases a pathogen’s ability to spread throughout an entire population, but this effect has yet to be demonstrated in a natural population. Here, we use network analysis to examine patterns of transmission of an environmentally transmitted parasite, Cryptosporidium spp., in Belding’s ground squirrels (Spermophilus beldingi). We found that the prevalence of Cryptosporidium was negatively correlated with transitivity, a measure of network clustering, and positively correlated with the percentage of juvenile males. Additionally, network transitivity decreased when there were higher percentages of juvenile males; the exploratory behavior demonstrated by juvenile males may have altered the structure of the network by reducing clustering, and low clustering was associated with high prevalence. We suggest that juvenile males are critical in mediating the ability of Cryptosporidium to spread through colonies, and thus may function as “super-spreaders.” Our results demonstrate the utility of a network approach in quantifying mechanistically how differences in contact patterns may lead to system-level differences in infection patterns.     

Relationship between Coefficient of Inbreeding and Parasite Burden in Endangered Gazelles

Abstract: We studied the effects of inbreeding depression on parasite infection in three species of endangered gazelles: Gazella cuvieri , G. dama, and G. dorcas . Coefficients of inbreeding were calculated for all individuals because complete genealogies were available. The levels of inbreeding differ both intra- and interspecifically. We collected samples of feces and determined nematode infection by counting nematode eggs in the samples. At the interspecific level, the species with the highest mean levels of inbreeding (  G. cuvieri ) had the highest levels of gastrointestinal parasites. Analyses done at the intraspecific level revealed a positive relationship between individual coefficient of inbreeding and parasite infection in G. cuvieri , but not in the species with the intermediate and lowest levels of inbreeding. Our findings suggest that high levels of inbreeding may make individuals more susceptible to parasitism, even under favorable environmental conditions, so this factor should be taken into account by those managing endangered species.     

Seasonality and the evolutionary divergence of plant parasites

The coexistence of closely related plant parasites is widespread. Yet, understanding the ecological determinants of evolutionary divergence in plant parasites remains an issue. Niche differentiation through resource specialization has been widely researched, but it hardly explains the coexistence of parasites exploiting the same host plant. Time-partitioning has so far received less attention, although in temperate climates, parasites may specialize on either the early or the late season. Accordingly, we investigated whether seasonality can also promote phenotypic divergence. For plant parasites, seasonality generally engenders periodic host absence. To account for abrupt seasonal events, we made use of an epidemic model that combines continuous and discrete dynamics. Based on the assumption of a trade-off between in-season transmission and inter-season survival, we found through an "evolutionary invasion analysis" that evolutionary divergence of the parasite phenotype can occur. Since such a trade-off has been reported, this study provides further ecological bases for the coexistence of closely related plant parasites. Moreover, this study provides original insights into the coexistence of sibling plant pathogens which perform either a single or several infection cycles within a season (mono- and polycyclic diseases, or uni- and multivoltine life cycles).     

Dissecting the drivers of population cycles: Interactions between parasites and mountain hare demography

There is a growing awareness that cyclic population dynamics in vertebrate species are driven by a complex set of interactions rather than a single causal factor. While theory suggests that direct host-parasite interactions may destabilise population dynamics, the interaction between host and parasite may also influence population dynamics through indirect effects that result in delayed responses to either density or to life-history traits. Using empirical data on mountain hares (Lepus timidus) infected with a nematode parasite (Trichostrongylus retortaeformis), we developed an individual-based model (IBM) that incorporated direct effects and delayed life-history effects (DLHEs) of a macroparasite, alternative transmission mechanisms and seasonality in host population dynamics. The full model describes mean characteristics of observed mountain hare time series and parasite abundance, but by systematically removing model structure we dissect out dynamic influences of DLHEs. The DLHEs were weakly destabilising, increasing the propensity for cyclic dynamics and suggesting DLHEs could be important processes in host-parasite systems. Further, by modifying model structure we identify a strong influence of parasite transmission mechanism on host population stability, and discuss the implications for parasite aggregation mechanisms, host movement and natural geographical variation in host population dynamics. The effect of T. retortaeformis on mountain hares likely forms part of a complex set of interactions that lead to population cycles.     

Species diversity reduces parasite infection through cross-generational effects on host abundance

With growing interest in the effects of biodiversity on disease, there is a critical need for studies that empirically identify the mechanisms underlying the diversity-disease relationship. Here, we combined wetland surveys of host community structure with mechanistic experiments involving a multi-host parasite to evaluate competing explanations for the dilution effect. Sampling of 320 wetlands in California indicated that snail host communities were strongly nested, with competent hosts for the trematode Ribeiroia ondatrae predominating in low-richness assemblages and unsuitable hosts increasingly present in more diverse communities. Moreover, competent host density was negatively associated with increases in snail species richness. These patterns in host community assembly support a key prerequisite underlying the dilution effect. Results of multigenerational mesocosm experiments designed to mimic field-observed community assemblages allowed us to evaluate the relative importance of host density and diversity in influencing parasite infection success. Increases in snail species richness (from one to four species) had sharply negative effects on the density of infected hosts (-90% reduction). However, this effect was indirect; competition associated with non-host species led to a 95% reduction in host density (susceptible host regulation), owing primarily to a reduction in host reproduction. Among susceptible hosts, there were no differences in infection prevalence as a function of community structure, indicating a lack of support for a direct effect of diversity on infection (encounter reduction). In monospecific conditions, higher initial host densities increased infection among adult hosts; however, compensatory reproduction in the low-density treatments equalized the final number of infected hosts by the next generation, underscoring the relevance of multigenerational studies in understanding the dilution effect. These findings highlight the role of interspecific competition in mediating the relationship between species richness and parasite infection and emphasize the importance of field-informed experimental research in understanding mechanisms underlying the diversity-disease relationship.     

Effects of Invasive Parasites on Bumble Bee Declines

Abstract: Bumble bees are a group of pollinators that are both ecologically and economically important and declining worldwide. Numerous mechanisms could be behind this decline, and the spread of parasites from commercial colonies into wild populations has been implicated recently in North America. Commercial breeding may lead to declines because commercial colonies may have high parasite loads, which can lead to colonization of native bumble bee populations; commercial rearing may allow higher parasite virulence to evolve; and global movement of commercial colonies may disrupt spatial patterns in local adaptation between hosts and parasites. We assessed parasite virulence, transmission mode, and infectivity. Microparasites and so‐called honey bee viruses may pose the greatest threat to native bumble bee populations because certain risk factors are present; for example, the probability of horizontal transmission of the trypanosome parasite Crithidia bombi is high. The microsporidian parasite Nosema bombi may play a role in declines of bumble bees in the United States. Preliminary indications that C. bombi and the neogregarine Apicystis bombi may not be native in parts of South America. We suggest that the development of molecular screening protocols, thorough sanitation efforts, and cooperation among nongovernmental organizations, governments, and commercial breeders might immediately mitigate these threats.     

Effects of vulture declines on facultative scavengers and potential implications for mammalian disease transmission

Vultures (Accipitridae and Cathartidae) are the only known obligate scavengers. They feed on rotting carcasses and are the most threatened avian functional group in the world. Possible effects of vulture declines include longer persistence of carcasses and increasing abundance of and contact between facultative scavengers at these carcasses. These changes could increase rates of transmission of infectious diseases, with carcasses serving as hubs of infection. To evaluate these possibilities, we conducted a series of observations and experimental tests of the effects of vulture extirpation on decomposition rates of livestock carcasses and mammalian scavengers in Kenya. We examined whether the absence of vultures changed carcass decomposition time, number of mammalian scavengers visiting carcasses, time spent by mammals at carcasses, and potential for disease transmission at carcasses (measured by changes in intraspecific contact rates). In the absence of vultures, mean carcass decomposition rates nearly tripled. Furthermore, the mean number of mammals at carcasses increased 3-fold (from 1.5 to 4.4 individuals/carcass), and the average time spent by mammals at carcasses increased almost 3-fold (from 55 min to 143 min). There was a nearly 3-fold increase in the mean number of contacts between mammalian scavengers at carcasses without vultures. These results highlight the role of vultures in carcass decomposition and level of contact among mammalian scavengers. In combination, our findings lead us to hypothesize that changes in vulture abundance may affect patterns of disease transmission among mammalian carnivores.     

Adding infection to injury: synergistic effects of predation and parasitism on amphibian malformations

We explored the importance of interactions between parasite infection and predation in driving an emerging phenomenon of conservation importance: amphibian limb malformations. We suggest that injury resulting from intraspecific predation in combination with trematode infection contributes to the frequency and severity of malformations in salamanders. By integrating field surveys and experiments, we evaluated the individual and combined effects of conspecific attack and parasite (Ribeiroia ondatrae) infection on limb development of long-toed salamanders (Ambystoma macrodactylum). In the absence of Ribeiroia, abnormalities involved missing digits, feet, or limbs and were similar to those produced by cannibalistic attack in experimental trials. At field sites that supported Ribeiroia, malformations were dominated by extra limbs and digits. Correspondingly, laboratory exposure of larval salamanders to Ribeiroia cercariae over a 30-day period induced high frequencies of malformations, including extra digits, extra limbs, cutaneous fusion, and micromelia. However, salamander limbs exposed to both injury and infection exhibited 3-5 times more abnormalities than those exposed to either factor alone. Infection also caused significant delays in limb regeneration and time-to-metamorphosis. Taken together, these results help to explain malformation patterns observed in natural salamander populations while emphasizing the importance of interactions between parasitism and predation in driving disease.