Infectious Diseases and Extinction Risk in Wild Mammals

Abstract:  Parasite-driven declines in wildlife have become increasingly common and can pose significant risks to natural populations. We used the IUCN Red List of Threatened and Endangered Species and compiled data on hosts threatened by infectious disease and their parasites to better understand the role of infectious disease in contemporary host extinctions. The majority of mammal species considered threatened by parasites were either carnivores or artiodactyls, two clades that include the majority of domesticated animals. Parasites affecting host threat status were predominantly viruses and bacteria that infect a wide range of host species, including domesticated animals. Counter to our predictions, parasites transmitted by close contact were more likely to cause extinction risk than those transmitted by other routes. Mammal species threatened by parasites were not better studied for infectious diseases than other threatened mammals and did not have more parasites or differ in four key traits demonstrated to affect parasite species richness in other comparative studies. Our findings underscore the need for better information concerning the distribution and impacts of infectious diseases in populations of endangered mammals. In addition, our results suggest that evolutionary similarity to domesticated animals may be a key factor associated with parasite-mediated declines; thus, efforts to limit contact between domesticated hosts and wildlife could reduce extinction risk.     

Using a common commensal bacterium in endangered Takahe as a model to explore pathogen dynamics in isolated wildlife populations

Predicting and preventing outbreaks of infectious disease in endangered wildlife is problematic without an understanding of the biotic and abiotic factors that influence pathogen transmission and the genetic variation of microorganisms within and between these highly modified host communities. We used a common commensal bacterium, Campylobacter spp., in endangered Takahe (Porphyrio hochstetteri) populations to develop a model with which to study pathogen dynamics in isolated wildlife populations connected through ongoing translocations. Takahe are endemic to New Zealand, where their total population is approximately 230 individuals. Takahe were translocated from a single remnant wild population to multiple offshore and mainland reserves. Several fragmented subpopulations are maintained and connected through regular translocations. We tested 118 Takahe from 8 locations for fecal Campylobacter spp. via culture and DNA extraction and used PCR for species assignment. Factors relating to population connectivity and host life history were explored using multivariate analytical methods to determine associations between host variables and bacterial prevalence. The apparent prevalence of Campylobacter spp. in Takahe was 99%, one of the highest reported in avian populations. Variation in prevalence was evident among Campylobacter species identified. C. sp. nova 1 (90%) colonized the majority of Takahe tested. Prevalence of C. jejuni (38%) and C. coli (24%) was different between Takahe subpopulations, and this difference was associated with factors related to population management, captivity, rearing environment, and the presence of agricultural practices in the location in which birds were sampled. Modeling results of Campylobacter spp. in Takahe metapopulations suggest that anthropogenic management of endangered species within altered environments may have unforeseen effects on microbial exposure, carriage, and disease risk. Translocation of wildlife between locations could have unpredictable consequences including the spread of novel microbes between isolated populations.     

Using survival analysis to study translocation success in the Gila topminnow (Poeciliopsis occidentalis).

Translocation, the intentional release of captive-propagated and/or wild-caught animals into the wild in an attempt to establish, reestablish, or augment a population, is a commonly used approach to species conservation. Despite the frequent mention of translocation as an aid in threatened or endangered species recovery plans, translocations have resulted in the establishment of few sustainable populations. To improve the effectiveness of translocation efforts, it is essential to identify and adopt features that contribute to successful translocations. This study analyzed 148 translocations of the endangered Gila topminnow (Poeciliopsis occidentalis) to identify various factors that have significantly influenced translocation success. We quantified success as the "persistence time" of translocated populations and used survival analysis to interpret the role of several factors. The following factors affected persistence times of translocated populations: season in which the fish were translocated, habitat type of the translocation site, and genetic origin of the fish stocked. In general, factors associated with stocking, the population stocked, and the site of translocation can significantly affect the persistence of translocated populations and thus increase the probability of translocation success. For Gila topminnow, future translocations should be undertaken in late summer or fall (not early summer), should occur into ponds (not streams, wells, or tanks), and should generally utilize individuals from genetic lineages other than Monkey Spring. For other species, a key lesson emerging from this work is that life history attributes for each translocated species need to be considered carefully.     

Monarch butterfly migration and parasite transmission in eastern North America

Seasonal migration occurs in many animal systems and is likely to influence interactions between animals and their parasites. Here, we focus on monarch butterflies (Danaus plexippus) and a protozoan parasite (Ophryocystis elektroscirrha) to investigate how host migration affects infectious disease processes. Previous work showed that parasite prevalence was lower among migratory than nonmigratory monarch populations; two explanations for this pattern are that (1) migration allows animals to periodically escape contaminated habitats (i.e., migratory escape), and (2) long-distance migration weeds out infected animals (i.e., migratory culling). We combined field-sampling and analysis of citizen science data to examine spatiotemporal trends of parasite prevalence and evaluate evidence for these two mechanisms. Analysis of within-breeding-season variation in eastern North America showed that parasite prevalence increased from early to late in the breeding season, consistent with the hypothesis of migratory escape. Prevalence was also positively related to monarch breeding activity, as indexed by larval density. Among adult monarchs captured at different points along the east coast fall migratory flyway, parasite prevalence declined as monarchs progressed southward, consistent with the hypothesis of migratory culling. Parasite prevalence was also lower among monarchs sampled at two overwintering sites in Mexico than among monarchs sampled during the summer breeding period. Collectively, these results indicate that seasonal migration can affect parasite transmission in wild animal populations, with implications for predicting disease risks for species with threatened migrations.     

Disease Risks of Wildlife Translocations

Threats posed to conservation programs by the translocation of pathogens along with the translocation of host species are being increasingly recognized. However, publications on this subject have appeared primarily in veterinary literature which often is not read widely by those who fund, plan, or carry out the majority of wildlife translocations. The problem of wildlife disease and translocations has been written about in detail recently, but in almost all cases has been limited to exploring the immediate effects of pathogens on the target species. I discuss the possible adverse effects of wildlife translocations that result from disease transmission. In addition to examining the effects on target species, I discuss the possible direct and indirect effects of parasite translocations on sympatric species and on the evolution of ecosystems in the long-term. To reduce potential disease risks presented by wildlife translocations, I propose some guidelines for hygiene and quarantine procedures and for monitoring the parasite status of both captive and free-living animals.     

Conservation Implications of Host Use for Rare Parasitic Plants

Both the study and management of parasites have historically focused on the control, and even elimination, of parasite populations. In contrast, rare parasitic plants represent an uncommon challenge for conservation biologists and managers who often wish to bolster populations of these parasites. Although parasitic plants may suffer any of the maladies known to affect small populations of plants, parasitic plants may also be limited by the additional suite of factors of host availability, host quality, host resistance to parasitism, and parasite preference. We describe studies that have examined parasite growth and reproductive performance with a variety of host species to argue that consideration of the host needs of parasitic plants is necessary for successful conservation of rare species using this mode of resource acquisition. Although it is clear that parasite performance varies greatly with the availability of different host species, little is known about the host requirements of most parasitic plants, and the relative importance of particular host species may not immediately be obvious. Further, because published host lists generally do not distinguish minor hosts from those that sustain parasite populations, such lists may be misleading for conservation efforts. We argue that successful conservation and restoration of parasitic plants may necessitate the management of thoughtfully selected host populations.     

Parasite genotypes identify source populations of migratory fish more accurately than fish genotypes

DNA-based assignment of individuals to their population of origin has many applications such as mixed-stock analysis, identifying individuals from protected populations, and elucidating migration patterns. However, low genetic differentiation among populations will cause misassignments. Thus, an alternative means of determining an individual's population of origin is needed in cases where there is little or no neutral differentiation among source populations. Here, we test the hypothesis that parasite genotypes can be used to identify the origins of hosts more accurately than host genotypes. Using microsatellite markers from steelhead trout and their trematode parasites, we show that the odds of correct assignment are four times greater with the parasite's genotypes than with the host's genotypes. Our analyses show that this result is simply explained by the greater genetic structure among populations of the trematode parasite. Recent studies on the comparative genetic structure of other host and parasite species suggest that our results are not unusual or unique to the host-parasite system we studied. Thus, our work indicates that parasites will be useful for a wide range of applied and basic research that requires the assignment of individuals to source populations.     

Limited contributions of released animals from zoos to North American conservation translocations

With the loss of biodiversity accelerating, conservation translocations such as reintroductions are becoming an increasingly common conservation tool. Conservation translocations must source individuals for release from either wild or captive-bred populations. We asked what proportion of North American conservation translocations rely on captive breeding and to what extent zoos and aquaria (hereafter zoos) fulfill captive breeding needs. We searched for mention of captive breeding and zoo involvement in all 1863 articles included in the North American Conservation Translocations database, which comprises journal articles and grey literature published before 2014 on conservation translocations in Canada, the United States, Mexico, the Caribbean, and Central America before 2014 as identified by a comprehensive literature review. Conservation translocations involved captive breeding for 162 (58%) of the 279 animal species translocated. Fifty-four zoos contributed animals for release. The 40 species of animals bred for release by zoos represented only 14% of all animal species for which conservation translocations were published and only 25% of all animal species that were bred for releases occurring in North America. Zoo contributions varied by taxon, ranging from zoo-bred animals released in 42% of amphibian conservation translocations to zero contributions for marine invertebrates. Proportional involvement of zoos in captive-breeding programs for release has increased from 1974 to 2014 (r = 0.325, p = 0.0313) as has the proportion of translocation-focused scientific papers coauthored by zoo professionals (from 0% in 1974 to 42% in 2013). Although zoos also contribute to conservation translocations through education, funding, and professional expertise, increasing the contribution of animals for release in responsible conservation translocation programs presents a future conservation need and opportunity. We especially encourage increased dialogue and planning between the zoo community, academic institutions, and governments to optimize the direct contribution zoos can make to wildlife conservation through conservation translocations.     

Toward an integrative molecular approach to wildlife disease

Pathogens pose serious threats to human health, agricultural investment, and biodiversity conservation through the emergence of zoonoses, spillover to domestic livestock, and epizootic outbreaks. As such, wildlife managers are often tasked with mitigating the negative effects of disease. Yet, parasites form a major component of biodiversity that often persist. This is due to logistical challenges of implementing management strategies and to insufficient understanding of host–parasite dynamics. We advocate for an inclusive understanding of molecular diversity in driving parasite infection and variable host disease states in wildlife systems. More specifically, we examine the roles of genetic, epigenetic, and commensal microbial variation in disease pathogenesis. These include mechanisms underlying parasite virulence and host resistance and tolerance, and the development, regulation, and parasite subversion of immune pathways, among other processes. Case studies of devil facial tumor disease in Tasmanian devils (Sarcophilus harrisii) and chytridiomycosis in globally distributed amphibians exemplify the broad range of questions that can be addressed by examining different facets of molecular diversity. For particularly complex systems, integrative molecular analyses present a promising frontier that can provide critical insights necessary to elucidate disease dynamics operating across scales. These insights enable more accurate risk assessment, reconstruction of transmission pathways, discernment of optimal intervention strategies, and development of more effective and ecologically sound treatments that minimize damage to the host population and environment. Such measures are crucial when mitigating threats posed by wildlife disease to humans, domestic animals, and species of conservation concern.     

Do these eggs smell funny to you?: an experimental study of egg discrimination by hosts of the social parasite Polyergus breviceps (Hymenoptera: Formicidae)

Social parasites exploit the behaviours of other social species. Infiltration of host systems involves a variety of mechanisms depending on the conditions within the host society and the needs of the social parasite. For many species of socially parasitic ants, colony establishment entails the usurpation of colonies of other species. This frequently involves the eviction or death of the host colony queen and the subsequent adoption of the invading queen. The social parasite queen achieves host worker acceptance by either manipulating the nest-mate recognition processes of the host or undergoing chemical modification. Little is known, however, about how host workers respond to social parasite eggs or whether host species defend against brood parasitism during parasite invasions. Host species are believed to adopt social parasite offspring because the recent common ancestry between many social parasites and their hosts may grant the sharing of certain characteristics such as chemical cues. Use of multiple host species, however, suggests other processes are needed for the social bond between host and parasite young to form. This study reports the findings of adoption bioassays in which eggs from a slave-maker ant, Polyergus breviceps, were offered to workers of two of its host species from unparasitised or newly parasitised nests to determine whether P. breviceps eggs generally elicit rearing behaviours from multiple host species. Comparisons of parasite egg survival until adulthood with conspecific egg survival reveal that workers of both host species, free-living or newly enslaved, do not typically accept slave-maker eggs. Both host species thus have sufficient discriminatory power to reject social parasite eggs although our hydrocarbon analysis indicates parasite eggs may be adapted to their local host species. Combined these results suggest that host rearing of P. breviceps eggs may reflect an evolutionary equilibrium that is maintained by probability and cost of recognition errors.Communicated by L. Sundström     

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.     

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     

Parasites as conservation tools

Parasite success typically depends on a close relationship with one or more hosts; therefore, attributes of parasitic infection have the potential to provide indirect details of host natural history and are biologically relevant to animal conservation. Characterization of parasite infections has been useful in delineating host populations and has served as a proxy for assessment of environmental quality. In other cases, the utility of parasites is just being explored, for example, as indicators of host connectivity. Innovative studies of parasite biology can provide information to manage major conservation threats by using parasite assemblage, prevalence, or genetic data to provide insights into the host. Overexploitation, habitat loss and fragmentation, invasive species, and climate change are major threats to animal conservation, and all of these can be informed by parasites.     

Paradigms for parasite conservation

Parasitic species, which depend directly on host species for their survival, represent a major regulatory force in ecosystems and a significant component of Earth's biodiversity. Yet the negative impacts of parasites observed at the host level have motivated a conservation paradigm of eradication, moving us farther from attainment of taxonomically unbiased conservation goals. Despite a growing body of literature highlighting the importance of parasite‐inclusive conservation, most parasite species remain understudied, underfunded, and underappreciated. We argue the protection of parasitic biodiversity requires a paradigm shift in the perception and valuation of their role as consumer species, similar to that of apex predators in the mid‐20th century. Beyond recognizing parasites as vital trophic regulators, existing tools available to conservation practitioners should explicitly account for the unique threats facing dependent species. We built upon concepts from epidemiology and economics (e.g., host‐density threshold and cost‐benefit analysis) to devise novel metrics of margin of error and minimum investment for parasite conservation. We define margin of error as the risk of accidental host extinction from misestimating equilibrium population sizes and predicted oscillations, while minimum investment represents the cost associated with conserving the additional hosts required to maintain viable parasite populations. This framework will aid in the identification of readily conserved parasites that present minimal health risks. To establish parasite conservation, we propose an extension of population viability analysis for host–parasite assemblages to assess extinction risk. In the direst cases, ex situ breeding programs for parasites should be evaluated to maximize success without undermining host protection. Though parasitic species pose a considerable conservation challenge, adaptations to conservation tools will help protect parasite biodiversity in the face of an uncertain environmental future.     

A systematic review of snake translocations to identify potential tactics for reducing postrelease effects

Advancements in the field of reintroduction biology are needed, but understanding of how to effectively conduct translocations, particularly with snakes, is lacking. We conducted a systematic review of snake translocation studies to identify potential tactics for reducing postrelease effects. We included studies on intentional, human-mediated, wild–wild, or captive–wild translocations to any location, regardless of motive or number of snakes translocated. Only studies that presented results for at least 1 of 4 outcomes (movement behavior, site fidelity, survival, or population establishment) were included. We systematically searched 4 databases for published studies and used 5 methods to search the gray literature. Our search and screening criteria yielded 121 data sources, representing 130 translocation cases. We quantified the association between 15 translocation tactics and short-term translocation outcomes by calculating odds ratios and used forest plots to display results. Snake translocations involved 47 species (from mainly 2 families), and most were motivated by research, were monitored for at least 6 months, occurred in North America, and took place from the 1990s onward. The odds of a positive snake translocation outcome were highest with release of captive reared or juvenile snakes, release of social groups together, delayed release, provision of environmental enrichment or social housing before release, or minimization of distance translocated. The odds of a positive outcome were lowest when snakes were released early in their active season. Our results do not demonstrate causation, but outcomes of snake translocation were associated with 8 tactics (4 of which were strongly correlated). In addition to targeted comparative studies, we recommend practitioners consider the possible influence of these tactics when planning snake translocations.     

Cuckoo wasps manipulate foraging and resting activities in their hosts

Parasite-induced alterations in host behaviour have been reported in a large number of taxa. However, some parasites are better than others to exploit the resources offered by their hosts. To date, our understanding of the extent to which some obligate parasites exploit social insect colonies is still limited. In this study, we examined parasite-mediated behavioural alterations of Polistes biglumis wasps parasitized by the obligate social parasite Polistes atrimandibularis by comparing host female-activity in parasitized and non-parasitized colonies. Host foundresses foraged more and rested less in parasitized than in non-parasitized colonies (controlling for the number of larvae in the nest, the time of day, and the day in the season). Next, we used short-term parasite removal experiments to investigate how social parasites manipulate their hosts. We found that parasitized hosts foraged more and rested less when social parasites were on the nest rather than after their removal, and we tested which kind of interactions occurred between parasites and hosts. P. atrimandibularis parasites may use mainly non-aggressive interactions (such as antennation and trophallaxis) to manipulate host activities, rather than visual, acoustic or chemical signals as other parasites do.     

Fitness costs of neighborhood disruption in translocations of a solitary mammal

Translocation is used to reestablish wild populations of animals, but translocation projects often do not meet their objectives because postrelease mortality of animals is high. One reason for translocation failure is that the behavioral or ecological requirements of released animals are unmet. Maintaining founder-group social relationships during release can affect reestablishment of social species. Solitary territorial species with stable neighbors (restricted dispersal and lifetime occupation of a home range) of the same species may also benefit from the maintenance of these social relationships during translocation. We translocated Stephens' kangaroo rats (Dipodomys stephensi), a solitary species listed as endangered under the U.S. Endangered Species Act, with and without neighboring kangaroo rats. We compared the settlement (establishment of a stable home range) decisions and fitness of kangaroo rats between the 2 treatments. Kangaroo rats translocated with neighbors traveled shorter distances before establishing territories, had higher survival rates, and had significantly higher reproductive success than kangaroo rats translocated without neighbors. Number of offspring was 24-fold higher for kangaroo rats translocated with neighbors than those translocated without neighbors. Differences in behavior following release may partially explain differences in survival between the 2 groups. Immediately following release, animals translocated with neighbors fought less and spent significantly more time foraging and digging burrows than animals translocated without neighbors. Our results indicate that even for solitary species, maintaining relationships among members of a translocated group of animals can influence translocation success. This study is the first empirical demonstration of the fitness consequences of disrupting social relationships among territorial neighbors.     

Risk of Myxobolus cerebralis infection to rainbow trout in the Madison River, Montana, USA.

Myxobolus cerebralis, the parasite that causes salmonid whirling disease, has had detrimental effects on several salmonid populations in the Intermountain West, including the rainbow trout in the Madison River, Montana, USA. The goal of this study was to examine relationships among characteristics of the environment, Tubifex tubifex (the alternate host) populations, and rainbow trout whirling disease risk in the Madison River. Environmental characteristics were measured in side channels of the Madison River, and differences were described with a principal components analysis. The density of T. tubifex, the prevalence of infection in T. tubifex, and the density of infected T. tubifex were determined for the side channels using benthic core samples and examination of live tubificids for infection. The site-specific contribution to whirling disease risk in the side channels was determined using in situ exposures of sentinel rainbow trout. Regression analyses were used to determine correlations among these characteristics. Side channels differed in site-specific contribution to rainbow trout whirling disease risk, which was positively correlated to the density of infected T. tubifex. Side channels with fine sediments and lower water temperatures made greater site-specific contribution to whirling disease risk and had higher densities of infected T. tubifex than side channels with coarser sediments and higher temperatures. The ability to characterize areas of high whirling disease risk is essential for improving our understanding of the dynamics of M. cerebralis such that appropriate management strategies can be implemented. In addition, this study provides a model of how the disease ecology of complex aquatic parasites can be examined when the influential processes operate on different spatial scales.     

Almost royal: incomplete suppression of host worker ovarian development by a social parasite wasp

Insect social parasites, like other parasites, may benefit from inhibiting their host from reproducing (complete or partial parasitic castration) because they can then exploit more of the host’s resources for their own reproduction. In particular, social parasites that kill or expel the host queen need to prevent host workers from reproducing; this is a common worker response to the absence of their queen. Indeed, host workers would benefit from detecting the presence of the parasite and investing in direct and indirect fitness. Studying whether and how social parasites control host worker reproduction can provide information about the degree of integration of the parasite in the host colony and help identify factors regulating workers’ reproductive decisions in social insects. We investigated whether the paper wasp social parasite, Polistes sulcifer, suppresses Polistes dominula (host) worker reproduction as efficiently as the dominant host female does in queen-right colonies by comparing worker reproductive efforts in parasitized and non-parasitized (control) colonies. Our results show that 6 weeks after usurpation of their colony by the social parasite, parasitized workers (1) had more developed ovaries than control workers and (2) laid more eggs as soon as the opportunity arose. This reproductive readiness of parasitized workers was not apparent 2 weeks after colony usurpation. This suggests that P. dominula workers have evolved means to react to social parasitism, as occurs in some ants, and that the parasite has only limited control over host reproduction.     

Refuge sharing network predicts ectoparasite load in a lizard

Living in social groups facilitates cross-infection by parasites. However, empirical studies on indirect transmission within wildlife populations are scarce. We investigated whether asynchronous overnight refuge sharing among neighboring sleepy lizards, Tiliqua rugosa, facilitates indirect transmission of its ectoparasitic tick, Amblyomma limbatum. We fitted 18 neighboring lizards with GPS recorders, observed their overnight refuge use each night over 3 months, and counted their ticks every fortnight. We constructed a transmission network to estimate the cross-infection risk based on asynchronous refuge sharing frequencies among all lizards and the life history traits of the tick. Although self-infection was possible, the network provided a powerful predictor of measured tick loads. Highly connected lizards that frequently used their neighbors’ refuges were characterized by higher tick loads. Thus, indirect contact had a major influence on transmission pathways and parasite loads. Furthermore, lizards that used many different refuges had lower cross- and self-infection risks and lower tick loads than individuals that used relatively fewer refuges. Increasing the number of refuges used by a lizard may be an important defense mechanism against ectoparasite transmission in this species. Our study provides important empirical data to further understand how indirectly transmitted parasites move through host populations and influence individual parasite loads.