Cross‐continental comparison of parasite communities in a wide‐ranging carnivore suggests associations with prey diversity and host density

1. Parasites are integral to ecosystem functioning yet often overlooked. Improved understanding of host–parasite associations is important, particularly for wide‐ranging species for which host range shifts and climate change could alter host–parasite interactions and their effects on ecosystem function.
2. Among the most widely distributed mammals with diverse diets, gray wolves (Canis lupus) host parasites that are transmitted among canids and via prey species. Wolf–parasite associations may therefore influence the population dynamics and ecological functions of both wolves and their prey. Our goal was to identify large‐scale processes that shape host–parasite interactions across populations, with the wolf as a model organism.
3. By compiling data from various studies, we examined the fecal prevalence of gastrointestinal parasites in six wolf populations from two continents in relation to wolf density, diet diversity, and other ecological conditions.
4. As expected, we found that the fecal prevalence of parasites transmitted directly to wolves via contact with other canids or their excreta was positively associated with wolf density. Contrary to our expectations, the fecal prevalence of parasites transmitted via prey was negatively associated with prey diversity. We also found that parasite communities reflected landscape characteristics and specific prey items available to wolves.
5. Several parasite taxa identified in this study, including hookworms and coccidian protozoans, can cause morbidity and mortality in canids, especially in pups, or in combination with other stressors. The density–prevalence relationship for parasites with simple life cycles may reflect a regulatory role of gastrointestinal parasites on wolf populations. Our result that fecal prevalence of parasites was lower in wolves with more diverse diets could provide insight into the mechanisms by which biodiversity may regulate disease. A diverse suite of predator–prey interactions could regulate the effects of parasitism on prey populations and mitigate the transmission of infectious agents, including zoonoses, spread via trophic interactions.

     

Ranging patterns and parasitism in primates

Competing hypotheses exist concerning the influence of ranging patterns on parasitism. More intensive use of a home range could result in greater exposure to infectious agents that accumulate in the soil. Alternatively, when more intensive ranging is associated with territorial defence, this could decrease home range overlap and produce lower levels of parasitism. We tested these hypotheses using phylogenetic comparative methods and parasite richness data for 119 primate species. Helminth richness increased with the defensibility index, a quantitative measure of home range use that correlates with the degree of territoriality in primates. This association was independent of other host traits that influence parasite richness in primates. Results involving non-vector transmitted helminths produced the most significant results, suggesting that the relationship between territorial behaviour and parasitism is driven by accumulation of parasites in defended home ranges. In addition, costs associated with greater ranging could increase susceptibility to infectious agents.     

Transmission Patterns of Pinworms in Two Sympatric Congeneric Primate Species

Understanding pathogen transmission is essential to addressing the dynamics of infectious diseases in animal populations. Directly transmitted parasites spread in host populations via 1) contact with infected individuals and 2) contact with contaminated substrates. Although studies exist that support social or ranging effects on transmission, it is less clear how these factors interact. We test the hypothesis that a combination of social, ranging, diet, and intrinsic factors account for Trypanoxyuris minutus (pinworm) infections in sympatric howler species Alouatta palliata and A. pigra. We collected 211 howler fecal samples from 34 adults living in four groups, two of each species, in Tabasco (Mexico), and calculated pinworm prevalence and eggs per gram of feces (EPG). We followed each group for 80 h to determine ranging, diet, frequency of contact, and conspecific proximity. Prevalence of Trypanoxyuris minutus was high, with 82% of all individuals infected. Logistic modeling indicated that pinworm prevalence was positively associated with proximity and the proportion of group members contacted by focal individuals. Although EPG results should be interpreted cautiously owing to variable egg excretion, this index was also positively associated with proximity and the proportion of group members that were contacted, as well as with dietary diversity and use of non-tree foods. Neither intrinsic factors such as species and sex, nor group and population level variables, such as group and home range size, home range overlap, and intensity of range use, were significant predictors of pinworm infection. We conclude that both sociality and feeding behavior are key factors in infection dynamics of Trypanoxyuris minutus in sympatric Alouatta palliata and A. pigra, confirming that contact with infected conspecifics and contaminated substrates are important mechanisms for directly transmitted parasites.     

Primate disease ecology in comparative and theoretical perspective

Infectious disease plays a major role in the lives of wild primates, and the past decade has witnessed significant strides in our understanding of primate disease ecology. In this review, I briefly describe some key findings from phylogenetic comparative approaches, focusing on analyses of parasite richness that use the Global Mammal Parasite Database. While these studies have provided new answers to fundamental questions, new questions have arisen, including questions about the underlying epidemiological mechanisms that produce the broader phylogenetic patterns. I discuss two examples in which theoretical models have given us new traction on these comparative questions. First, drawing on findings of a positive association between range use intensity and the richness of helminth parasites, we developed a spatially explicit agent-based model to investigate the underlying drivers of this pattern. From this model, we are gaining deeper understanding of how range use intensity results in greater exposure to parasites, thus producing higher prevalence in the simulated populations-and, plausibly, higher parasite richness in comparative analyses. Second, I show how a model of disease spread on social networks provides solid theoretical foundations for understanding the effects of sociality and group size on parasitism across primate species. This study further revealed that larger social groups are more subdivided, which should slow the spread of infectious diseases. This effect could offset the increased disease risk expected in larger social groups, which has yet to receive strong empirical support in our comparative analyses. In addition to these examples, I discuss the need for more meta-analyses of individual-level phenomena documented in the field, and for greater linkage between theoretical modeling and field research.     

Does habitat disturbance increase infectious disease risk for primates?

Many studies have suggested that ecosystem conservation protects human and wildlife populations against infectious disease. We tested this hypothesis using data on primates and their parasites. First, we tested for relationships between species' resilience to human disturbance and their parasite richness, prevalence and immune defences, but found no associations. We then conducted a meta‐analysis of the effects of disturbance on parasite prevalence, which revealed no overall effect, but a positive effect for one of four types of parasites (indirectly transmitted parasites). Finally, we conducted intraspecific analyses of malaria prevalence as a function of mammalian species richness in chimpanzees and gorillas, and an interspecific analysis of geographic overlap and parasite species richness, finding that higher levels of host richness favoured greater parasite risk. These results suggest that anthropogenic effects on disease transmission are complex, and highlight the need to define the conditions under which environmental change will increase or decrease disease transmission.     

The anthropogenic environment lessens the intensity and prevalence of gastrointestinal parasites in Balinese long-tailed macaques (<Emphasis Type="Italic">Macaca fascicularis</Emphasis>)

The distribution of wildlife parasites in a landscape is intimately tied to the spatial distribution of hosts. In parasite species, including many gastrointestinal parasites, with obligate or common environmental life stages, the dynamics of the parasite can also be strongly affected by geophysical components of the environment. This is especially salient in host species, for example humans and macaques, which thrive across a wide variety of habitat types and quality and so are exposed to a wealth of environmentally resilient parasites. Here, we examine the effect of environmental and anthropogenic components of the landscape on the prevalence, intensity, and species diversity of gastrointestinal parasites across a metapopulation of long-tailed macaques on the island of Bali, Indonesia. Using principal-components analysis, we identified significant interaction effects between specific environmental and anthropogenic components of the landscape, parsing the Balinese landscape into anthropogenic (PC1), mixed environment (PC2), and non-anthropogenic (PC3) components. Further, we determined that the anthropogenic environment can mitigate the prevalence and intensity of specific gut parasites and the intensity of the overall community of gut parasites, but that non-anthropogenically driven landscape components have no significant effect in increasing or reducing the intensity or prevalence of the community of gut parasites in Balinese macaques.     

Spread of an introduced parasite across the Hawaiian archipelago independent of its introduced host

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Priority effects within coinfected hosts can drive unexpected population‐scale patterns of parasite prevalence

Organisms are frequently coinfected by multiple parasite strains and species, and interactions between parasites within hosts are known to influence parasite prevalence and diversity, as well as epidemic timing. Importantly, interactions between coinfecting parasites can be affected by the order in which they infect hosts (i.e. within‐host priority effects). In this study, we use a single‐host, two‐pathogen, SI model with environmental transmission to explore how within‐host priority effects scale up to alter host population‐scale infection patterns. Specifically, we ask how parasite prevalence changes in the presence of different types of priority effects. We consider two scenarios without priority effects and four scenarios with priority effects where there is either an advantage or a disadvantage to being the first to infect in a coinfected host. Models without priority effects always predict negative relationships between the prevalences of both parasites. In contrast, models with priority effects can yield unimodal prevalence relationships where the prevalence of a focal parasite is minimized or maximized at intermediate prevalences of a coinfecting parasite. The mechanism behind this pattern is that as the prevalence of the coinfecting parasite increases, most infections of the focal parasite change from occurring as solo infections, to first arrival coinfections, to second arrival coinfections. The corresponding changes in parasite fitness as the focal parasite moves from one infection class to another then map to changes in focal parasite prevalence. Further, we found that even when parasites interact negatively within a host, they still can have positive prevalence relationships at the population scale. These results suggest that within‐host priority effects can change host population‐scale infection patterns in systematic (and initially counterintuitive) ways, and that taking them into account may improve disease forecasting in coinfected populations.     

Experimental warming drives a seasonal shift in the timing of host‐parasite dynamics with consequences for disease risk

Multi‐species experiments are critical for identifying the mechanisms through which climate change influences population dynamics and community interactions within ecological systems, including infectious diseases. Using a host–parasite system involving freshwater snails, amphibians and trematode parasites, we conducted a year‐long, outdoor experiment to evaluate how warming affected net parasite production, the timing of infection and the resultant pathology. Warming of 3 °C caused snail intermediate hosts to release parasites 9 months earlier and increased infected snail mortality by fourfold, leading to decreased overlap between amphibians and parasites. As a result, warming halved amphibian infection loads and reduced pathology by 67%, despite comparable total parasite production across temperature treatments. These results demonstrate that climate–disease theory should be expanded to account for predicted changes in host and parasite phenology, which may often be more important than changes in total parasite output for predicting climate‐driven changes in disease risk.     

Effects of hunting on cougar spatial organization

The effects of increased mortality on the spatial dynamics of solitary carnivores are not well understood. We examined the spatial ecology of two cougar populations that differed in hunting intensity to test whether increased mortality affected home range size and overlap. The stability hypothesis predicts that home range size and overlap will be similar for both sexes among the two areas. The instability hypothesis predicts that home range size and overlap will be greater in the heavily hunted population, although may differ for males versus females due to behavior strategies. We marked 22 adult resident cougars in the lightly hunted population and 20 in the heavily hunted population with GPS collars from 2002 to 2008. Cougar densities and predation rates were similar among areas, suggesting no difference in per capita resources. We compared home range size, two‐dimensional home range overlap, and three‐dimensional utilization distribution overlap index (UDOI) among annual home ranges for male and female cougars. Male cougars in the heavily hunted area had larger sized home ranges and greater two‐dimensional and three‐dimensional UDOI overlap than those in the lightly hunted area. Females showed no difference in size and overlap of home range areas between study populations – further suggesting that differences in prey quantity and distribution between study areas did not explain differences in male spatial organization. We reject the spatial stability hypothesis and provide evidence to support the spatial instability hypothesis. Increased hunting and ensuing increased male home range size and overlap may result in negative demographic effects for cougars and potential unintended consequences for managers.     

High intensity and prevalence of two species of trematode metacercariae in the fathead minnow (Pimephales promelas) with no compromise of minnow anti-predator competence

Opportunity for parasites to manipulate host behavioral phenotype may be influenced by several factors, including the host ecology and the presence of cohabiting parasites in the same host. Metacercariae of Ornithodiplostomum ptychocheilus and "black spot" Crassiphiala bulboglossa have similar life cycles. Each parasite uses a littoral snail as a first intermediate host, fathead minnows as a second intermediate host, and a piscivorous bird as a final host. Metacercariae of black spot encyst in the dermal and epidermal tissues, while metacercariae of O. ptychocheilus encyst on the brain over a region that coordinates optomotor responses. Because of site differences within the host, we predicted that O. ptychocheilus metacercariae might manipulate the behavioral phenotype of minnows to facilitate transmission to the final host, but metacercariae of black spot would not. In our study population, prevalence was 100% for O. ptychocheilus , with an overall median intensity of 105 metacercariae per minnow. Prevalence of black spot was 60%, with a median abundance and intensity of 12 and 20 metacercariae per minnow for the overall sample and for infected fish, respectively. Minnows accumulated both parasites over time, producing significant correlations between intensity and minnow body length and between intensities of the 2 parasites. Minnows infected with black spot had on average twice as many O. ptychocheilus metacercariae as similar-sized minnows without any black spot cercariae. We found no correlation between body condition of minnows and intensity for either parasite. We measured 2 aspects of anti-predator competence to test for effects linked to parasite intensity. We found no correlation between intensity of either species of parasite and latency to behavioral response to attack from a mechanical model heron, nor was there any effect of parasite intensity on a measure of shoaling affinity. The absence of any detectable effect of metacercariae on anti-predator competence in minnows may reflect selection against parasite pathology from predation by non-hosts of the parasites and overwinter mortality due to low dissolved oxygen.     

Does home range use explain the relationship between group size and parasitism? A test with two sympatric species of howler monkeys

Group size is related to parasite infections in primates. This relationship probably reflects the fact that group size is associated with body contact between group members and with contact with contaminated items in the environment. The latter is highly associated with range use. In the present study we hypothesized that if infection by directly transmitted parasites (DTP) is mainly determined by the exposure of individuals to parasites that accumulate in the environment, and group size correlates negatively with the intensity of home range use, then smaller groups should be more infected by DTP. Additionally, groups that share a higher proportion of their home range with other groups should be more infected. To test our hypothesis we observed and collected fecal samples of two groups of Alouatta palliata (large group size) and two groups of A. pigra (small group size) that live sympatrically in a forest fragment located in Macuspana (Mexico). Group size was positively correlated with range area size and negatively correlated with the intensity of home range use. Range use variables were not related to either DTP prevalence or load. However, there were significant differences in DTP loads between groups, which were positively correlated with group size. Our results suggest that the intensity of home range use is a poor predictor of DTP infection parameters in groups with marked differences in size. Therefore, it is possible that the individual or combined effects of other ecological (e.g., microclimate), social (e.g., contact rate), or physiological (e.g., immune function) factors are more important in the dynamics of DTP in free-ranging primates.     

Links between habitat degradation,and social group size,ranging, fecundity,and parasite prevalence in the Tana River mangabey (Cercocebus galeritus)

We investigated the effects of anthropogenic habitat degradation on group size, ranging, fecundity, and parasite dynamics in four groups of the Tana River mangabey (Cercocebus galeritus). Two groups occupied a forest disturbed by human activities, while the other two occupied a forest with no human disturbance. We predicted that the groups in the disturbed forest would be smaller, travel longer distances daily, and have larger home ranges due to low food tree abundance. Consequently, these groups would have lower fecundity and higher parasite prevalence and richness (number of parasite species). We measured the abundance of food trees and anthropogenic activity in the forests, the groups' daily travel distances and home range sizes, and censused social groups over 12 months. We also analyzed fecal samples for gastrointestinal parasites from three of the groups. The disturbed forest had a lower abundance of food trees, and groups in this forest traveled longer distances, had larger home range sizes, were smaller, and had lower fecundity. The groups in the disturbed forest had higher, although not statistically significant, parasite prevalence and richness. This study contributes to a better understanding of how anthropogenic habitat change influences fecundity and parasite infections in primates. Our results also emphasize the strong influence of habitat quality in determining daily travel distance and home range size in primates. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density

Aim  Comparative studies have revealed strong links between ecological factors and the number of parasite species harboured by different hosts, but studies of different taxonomic host groups have produced inconsistent results. As a step towards understanding the general patterns of parasite species richness, we present results from a new comprehensive data base of over 7000 host–parasite combinations representing 146 species of carnivores (Mammalia: Carnivora) and 980 species of parasites.
Methods  We used both phylogenetic and non-phylogenetic comparative methods while controlling for unequal sampling effort within a multivariate framework to ascertain the main determinants of parasite species richness in carnivores.
Results  We found that body mass, population density, geographical range size and distance from the equator are correlated with overall parasite species richness in fissiped carnivores. When parasites are classified by transmission mode, body mass and home range area are the main determinants of the richness of parasites spread by close contact between hosts, and population density, geographical range size and distance from the equator account for the diversity of parasites that are not dependent on close contact. For generalist parasites, population density, geographical range size and latitude are the primary predictors of parasite species richness. We found no significant ecological correlates for the richness of specialist or vector-borne parasites.
Main conclusions  Although we found that parasite species richness increases instead of decreases with distance from the equator, other comparative patterns in carnivores support previous findings in primates, suggesting that similar ecological factors operate in both these independent evolutionary lineages.     

Helminth communities of the lesser sandeel Ammodytes tobianus L. off the west coast of Ireland

The helminth parasites present in 412 lesser sandeels (Ammodytes tobianus) taken from June 1996 to May 1997 from the Aran Islands on the west coast of Ireland were examined. Ten helminth parasite species were recorded, and more than 92% of the sandeels were infected with at least 1 helminth species. Seven of the species were digeneans, including Brachyphallus crenatus, Hemiurus communis, Derogenes varicus, Lecithaster gibbosus, Opechona bacillaris, Cryptocotyle lingua, and Galactosomum lacteum; 2 nematodes, including Hysterothylacium sp. and Contracaecum sp.; and 1 cestode, Scolex pleuronectis. Three of the 7 digenean species were either larvae or immature. Only 2 species, the digeneans G. lacteum and H. communis, had prevalences greater than 50%. The dominant species was G. lacteum, accounting for 67% of all parasites present. The relationship between spawned groups, host length, and season versus the abundance, prevalence, species richness, and the total number of parasites in the infracommunities was investigated. No difference was found between the parasite communities of the 2 spawning races of the host population. Mean abundance and prevalence of the different parasite species showed seasonal variation. Numbers of parasite species and numbers of parasites increased with fish length. The role of A. tobianus as an intermediate host for helminths was assessed; it was determined that most were infectious to birds or mammals, with the majority of the parasite species being autogenic (infectious to fish). The mean number of parasites per fish was nearly a quarter of the value recorded for A. tobianus in the North Sea, where a much higher intensity of infection was recorded.     

An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence

Epidemiological models predict a positive relationship between host population density and abundance of macroparasites. Here I lest these by a comparative study. I used data on communities of four groups of parasites inhabiting the gastrointestinal tract of mammals, nematodes of the orders Oxyurida. Ascarida. Enoplida and Spirurida. respectively. The data came from 44 mammalian species and represent examination of 16886 individual hosts. I studied average prevalence of all nematodes within an order in a host species, a measure of community level abundance, and considered the potential confounding effects of host body weight, fecundity, age at maturity and diet. Host population density was positively correlated with parasite prevalence within the order Oxyurida, where all species have direct life cycles. Considering the effects of other variables did not change this. This supports the assumption that parasite transmission rate generally is a positive function of host population density_: It also strengthens the hypothesis that host densities generally act as important determinants of species richness among directly transmitted parasites and suggests that negative influence of such parasites on host population growth rate increase with increasing host population density among host species. Within the other three nematode orders, where a substantial number of the species have indirect life cycles, no relationships between prevalence and host population density were seen, Again. considering the effects of other variables did not affect this conclusion. This suggests that host population density is a poor predictor of species richness of indirectly transmitted parasites and that effects of such parasites on host population dynamics do not scale with host densities among species of hosts.     

Gastrointestinal parasites of critically endangered primates endemic to Tana River, Kenya: Tana River red colobus (Procolobus rufomitratus) and crested mangabey (Cercocebus galeritus)

We conducted fecal egg counts of gastrointestinal parasites of 2 critically endangered primates endemic to the forest of Tana River, Kenya. We aimed to use the fecal egg counts as proxies to quantify the prevalence of gastrointestinal parasites between the 2 primates. The Tana River red colobus (Procolobus rufomitratus) and crested mangabey (Cercocebus galeritus) are of similar body size, but their behavioral ecology is very different. We predicted that mangabeys would have a higher prevalence of parasites because they are mostly terrestrial omnivores, live in larger social groups, and therefore range widely. We detected 10 nematodes and 3 protozoans in mangabeys and 7 nematodes and 2 protozoans in colobus. We detected a higher number of different parasite species in individual mangabeys, and 4 of the 5 nematodes requiring intermediate hosts were found in mangabeys. The overall prevalence of parasites was higher for mangabeys, but this difference was not statistically significant. For colobus, we found a trend whereby the number of different parasite species in individual monkeys was higher in males and in lactating females. However, there was no difference in the prevalence of parasites between the sexes or between lactating and nonlactating females.     

Seasonal dynamics of the acanthocephalan Pomphorhynchm laevis (Müller, 1776) in its intermediate and preferred definitive hosts

No seasonal cycle was found in either the prevalence or the intensity of natural Pomphorhynchus laevis infections in Leuciscus cephalus . There was a slight seasonal change in female maturity distribution but only irregular fluctuations in the size structure of the adult parasite population throughout the year. Cystacanths were available in all seasons. Rates of parasite growth, maturation and mortality, but not establishment, increased with water temperature (or factors indirectly associated with elevated water temperature) in laboratory-infected Salmo gairdneri . Increased rates of parasite growth and maturation mask any marked shifts in the size and maturity structure of the adult parasite population which might otherwise be due to the higher turnover of adult parasites in the summer months.     

Density dependence and the spread of anthelmintic resistance

Variation in the strength of selection pressures acting upon different subpopulations may cause density-dependent regulatory processes to act differentially on particular genotypes and may influence the rate of selection of adaptive traits. Using host-helminth parasite systems as examples, we investigate the impact of different positive and negative density dependence on the potential spread of anthelmintic resistance. Following chemotherapy, the negative density-dependent processes restricting parasite population growth will be relaxed, increasing the genetic contribution of resistant parasites to the next generation. Simple deterministic models of directly transmitted nematodes that merge population dynamics and genetics show that the frequency of drug-resistant alleles may increase faster in species whose population size is down-regulated by density-dependent parasite fecundity than in species with density-dependent establishment or parasite mortality. A genetically structured population dynamics model of an indirectly transmitted nematode is used to highlight how population regulation will influence the resistance allele frequency in different parasite lifestages. Results indicate that surveys aimed at monitoring the evolution of drug resistance should consider carefully which life stage to sample, and the time following treatment samples should be collected. Anthelmintic resistance offers a good opportunity to apply fundamental evolutionary and ecological principles to the management of a potentially crucial public health problem.