Endoparasite Species Richness of Iberian Carnivores: Influences of Host Density and Range Distribution

We investigate the determinants of macroparasite species richness of Iberian carnivores. For this, we used the parasitological data collected on 14 species of carnivores over a 10-year period. These previously unpublished data permitted to estimate parasite species richness using estimators of species richness, i.e. Jackknife first order and Chao 2. Most of the parasite species were rare, with low prevalence. Potential determinants were investigated as possible factors explaining the variability of parasites species richness among carnivores host body mass, host geographical range, host longevity and host density. Using independent contrasts, we found positive relationships between residuals of estimates of parasite species richness and residuals in host density, and between residuals of estimates of parasite species richness and residuals in host range. These results are discussed in terms of risk of extinction and invasion abilities related to a possible investment in immune defences correlated with parasite diversity.     

Bat fly species richness in Neotropical bats: correlations with host ecology and host brain

Patterns of ectoparasite species richness in mammals have been investigated in various terrestrial mammalian taxa such as primates, ungulates and carnivores. Several ecological or life traits of hosts are expected to explain much of the variability in species richness of parasites. In the present comparative analysis we investigate some determinants of parasite richness in bats, a large and understudied group of flying mammals, and their obligate blood-sucking ectoparasite, streblid bat flies (Diptera). We investigate the effects of host body size, geographical range, group size and roosting ecology on the species richness of bat flies in tropical areas of Venezuela and Peru, where both host and parasite diversities are high. We use the data from a major sampling effort on 138 bat species from nine families. We also investigate potential correlation between bat fly species richness and brain size (corrected for body size) in these tropical bats. We expect a relationship if there is a potential energetic trade-off between costly large brains and parasite-mediated impacts. We show that body size and roosting in cavities are positively correlated with bat fly species richness. No effects of bat range size and group size were observed. Our results also suggest an association between body mass-independent brain size and bat fly species richness. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

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.     

Sexual selection explains more functional variation in the mammalian major histocompatibility complex than parasitism

Understanding drivers of genetic diversity at the major histocompatibility complex (MHC) is vitally important for predicting how vertebrate immune defence might respond to future selection pressures and for preserving immunogenetic diversity in declining populations. Parasite-mediated selection is believed to be the major selective force generating MHC polymorphism, and while MHC-based mating preferences also exist for multiple species including humans, the general importance of mate choice is debated. To investigate the contributions of parasitism and sexual selection in explaining among-species variation in MHC diversity, we applied comparative methods and meta-analysis across 112 mammal species, including carnivores, bats, primates, rodents and ungulates. We tested whether MHC diversity increased with parasite richness and relative testes size (as an indicator of the potential for mate choice), while controlling for phylogenetic autocorrelation, neutral mutation rate and confounding ecological variables. We found that MHC nucleotide diversity increased with parasite richness for bats and ungulates but decreased with parasite richness for carnivores. By contrast, nucleotide diversity increased with relative testes size for all taxa. This study provides support for both parasite-mediated and sexual selection in shaping functional MHC polymorphism across mammals, and importantly, suggests that sexual selection could have a more general role than previously thought.     

Life history, ecology and parasite community structure in Soviet birds

The paper describes an investigation of parasite richness in relation to host life history and ecology using data from an extensive survey of helminth parasites (cestodes, trematodes and nematodes) in Soviet birds. Correlates of parasite richness (number of parasite species per host species) were sought among 13 life-history variables, 13 ecological variables and one non-biological variable (number of host individuals examined) across a sample of 158 species of host. A statistical method to control for the effects of phylogenetic association was adopted throughout. Parasite richness correlates positively with the number of hosts examined (sample size) in all three parasite groups. Positive correlations (after controlling for the effects of sample size) were also found between host body weight and parasite richness for trematodes and nematodes, but not for cestodes.
A number of ecological variables were associated with parasite richness. However, when the effects of sample size and body weight were controlled for, only a single significant correlation (an association between trematode richness and aquatic habitat) remained. Similarly, a number of significant correlates of parasite richness were found among the life-history variables examined. Though several of these were robust to the confounding effects of sample size, all could be explained by the co-variation between life-history traits and body weight among the host species under investigation.     

MHC variability, life-traits and parasite diversity of European cyprinid fish

Potential links between fish life history traits, an immune investment as measured by variability of the MHC genes and parasitism were analysed in 14 species of cyprinid fish. The hypothesis of the diversity of MHC genes being driven by high parasite diversity, i.e. species richness, was tested and a potential relationship between the MHC diversity and fish life-history traits including adult mortality rate, fecundity, longevity and maturity was investigated. Molecular techniques (SSCP and sequencing) were applied to analyse the MHC nucleotide diversity of the exons 2 and 3 of DAB genes belonging to the MHC class IIB. The comparative analyses, using phylogenetic independent contrasts, revealed a negative relationship between parasite species richness and adult fish mortality rate. We also found a positive relationship between nucleotide diversity of the exon 2 and parasite species richness. Our results suggest that fish species, of which populations are exposed to high parasite pressure, in terms of high parasite species richness, maintain a high genetic diversity of the exon 2 of the MHC genes (presenting the peptide binding regions), allowing them to decrease their natural mortality rate.     

Parasite diversity declines with host evolutionary distinctiveness: A global analysis of carnivores

Evolutionarily distinctive host lineages might harbor fewer parasite species because they have fewer opportunities for parasite sharing than hosts having extant close relatives, or because diverse parasite assemblages promote host diversification. We evaluate these hypotheses using data from 930 species of parasites reported to infect free‐living carnivores. We applied nonparametric richness estimators to estimate parasite diversity among well‐sampled carnivore species and assessed how well host evolutionary distinctiveness, relative to other biological and environmental factors, explained variation in estimated parasite diversity. Species richness estimates indicate that the current published literature captures less than 50% of the true parasite diversity for most carnivores. Parasite species richness declined with evolutionary distinctiveness of carnivore hosts (i.e., length of terminal ranches of the phylogeny) and increased with host species body mass and geographic range area. We found no support for the hypothesis that hosts from more diverse lineages support a higher number of generalist parasites, but we did find evidence that parasite assemblages might have driven host lineage diversification through mechanisms linked to sexual selection. Collectively, this work provides strong support for host evolutionary history being an essential predictor of parasite diversity, and offers a simple model for predicting parasite diversity in understudied carnivore species.     

Species loss on spatial patterns and composition of zoonotic parasites

Species loss can result in the subsequent loss of affiliate species. Though largely ignored to date, these coextinctions can pose threats to human health by altering the composition, quantity and distribution of zoonotic parasites. We simulated host extinctions from more than 1300 host–parasite associations for 29 North American carnivores to investigate changes in parasite composition and species richness. We also explored the geography of zoonotic parasite richness under three carnivore composition scenarios and examined corresponding levels of human exposure. We found that changes in parasite assemblages differed among parasite groups. Because viruses tend to be generalists, the proportion of parasites that are viruses increased as more carnivores went extinct. Coextinction of carnivore parasites is unlikely to be common, given that few specialist parasites exploit hosts of conservation concern. However, local extirpations of widespread carnivore hosts can reduce overall zoonotic richness and shift distributions of parasite-rich areas. How biodiversity influences disease risks remains the subject of debate. Our results make clear that hosts vary in their contribution to human health risks. As a consequence, so too does the loss (or gain) of particular hosts. Anticipating changes in host composition in future environments may help inform parasite conservation and disease mitigation efforts.     

Do threatened hosts have fewer parasites? A comparative study in primates

1. Parasites and infectious diseases have become a major concern in conservation biology, in part because they can trigger or accelerate species or population declines. Focusing on primates as a well-studied host clade, we tested whether the species richness and prevalence of parasites differed between threatened and non-threatened host species. 2. We collated data on 386 species of parasites (including viruses, bacteria, protozoa, helminths and arthropods) reported to infect wild populations of 36 threatened and 81 non-threatened primate species. Analyses controlled for uneven sampling effort and host phylogeny. 3. Results showed that total parasite species richness was lower among threatened primates, supporting the prediction that small, isolated host populations harbour fewer parasite species. This trend was consistent across three major parasite groups found in primates (helminths, protozoa and viruses). Counter to our predictions, patterns of parasite species richness were independent of parasite transmission mode and the degree of host specificity. 4. We also examined the prevalence of selected parasite genera among primate sister-taxa that differed in their ranked threat categories, but found no significant differences in prevalence between threatened and non-threatened hosts. 5. This study is the first to demonstrate differences in parasite richness relative to host threat status. Results indicate that human activities and host characteristics that increase the extinction risk of wild animal species may lead simultaneously to the loss of parasites. Lower average parasite richness in threatened host taxa also points to the need for a better understanding of the cascading effects of host biodiversity loss for affiliated parasite species.     

Host traits associated with species roles in parasite sharing networks

The community of host species that a parasite infects is often explained by functional traits and phylogeny, predicting that closely related hosts or those with particular traits share more parasites with other hosts. Previous research has examined parasite community similarity by regressing pairwise parasite community dissimilarity between two host species against host phylogenetic distance. However, pairwise approaches cannot target specific host species responsible for disproportionate levels of parasite sharing. To better identify why some host species contribute differentially to parasite diversity patterns, we represent parasite sharing using ecological networks consisting of host species connected by instances of shared parasitism. These networks can help identify host species and traits associated with high levels of parasite sharing that may subsequently identify important hosts for parasite maintenance and transmission within communities. We used global‐scale parasite sharing networks of ungulates, carnivores, and primates to determine if host importance – encapsulated by the network measures degree, closeness, betweenness, and eigenvector centrality – was predictable based on host traits. Our findings suggest that host centrality in parasite sharing networks is a function of host population density and range size, with range size reflecting both species geographic range and the home range of those species. In the full network, host taxonomic family became an important predictor of centrality, suggesting a role for evolutionary relationships between host and parasite species. More broadly, these findings show that trait data predict key properties of ecological networks, thus highlighting a role for species traits in understanding network assembly, stability, and structure.     

Incorporating parasite systematics in comparative analyses of variation in spleen mass and testes sizes of rodents

Parasite diversity is hypothesized to act on host life-history traits through investment in immunity. In order to incorporate the diversity of the parasite community that an individual host or a host species may face, two indices can be used: Taxonomic Species Richness and Taxonomic Entropy, where the taxonomic information is incorporated with the taxonomic weight. We tested whether these indices correlate with several morphological traits potentially implicated in immune defence and in reproduction, using data on gastrointestinal helminths and their rodent hosts sampled in Southeast Asia. We found no relationship between parasite diversity indices and either spleen mass or testes size at the intraspecific level, i.e. at the level of individuals. At the interspecific level, we found no relationship between the parasite diversity indices and testes size. However, we found that female spleen mass is significantly influenced by the specific species richness of parasites, whereas male spleen mass is influenced by individual mean parasite diversity indices. We concluded that female spleen mass may have evolved in response to gastrointestinal helminth pressure acting at species levels, while in males, the individual spleen mass could be constrained by other factors, such as the blood storage function of the spleen.     

Host traits and parasite species richness in even and odd-toed hoofed mammals, Artiodactyla and Perissodactyla

Host social, ecological and life history traits are predicted to influence both parasite establishment within host species and the distribution of parasites among host species. Yet only a few studies have investigated the role multiple host traits play in determining patterns of infection across diverse parasite groups. To explore the association between host traits and parasite species richness (PSR), we assembled a comprehensive database encompassing 601 parasites (including viruses, bacteria, protozoa, helminths and arthropods) reported to infect 96 species from two well-studied and diverse host clades: even- and odd-toed hoofed mammals (Artiodactyla and Perissodactyla). Comparative analyses were used to examine associations between three sets of host variables (life history and body mass, social and mating behavior, and ecological traits) and PSR for all parasites combined and for distinct parasite sub-groups. Results from a combination of phylogenetic and non-phylogenetic tests showed that PSR increased with host body size across all parasites groups. Counter to expectations, measures of parasite diversity decreased with host longevity and social group size, and associations between group size and PSR further depended on the underlying mating system of the host species. Our results suggest that body mass, longevity, and social organization influence the diversity and types of parasites reported to infect wild populations of hoofed mammals, and that multiple host and parasite traits can combine in unexpected ways to shape observed patterns.     

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.     

Host-parasite coevolution: comparative evidence for covariation of life history traits in primates and oxyurid parasites.

The environmental factors that drive the evolution of parasite life histories are mostly unknown. Given that hosts provide the principal environmental features parasites have to deal with, and given that these features (such as resource availability and immune responses) are well characterized by the life history of the host, we may expect natural selection to result in covariation between parasite and host life histories. Moreover, some parasites show a high degree of host specificity, and cladistic analyses have shown that host and parasite phylogenies can be highly congruent. These considerations suggest that parasite and host life histories may covary. The central argument in the theory of life history evolution concerns the existence of trade-offs between traits. For parasitic nematodes it has been shown that larger body sizes induce higher fecundity, but this is achieved at the expense of delayed maturity. As high adult mortality would select for reduced age at maturity, the selective benefit of increased fecundity is expressed only if adult mortality is low. Parasite adult mortality may depend on a number of factors, including host longevity. Here we tested the hypothesis concerning the positive covariation between parasite body size (which reflects parasite longevity) and host longevity. To achieve this goal, we used the association between the pinworms (Oxyuridae, Nematoda) and their primate hosts. Oxyurids are highly host specific and are supposed to be involved in a coevolutionary process with their hosts. We found that female parasite body length was positively correlated with host longevity after correcting for phylogeny and host body mass. Conversely, male parasite body length and host longevity were not correlated. These results confirm that host longevity may represent a constraint on the evolution of body size in oxyurids, at least in females. The discrepancy between female and male oxyurids is likely to depend on the particular mode of reproduction of this taxon (haplodiploidy), which should result in weak (or even null) selection pressures to an increase of body size in males.     

Does investment into ��expensive�� tissue compromise anti-parasitic defence? Testes size, brain size and parasite diversity in rodent hosts

Species richness of parasite assemblages varies among host species. Earlier studies that searched for host-related determinants of parasite diversity mainly considered host traits that affect the probability of host encounter with parasites, whereas host traits related to defensibility against parasites have rarely been investigated. From the latter perspective, evolutionary investment in ??expensive?? tissue or organs (like testes or brain) may trade off against energetically costly anti-parasitic defences. If so, richer parasite assemblages are expected in hosts with larger testes and brains. We studied the relationships between testes and brain size and diversity of parasites (fleas, gamasid mites and helminths) in 55 rodent species using a comparative approach and application of two methods, namely the method of independent contrasts and generalized least-squares (GLS) analysis. Both phylogenetically correct methods produced similar results for flea and helminth species richness. Testes size positively correlated with flea and helminth species richness but not gamasid mite species richness. No correlation between brain size and species richness of any parasite group was found by the method of independent contrasts. However, GLS analysis indicated negative correlation between brain size and mite species richness. Our results cast doubt on the validity of the expensive tissue hypothesis, but suggest instead that larger testes are associated with higher parasite diversity via their effect on mobility and/or testosterone-mediated immunosuppression.     

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.     

A comparative study of white blood cell counts and disease risk in carnivores

In primates, baseline levels of white blood cell (WBC) counts are related to mating promiscuity. It was hypothesized that differences in the primate immune system reflect pathogen risks from sexually transmitted diseases (STDs). Here, we test for the generality of this result by examining hypotheses involving behavioural, ecological and life-history factors in carnivores. Again, we find a significant correlation in carnivores between mating promiscuity and elevated levels of WBC counts. In addition, we find relationships with measures of sociality, substrate use and life-history parameters. These comparative results across independent taxonomic orders indicate that the evolution of the immune system, as represented by phylogenetic differences in basal levels of blood cell counts, is closely linked to disease risk involved with promiscuous mating and associated variables. We found only limited support for an association between the percentage of meat in the diet and WBC counts, which is consistent with the behavioural and physiological mechanisms that carnivores use to avoid parasite transmission from their prey. We discuss additional comparative questions related to taxonomic differences in disease risk, modes of parasite transmission and implications for conservation biology.     

Correlated evolution between host immunity and parasite life histories in primates and oxyurid parasites

Maturation time is a pivotal life-history trait of parasitic nematodes, determining adult body size, as well as daily and total fecundity. Recent theoretical work has emphasized the influence of prematurational mortality on the optimal values of age and size at maturity in nematodes. Eosinophils are a family of white blood cells often associated with infections by parasitic nematodes. Although the role of eosinophils in nematode resistance is controversial, recent work has suggested that the action of these immune effectors might be limited to the larval stages of the parasite. If eosinophils act on larval survival, one might predict, in line with theoretical models, that nematode species living in hosts with large eosinophil numbers should show reduced age and size at maturity. We tested this prediction using the association between the pinworms (Oxyuridae, Nematoda) and their primate hosts. Pinworms are highly host specific and are expected to be involved in a coevolutionary process with their hosts. We found that the body size of female parasites was negatively correlated with eosinophil concentration, whereas the concentration of two other leucocyte families-neutrophils and lymphocytes-was unrelated to female body size. Egg size of parasites also decreased with host eosinophil concentration, independently of female size. Male body size was unrelated to host immune parameters. Primates with the highest immune defence, therefore, harbour small female pinworms laying small eggs. These results are in agreement with theoretical expectations and suggest that life histories of oxyurid parasites covary with the immune defence of their hosts. Our findings illustrate the potential for host immune defence as a factor driving parasite life-history evolution.     

Patterns of parasite species richness of Western Palaeartic micro-mammals: island effects

We investigate the patterns of parasite species richness of small mammals of the Western Palaearctic, and the effects of insularity. We compiled 28 studies dealing with 16 species of mammals. There was a significant effect of area size on the total parasite species richness, controlling for host sample size. Four mammal species were sufficiently sampled. Two are associated with humans: Mus musculus, and Rattus rattus , and two are not associated with humans, Apodemus sylvaticus and Clethrionomys glaerolus. We show that there is an effect of insularity on parasite species richness of A. sylvaticus . Rodents associated with humans show no effect of insularity on parasite species richness. These rodents appear to reflect a more complex pattern of parasite species richness, probably because of their close association with humans. Host specificity of parasites significantly decreases on islands, with the exception of Rattus rattus . We use parasitological data in order to explore the geographical connections between host populations. We show that parasites may help to resolve these connections but we emphasise that parasites are better geographic than phylogenetic markers.     

Higher parasite richness, abundance and impact in native versus introduced cichlid fishes

Empirical studies suggest that most exotic species have fewer parasite species in their introduced range relative to their native range. However, it is less clear how, ecologically, the loss of parasite species translates into a measurable advantage for invaders relative to native species in the new community. We compared parasitism at three levels (species richness, abundance and impact) for a pair of native and introduced cichlid fishes which compete for resources in the Panama Canal watershed. The introduced Nile tilapia, Oreochromis niloticus, was infected by a single parasite species from its native range, but shared eight native parasite species with the native Vieja maculicauda. Despite acquiring new parasites in its introduced range, O. niloticus had both lower parasite species richness and lower parasite abundance compared with its native competitor. There was also a significant negative association between parasite load (abundance per individual fish) and host condition for the native fish, but no such association for the invader. The effects of parasites on the native fish varied across sites and types of parasites, suggesting that release from parasites may benefit the invader, but that the magnitude of release may depend upon interactions between the host, parasites and the environment.