Richness,nestedness, and randomness in parasite infracommunity structure

Within a host population, parasite infracommunities vary in both richness and species composition. If interspecific interactions among parasites are important in shaping infracommunities, the structure of these assemblages is expected to differ from the one predicted by null models, i.e. from the one that would result from chance alone. Using data from the literature, I tested for discrepancies between observed and random patterns in the richness and composition of gastrointestinal helminth infracommunities of birds and mammals. Both the Poisson distribution and a more sophisticated null model, derived from prevalence of the different parasite species in the host population, usually provided a good fit to the observed distributions of infracommunity richness among hosts. This suggests that parasite species do not co-occur more or less frequently than expected by chance. In mammals, the co-occurrence of all available parasite species in the same host individual, or maximum potential infracommunity richness, was less likely to be observed when several parasite species were available; this is also a phenomenon expected from the random assembly of parasite species. Finally, there was no evidence for a nested subset pattern among parasite species in a host population: rate species were distributed independently of common ones. The overall picture emerging from these results is one in which parasite assemblages are more likely to be the product of random events than of predictable and repeatable processes.     

Metazoan parasite infracommunities of Florida pompano (Trachinotus carolinus) from the coast of the Yucatan Peninsula,Mexico

Metazoan parasite infracommunities of the Florida pompano (Trachinotus carolinus) were studied in terms of species composition, species richness, diversity, numerical dominance, and similarity. Seventy-five fishes were collected from 4 localities along the Yucatan Peninsula coast and 24 parasite species recovered. Most were digeneans (8 species) and nematodes (7). Other species were monogeneans (3). aspidogastreans (2), cestodes (1), acanthocephalans (1), and crustaceans (2). Only 4 species were common in at least I locality. Mean values for species richness, abundance, diversity, numerical dominance, and similarity in total (all species in the individual fish), gastrointestinal, and ectoparasite infracommunities were within ranges observed for most helminth infracommunities of marine fishes from temperate and tropical latitudes. These infracommunities had low species richness, abundance, diversity, and predictability (except ectoparasite infracommunities) and high dominance. Within the predictable element (common species), the specialist monogenean Pseudobicotylophora atlantica was the main reason for the increase in predictability because it was the only common species at all 4 localities. Host feeding habits, the distribution of intermediate hosts and infective stages, the local species pool, and a phylogenetic component seem to be determining the characteristics of these metazoan parasite infracommunities.     

Host patch traits have scale-dependent effects on diversity in a stickleback parasite metacommunity

Many metacommunities are distributed across habitat patches that are themselves aggregated into groups. Perhaps the clearest example of this nested metacommunity structure comes from multi-species parasite assemblages, which occupy individual hosts that are aggregated into host populations. At both spatial scales, we expect parasite community diversity in a given patch (either individual host or population) to depend on patch characteristics that affect colonization rates and species sorting. But, are these patch effects consistent across spatial scales? Or, do different processes govern the distribution of parasite community diversity among individual hosts, versus among host patches? To answer these questions, we document the distribution of parasite richness among host individuals and among populations in a metapopulation of threespine stickleback Gasterosteus aculeatus. We find some host traits (host size, gape width) are associated with increased parasite richness at both spatial scales. Other patch characteristics affect parasite richness only among individuals (sex), or among populations (lake size, lake area, elevation and population mean heterozygosity). These results demonstrate that some rules governing parasite richness in this metacommunity are shared across scales, while others are scale-specific.     

Richness, structure and functioning in metazoan parasite communities

Ecosystem functioning, characterized by components such as productivity and stability, has been extensively linked with diversity in recent years, mainly in plant ecology. The aim of our study was thus to quantify general relationships between diversity, community structure and ecosystem functions in metazoan parasite communities. We used data on parasite communities from 15 species of marine fish hosts from coastal Chile. The volumetric abundance (volume of all parasite species per individual host, in mm³) was used as a surrogate for productivity. Species diversity was measured using both species richness and evenness, while community structure was estimated using the co‐occurrence indices V‐ratio, C‐score and a new C‐score_s index standardized for the number of host replicates. After correcting for fish size, 47% of host species show no relationship, 13% show a hump shaped curve and 40% show positive monotonic relationships between productivity and parasite richness across all host individuals in a sample. We obtained a logarithmically decreasing relationship between evenness and productivity for all fish species, and propose a ‘dominance‐resistance’ hypothesis based on immunity to explain this pattern. The stability of the parasite community, measured as the coefficient of variation in productivity among individual hosts, was strongly and positively related to mean species richness across the 15 host species. The C‐score_s index, based on the number of checkerboard units in the host‐parasite presence/absence matrix, increases linearly with mean productivity across the 15 host species, suggesting that parasite communities tend to be more structured when they are more productive. This is the likely reason why linear relationships between richness and productivity were not observed consistently in all fish species. Parasite communities provide some clear patterns for the diversity–ecosystem functioning debate in ecology, although other factors, such as the history of community assembly, may also influence these patterns.     

Ecological determinants of parasite acquisition by exotic fish species

Disease‐mediated threats posed by exotic species to native counterparts are not limited to introduced parasites alone, since exotic hosts frequently acquire native parasites with possible consequences for infection patterns in native hosts. Several biological and geographical factors are thought to explain both the richness of parasites in native hosts, and the invasion success of free‐living exotic species. However, the determinants of native parasite acquisition by exotic hosts remain unknown. Here, we investigated native parasite communities of exotic freshwater fish to determine which traits influence acquisition of native parasites by exotic hosts. Model selection suggested that five factors (total body length, time since introduction, phylogenetic relatedness to the native fish fauna, trophic level and native fish species richness) may be linked to native parasite acquisition by exotic fish, but 95% confidence intervals of coefficient estimates indicated these explained little of the variance in parasite richness. Based on R²‐values, weak positive relationships may exist only between the number of parasites acquired and either host size or time since introduction. Whilst our results suggest that factors influencing parasite richness in native host communities may be less important for exotic species, it seems that analyses of general ecological factors currently fail to adequately incorporate the physiological and immunological complexity of whether a given animal species will become a host for a new parasite.     

Ecology of a diplozoon parasite on the gills of the African cyprinid Barbus neumayeri

In oxygen‐deficient waters, the difficulties of oxygen uptake in gill parasites and their fish hosts may influence host and parasite densities, site selection by the parasite, and effects of the parasite on host condition. This study quantified the prevalence and intensity of the gill monogenean Neodiplozoon polycotyleus in the African cyprinid fish Barbus neumayeri from an intermittent forest stream in western Uganda. Oxygen levels were low in the stream over the 12‐month study, averaging only 2.5 mg litre^?1 (monthly range = 1.2–4.3 mg litre^?1). However, parasite prevalence was high (47.2%), suggesting high tolerance to low oxygen in N. polycotyleus. The prevalence of parasites varied with host body size, with the highest frequency of occurrence in the middle size classes. Prevalence also varied over the year; seasonal peaks of rainfall coincided with a lower frequency of N. polycotyleus. The significantly nonrandom frequency distribution of parasites among hosts suggests regulation of parasite numbers. Of the hosts infected, 37.1% harboured one N. polycotyleus parasite, and 62.9% harboured two parasites. No fish were infected with more than two diplozoons. There was evidence for strong site specificity by N. polycotyleus within hosts; 77.7% of the parasites were located on the filaments of the second gill arch, which may relate to increased oxygen availability. In addition, only one of the 178 infected fish had more than one parasite on one side of the branchial basket. Although N. polycotyleus is undoubtedly parasitic, we found no evidence of a negative parasitic effect on the condition or reproductive status of B. neumayeri.     

Can host body size explain the parasite species richness in tropical freshwater fishes?

Summary The variability of monogenean gill ectoparasite species richness in 19 West African cyprinid species was analyzed using the following seven predictor variables: host size, number of drainage basins, number of sympatric cyprinid species, host diversity, association with mainland forest, host ecology, and monogenean biological labelling. The size of the host species accounted for 77% of the variation in the number of parasite species per host, and host ecology an additional 8%. Together the effects of host size and host ecology accounted for 85% of the variation in monogenean species richness. This study shows that the deciding factors for explaining monogenean species richness in West African cyprinid fishes are host species size and host ecology. These results were compared with main factors responsible for parasite species richness in fish communities. Other possible explanations of monogenean community structure in west African cyprinids are discussed.     

Determinants of parasite species richness on small taxonomical and geographical scales: Lamellodiscus monogeneans of northwestern Mediterranean sparid fish

Determinants of parasite species richness have been investigated in a host-parasite system comprising fish of the family Sparidae and their monogenean gill ectoparasites of the genus Lamellodiscus. This study was carried out on a small geographical scale in the northwestern Mediterranean Sea. Host phylogenetic relationships were taken into account by phylogenetic eigenvector regression which required the reconstruction of a phylogenetic tree for the sparid fish species using mtDNA sequences. Several ecological variables potentially acting on Lamellodiscus species richness were considered. Host body size and host migratory behaviour appeared to be the main determinants of parasite species richness in this system. It is concluded that structuring of monogenean communities is controlled more by ecological than evolutionary factors.     

Spatial and temporal predictability of the parasite community structure of a benthic marine fish along its distributional range

The search for consistent patterns of organisation in parasite communities remains a central theme in parasite community ecology. However, to date, much evidence comes from studies without replication in both space and time; when replicate communities are examined, repeatable patterns are rarely observed. Here we determine, using nested subset analyses, whether the infracommunities of ectoparasites and endoparasites of a benthic marine fish (Sebastes capensis) show non-random structure. Then we examine the spatial repeatability of parasite community structure across the host's distribution in the southern Pacific, and the temporal repeatability of ectoparasite community structure from one locality. In total, 537 fish were captured from different latitudes (between 11 degrees S and 52 degrees S) along the Pacific coast of South America; a further 122 specimens were captured in two other years from one of the sampling localities, Valdivia (40 degrees S). In spite of variation in fish sizes among samples, fish size generally did not correlate with either ecto- or endoparasite species richness. The ecto- and endoparasite species richness of the component communities were also not correlated with fish sample size across the nine localities. Significant nested patterns were found in the ectoparasite communities of S. capensis at all eight localities, except at latitude 52 degrees S. Significant nested patterns were also found in the endoparasite infracommunities of S. capensis at seven of the nine localities, the exceptions being those from latitudes 11 degrees S and 20 degrees S. On a temporal scale, significant nestedness was observed in the ectoparasite infracommunities of S. capensis during each of the 3 years of sampling at Valdivia. In general, the same parasite species are responsible for the repeatability of nested patterns, though their importance varies among localities. The spatial and temporal predictability of the parasite community structure in S. capensis may be associated with the fish's benthic habitat and territorial behavior, suggesting that host biology may be a key determinant of the structure of parasite communities.     

Parasite community structure within and across host populations of a marine pelagic fish: how repeatable is it?

The geographical variation in parasite community structure among populations of the same host species remains one of the least understood aspects of parasite community ecology. Why are parasite communities clearly structured in some host populations, and randomly assembled in others? Here, we address this fundamental question using data on the metazoan parasite communities of different host size-classes of four distinct populations of a small pelagic fish, the Argentine anchovy, Engraulis anchoita, from the South West Atlantic. Within each fish sample, fish length was correlated with both the total intensity of parasites and species richness among infracommunities. More importantly, average fish length correlated with mean infracommunity richness and mean total intensity across the fish samples, indicating that the characteristics of parasite assemblages in a fish population are strongly influenced by the size of its fish in relation to those in other populations. Nested subset patterns were observed in about half of the fish samples. This means that the presence or absence of parasite species among fish individuals is often not random; however, no repeatability of nestedness among component communities was observed. Average fish length did not influence directly the likelihood that a parasite assemblage was significantly nested. However, variables influenced by average fish length, namely mean infracommunity richness and mean total intensity, determine the probability that a nested hierarchy will be observed; host size may thus indirectly affect parasite community structure either itself or via its influence on host movement and feeding patterns. To some extent, this apparent link may be due to the sensitivity of nestedness analyses to the proportion of presence in a presence/absence matrix; this in itself is a biological feature of the parasite community, however, which is associated with mean host length.     

Helminth parasite diversity discloses age and sex differences in the foraging behaviour of southern lapwings (Vanellus chilensis)

Parasites with heteroxen cycles are important sources of information on the trophic relations of hosts. This is particularly instructive for species whose age‐based or sex‐based differences are hardly detected by behavioural observations. Here, we describe the helminth community of the omnivorous southern lapwing (Vanellus chilensis) and evaluate whether it is affected by the host's sex, age and body size. The species is sexually monomorphic in body length, but males are slightly heavier than females. We analysed 112 individuals collected in Curitiba, Brazil, in March 2010. All hosts were parasitized. The helminth community was composed of 10 species (the digeneans Leucochloridium parcum and Athesmia sp., the cestode Infula macrophallus, the acantocephalans Plagiorhynchus sp., Centrorhynchus sp., Mediorhynchus sp., and an unidentified Gigantorhynchida, and the nematodes Heterakis psophiae, Dispharynx nasuta and an unidentified Capillariidae), seven of which were novel reports for this host species. Prevalence ranged from <1% to 99%. Whereas I. macrophallus was the most prevalent species, D. nasuta showed the highest mean intensity and abundance of infection. The former was found in most hosts as single male–female pairs, suggesting the occurrence of intrasexual competition. The infracommunities of juvenile birds showed a higher parasite species richness than those of adult males and females, suggesting the exploitation of a wider array of prey. However, the three classes harboured seven parasite species. Differences in parasite diversity (lower in juveniles, intermediate in adult males and higher in adult females) reflect the evenness in the distribution of parasite specimens among taxa in each age–sex class and are compatible with differences in their foraging strategy. Finally, we conclude based on the cycles of the heteroxen species that southern lapwings preyed upon molluscs, coleopterans, woodlice and earthworms.     

Group-living and the richness of the parasite fauna in Canadian freshwater fishes

Summary An increased transmission of ectoparasites among individual animals is considered to be an inevitable cost of living in groups, since several kinds of ectoparasites require close proximity between large numbers of hosts for successful transmission. However, we do not know whether individuals belonging to group-living species incur a greater risk of ectoparasitism than individuals of solitary species. Here, using published data from 3 families (60 species) of Canadian freshwater fishes, I test the hypothesis that group-living species are host to more species of contagious ectoparasites (copepods and monogeneans) than solitary host species. As the different fish species have been studied with varying intensity, I used the mean number of parasite species recorded per study as a standard measure of parasite numbers. Multiple regression analyses were performed separately for each family to determine the effects of group-living and of 3 other variables (host size, age, and range) on the richness of the recorded parasite fauna. Once the effects of the other variables were removed, I found no significant effect of sociality on the richness of the parasite fauna per fish species, for contagious ectoparasites and other types of parasites. Neither of the other variables had any influence on the numbers of parasite species per fish species. These results suggest that a richer ectoparasite fauna is not a cost of group-living in fishes.     

Species accumulation curves and their applications in parasite ecology

Species accumulation curves (SACs) chart the increase in recovery of new species as a function of some measure of sampling effort. Studies of parasite diversity can benefit from the application of SACs, both as empirical tools to guide sampling efforts and predict richness, and because their properties are informative about community patterns and the structure of parasite diversity. SACs can be used to infer interactivity in parasite infracommunities, to partition species richness into contributions from different spatial scales and different levels of the host hierarchy (individuals, populations and communities) or to identify modes of community assembly (niche versus dispersal). A historical tendency to treat individual hosts as statistically equivalent replicates (quadrats) seemingly satisfies the sample-based subgroup of SACs but care is required in this because of the inequality of hosts as sampling units. Knowledge of the true distribution of parasite richness over multiple host-derived and spatial scales is far from complete but SACs can improve the understanding of diversity patterns in parasite assemblages.     

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.     

Use of fish parasite species richness indices in analyzing anthropogenically impacted coastal marine ecosystems

The diversity of fish parasite life history strategies makes these species sensitive bioindicators of aquatic ecosystem health. While monoxenous (single-host) species may persist in highly perturbed, extreme environments, this is not necessarily true for heteroxenous (multiple-host) species. As many parasites possess complex life cycles and are transmitted through a chain of host species, their dependency on the latter to complete their life cycles renders them sensitive to perturbed environments. In the present study, parasite communities of grey mullet Liza aurata and Liza ramada (Mugilidae) were investigated at two Mediterranean coastal sites in northern Israel: the highly polluted Kishon Harbor (KH) and the relatively unspoiled reference site, Ma'agan Michael (MM). Both are estuarine sites in which grey mullet are one of the most common fish species. The results indicate that fish at the polluted site had significantly less trematode metacercariae than fish at the reference site. Heteroxenous gut helminths were completely absent at the polluted sampling site. Consequently, KH fish displayed lower mean parasite species richness. At the same time, KH fish mean monoxenous parasite richness was higher, although the prevalence of different monoxenous taxa was variable. Copepods had an increased prevalence while monogenean prevalence was significantly reduced at the polluted site. This variability may be attributed to the differential susceptibility of the parasites to the toxicity of different pollutants, their concentration, the exposure time and possible synergistic effects. In this study, we used the cumulative species curve model that extrapolates "true" species richness of a given habitat as a function of increasing sample size. We considered the heteroxenous and monoxenous species separately for each site, and comparison of curves yielded significant results. It is proposed to employ this approach, originally developed for estimating the "true" parasite species richness for a given habitat, in the characterization of communities of differentially impacted coastal marine ecosystems. Communicated by H. von Westernhagen, A. Diamant     

Helminth parasite richness among vertebrates

The numbers of intestinal helminth species (parasite richnesS) recorded from each of 488 vertebrate host species are compared using data compiled from the published literature. Associations between parasite richness, sampling effort, host size and host habitat (aquatic versus terrestrial) are assessed using a method designed to control for phylogenetic association. Parasite richness increases with the number of surveys on which each estimate of parasite richness is based (sampling effort). When the effects of sampling effort are controlled for, there remains a strong positive relationship between parasite richness and host body size. There is no tendency for aquatic hosts to harbour more parasite species than terrestrial hosts independently of differences in sampling effort and body size. The results are interpreted in the context of hosts representing habitats for parasite colonization, resource allocation between parasite species, and the age of the major mammalian radiations.     

Native and invasive hosts play different roles in host–parasite networks

Parasites are often key players in biological invasions since they can mediate the impact of host invasions or can themselves become invasive species. However, the nature and extent of parasite-mediated invasions are often difficult to delineate. Here, we used individual-based, weighted bipartite networks to study the roles (degrees of interactions of individuals in a modular network according to their within- and among-module connections) played by native and invasive host individuals to their parasite communities. We studied two phylogenetically and ecologically close fish species, Mugil cephalus s.l. and Planiliza haematocheilus (Teleostei: Mugilidae). Planiliza haematocheilus is native to the Sea of Japan and invasive in the Sea of Azov whereas, M. cephalus s.l. is native to both seas. Based on the common evolutionary history that drives native host–parasite networks, we hypothesised that 1) native networks have higher modularity than invaded ones; and 2) invasive hosts in the invaded area play a peripheral role to structure parasite communities. We analysed the whole parasite community and subsets based on transmission strategy and host specificity of the parasite species to establish whether modularity and host roles are related to these features in the native and invaded areas. All networks were found to be modular. However, modularity tended to be higher in networks of the native area rather than those of the invaded area. Host individuals of both fish species played similar roles in the native area, whereas invasive hosts played a peripheral role in the networks of the invaded area. We propose that long-term monitoring of the roles of invasive hosts in parasite communities can be a useful proxy for estimating the maturity of the establishment of the invasive hosts in an ecosystem.     

Overwinter body condition,mortality and parasite infection in two size classes of 0+ year juvenile European bitterling Rhodeus amarus

Body condition and parasite abundance were examined in two size classes of European bitterling Rhodeus amarus during the first overwintering period in two seasons (2007–2008 and 2009–2010). Body condition of large fish did not change during winter, and increased significantly in March. From November to February, small fish showed a decreasing trend in condition. Despite a significant increase in March condition of small fish only reached the same level as before winter. Total parasite abundance increased significantly in winter in both fish size classes, reflecting a seasonal increase in monogenean infection. Large fish were parasitized significantly more than small fish during winter, but only in small fish was a negative correlation between parasite infection and condition found and a significant decrease in parasite abundance recorded after wintering, indicating mortality of heavily infected individuals with low condition during the winter. A trend for higher overwinter mortality in small fish was found under semi‐experimental conditions. The decrease in condition during the winter period in small fish may reflect faster energy depletion generally expected in smaller individuals. The results indicate that parasite infection may contribute to the overwinter mortality of 0+ year R. amarus, with a stronger effect in smaller individuals.     

Infracommunity structure of parasites of Hemigymnus melapterus (Pisces: Labridae) from Lizard Island, Australia: the importance of habitat and parasite body size

This study describes the community of all metazoan parasites from 14 individuals of thicklip wrasse, Hemigymnus melapterus, from Lizard Island, Australia. All fish were parasitized, and 4,649 parasite individuals were found. Twenty-six parasite species were identified although only 6 species were abundant and prevalent: gnathiid isopods, the copepod Hatschekia hemigymni, the digenean Callohelmis pichelinae, and 3 morphotypes of tetraphyllidean cestode larvae. We analyzed whether the body size and microhabitat of the parasites and size of the host affected understanding of the structure of the parasite community. We related the abundance, biovolume, and density of parasites with the host body size and analyzed the abundances and volumetric densities of some parasite species within microhabitats. Although the 2 most abundant species comprised 75% of all parasite individuals, 4 species, each in similar proportion, comprised 85% of the total biovolume. Although larger host individuals had higher richness, abundance, and biovolume of parasites than smaller individuals, overall parasite volumetric density actually decreased with the host body size. Moreover, parasites exhibited abundances and densities significantly different among microhabitats; some parasite species depended on the area available, whereas others selected a specific microhabitat. Parasite and habitat size exhibited interesting relationships that should be considered more frequently. Considerations of these parameters improve understanding of parasite community structure and how the parasites use their habitats.