Detection of interspecific competition in parasite communities

Matrices of correlation coefficients between the abundances or intensities of all pairs of helminth species, across all individual hosts in a sample, are regularly used to detect possible cases of interspecific competition in parasite communities. In these matrices, however, the range of possible values that any correlation coefficient can take is not -1 to 1, contrary to what is generally assumed. The number and magnitude of other correlation coefficients in a matrix will constrain the values that any given correlation can achieve. This property of matrices, and of inter-related natural variables, is explained and illustrated with 2 examples from real helminth communities. As a rule, the presence of many negative correlations in a matrix raises the lower value that any of them can possibly achieve. This has important but previously overlooked implications for the interpretation of correlation coefficients, and the detection of competition in natural parasite communities.     

How parasite interaction strategies alter virulence evolution in multi‐parasite communities

The majority of organisms host multiple parasite species, each of which can interact with hosts and competitors through a diverse range of direct and indirect mechanisms. These within‐host interactions can directly alter the mortality rate of coinfected hosts and alter the evolution of virulence (parasite‐induced host mortality). Yet we still know little about how within‐host interactions affect the evolution of parasite virulence in multi‐parasite communities. Here, we modeled the virulence evolution of two coinfecting parasites in a host population in which parasites interacted through cross immunity, immune suppression, immunopathology, or spite. We show (1) that these within‐host interactions have different effects on virulence evolution when all parasites interact with each other in the same way versus when coinfecting parasites have unique interaction strategies, (2) that these interactions cause the evolution of lower virulence in some hosts, and higher virulence in other hosts, depending on the hosts infection status, and (3) that for cross immunity and spite, whether parasites increase or decrease the evolutionarily stable virulence in coinfected hosts depended on interaction strength. These results improve our understanding of virulence evolution in complex parasite communities, and show that virulence evolution must be understood at the community scale.     

Host densities as determinants of abundance in parasite communities

Several epidemiological models predict a positive relationship between host population density and abundance of directly transmitted macroparasites. Here, we generalize these, and test the prediction by a comparative study. We used data on communities of gastrointestinal strongylid nematodes from 19 mammalian species, representing examination of 6670 individual hosts. We studied both the average abundance of all strongylid nematodes within a host species, and the two components of abundance, prevalence and intensity. The effects of host body weight, diet, fecundity and age at maturity and parasite body size were controlled for directly, and the phylogenetically independent contrast method was used to control for confounding factors more generally. Host population density and average parasite abundance were strongly positively correlated within mammalian taxa, and across all species when the effects of host body weight were controlled for. Controlling for other variables did not change this. Even when looking at single parasite species occurring in several host species, abundance was highest in the host species with the highest population density. Prevalence and intensity showed similar patterns. These patterns provide the first macroecological evidence consistent with the prediction that transmission rates depend on host population density in natural parasite communities.     

Latitudinal gradient in the taxonomic composition of parasite communities

Although latitudinal gradients in diversity have been well studied, latitudinal variation in the taxonomic composition of communities has received less attention. Here, we use a large dataset including 950 surveys of helminth endoparasite communities in 650 species of vertebrate hosts to test for latitudinal changes in the relative contributions of trematodes, cestodes, nematodes and acanthocephalans to parasite assemblages. Although the species richness of helminth communities showed no consistent latitudinal variation, their taxonomic composition varied as a function of both host type and latitude. First, trematodes and acanthocephalans accounted for a higher proportion of species in helminth communities of fish, whereas nematodes achieved a higher proportion of the species in communities of bird and especially mammal hosts. Second, the proportion of trematodes in helminth communities of birds and mammals increased toward higher latitudes. Finally, the proportion of nematodes per community increased toward lower latitudes regardless of the type of host. We present tentative explanations for these patterns, and argue that new insights in parasite community ecology can be gained by searching for latitudinal gradients not only in parasite species richness, but also in the taxonomic composition of parasite assemblages.     

Patterns in metazoan parasite communities of some oyster species

Metazoan parasite communities of Crassostrea gigas and Ostrea edulis from Great Britain, Crassostrea virginica from Mexico, and Saccostrea commercialis from Australia are described and summarized in terms of species composition, species richness, total number of individuals and dominance. Metazoan parasite communities in all host species were composed of turbellarians and the metacercarial stage of digeneans, with the exception of S. commercialis where only metacercariae were found. Arthropods, including one copepod and one mite species, were present only in British oyster species. All metazoan parasite communities of oysters had few species and low density of individuals. Richest communities were found in C. virginica at both component and infracommunity level. The least diverse component community occurred in S. commercialis. Infracommunities in O. edulis and S. commercialis never exceeded one species per host. The host response against parasites is suggested as the principal factor responsible for depauperate parasite communities of oysters. Environmental factors characteristic of tropical latitudes are likely to have enhanced both the number of species and the densities of parasites per host in the infracommunities of C. virginica.     

A new index of interactivity in parasite communities.

A new index of interactivity which allows objective evaluation and comparison of interactivity in communities between different host species is presented. The index is derived from the equations for species-accumulation curves generated using non-linear regression (with the Levenberg-Marquardt algorithm) of sample infracommunity richness data. It is advantageous in that it requires only presence/absence data to calculate, is applicable to all parasite taxa (including asexual species), is largely independent of sample size and allows objective comparison of parasite communities while correcting for differences in total richness. Iterative randomisation of infracommunity richness values to generate a mean value for the index avoids spurious results which may be generated by heterogeneity in infracommunity richness and the variation this produces in the non-linear regression results.     

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.     

Metabarcoding of eukaryotic parasite communities describes diverse parasite assemblages spanning the primate phylogeny

Despite their ubiquity, in most cases little is known about the impact of eukaryotic parasites on their mammalian hosts. Comparative approaches provide a powerful method to investigate the impact of parasites on host ecology and evolution, though two issues are critical for such efforts: controlling for variation in methods of identifying parasites and incorporating heterogeneity in sampling effort across host species. To address these issues, there is a need for standardized methods to catalogue eukaryotic parasite diversity across broad phylogenetic host ranges. We demonstrate the feasibility of a metabarcoding approach for describing parasite communities by analysing faecal samples from 11 nonhuman primate species representing divergent lineages of the primate phylogeny and the full range of sampling effort (i.e. from no parasites reported in the literature to the best‐studied primates). We detected a number of parasite families and regardless of prior sampling effort, metabarcoding of only ten faecal samples identified parasite families previously undescribed in each host (x? = 8.5 new families per species). We found more overlap between parasite families detected with metabarcoding and published literature when more research effort—measured as the number of publications—had been conducted on the host species' parasites. More closely related primates and those from the same continent had more similar parasite communities, highlighting the biological relevance of sampling even a small number of hosts. Collectively, results demonstrate that metabarcoding methods are sensitive and powerful enough to standardize studies of eukaryotic parasite communities across host species, providing essential new tools for macroecological studies of parasitism.     

Temporal stability of insular avian malarial parasite communities

Avian malaria is caused by a diverse community of genetically differentiated parasites of the genera Plasmodium and Haemoproteus. Rapid seasonal and annual antigenic allele turnover resulting from selection by host immune systems, as observed in some parasite populations infecting humans, may extend analogously to dynamic species compositions within communities of avian malarial parasites. To address this issue, we examined the stability of avian malarial parasite lineages across multiple time-scales within two insular host communities. Parasite communities in Puerto Rico and St Lucia included 20 and 14 genetically distinct parasite lineages, respectively. Lineage composition of the parasite community in Puerto Rico did not vary seasonally or over a 1 year interval. However, over intervals approaching a decade, the avian communities of both islands experienced an apparent loss or gain of one malarial parasite lineage, indicating the potential for relatively frequent lineage turnover. Patterns of temporal variation of parasite lineages in this study suggest periodic colonization and extinction events driven by a combination of host-specific immune responses, competition between lineages and drift. However, the occasional and ecologically dynamic lineage turnover exhibited by insular avian parasite communities is not as rapid as antigenic allele turnover within populations of human malaria.     

Microbial communities are indicators of parasite infection status

Growing evidence suggests that microbiomes have been shaping the evolutionary pathways of macroorganisms for millennia and that these tiny symbionts can influence, and possibly even control, species interactions like host–parasite relationships. Yet, while studies have investigated host–parasites and microbiomes separately, little has been done to understand all three groups synergistically. Here, we collected infected and uninfected Eurypanopeus depressus crab hosts from a coastal North Carolina oyster reef three times over 4 months. Infected crabs demonstrated an external stage of the rhizocephalan parasite, Loxothylacus panopaei. Community analyses revealed that microbial richness and diversity were significantly different among tissue types (uninfected crab, infected crab, parasite externae and parasite larvae) and over time (summer and fall). Specifically, the microbial communities from parasite externae and larvae had similar microbiomes that were consistent through time. Infected crabs demonstrated microbial communities spanning those of their host and parasite, while uninfected crabs showed more distinctive communities with greater variability over time. Microbial communities were also found to be indicators of early-stage infections. Resolving the microbial community composition of a host and its parasite is an important step in understanding the microbiome's role in the host–parasite relationship and determining how this tripartite relationship impacts coevolutionary processes.     

Defining parasite communities is a challenge for neutral theory

The neutral theory of biodiversity and biogeography is a null model of community structure that suggests that it may be possible to explain the richness and relative abundance of species through neutral processes of immigration, extinction, and speciation, without resort to interactive processes such as competition. There have been no attempts to fit neutral models to parasite communities to date. The nature of parasite communities, however, challenges the basic assumptions of neutral theory. In particular, the spatially dynamic relationships between hosts as habitat patches result in immigration rates that are in a constant state of flux. In addition, the partial compositional overlap of many component communities means that they can affect each other's process rates, which violates the zero-sum assumptions of neutral theory. Despite these obstacles, many of the patterns that neutral theory seeks to explain are still present in parasite communities. Far from being an esoteric special case, parasite communities are ubiquitous in nature and, therefore, any attempts to produce unified theoretical frameworks should accommodate the characteristics of parasite communities, or risk obsolescence.     

Testing for deterministic succession in metazoan parasite communities of marine fish

Parasite communities are similar to free‐living communities; decay of similarity over geographic distance, theory of island biogeography, species–area relationships and nestedness have been documented in both communities. Ecological succession has been studied in free‐living communities but has rarely been examined in parasite communities. We use seriation with replication to test the hypothesis that succession of parasite community structure is deterministic, thus developing throughout consecutive changes along the fish ontogeny, via a seriated pattern. 12 306 marine fishes (95 species) were studied. In 40 species, a seriated pattern was detected; 25 had a tendency towards a seriated pattern, and for 31 species, succession was at random. Age‐classes for each host species explained deterministic successional patterns for whole parasite communities and ectoparasites. Richness and number of age‐classes explained this pattern for endoparasites. Seriated successional pattern was evident for parasite communities of long‐lived marine fish, indicating that parasite communities follow sequential changes over time, like many free‐living communities.     

The relationship between species richness and productivity in metazoan parasite communities

Biodiversity is not distributed homogeneously in space, and it often covaries with productivity. The shape of the relationship between diversity and productivity, however, varies from a monotonic linear increase to a hump-shaped curve with maximum diversity values corresponding to intermediate productivity. The system studied and the spatial scale of study may affect this relationship. Parasite communities are useful models to test the productivity-diversity relationship because they consist of species belonging to a restricted set of higher taxa common to all host species. Using total parasite biovolume per host individual as a surrogate for community productivity, we tested the relationship between productivity and species richness among assemblages of metazoan parasites in 131 vertebrate host species. Across all host species, we found a linear relationship between total parasite biovolume and parasite species richness, with no trace of a hump-shaped curve. This result remained after corrections for the potential confounding effect of the number of host individuals examined per host species, host body mass, and phylogenetic relationships among host species. Although weaker, the linear relationship remained when the analyses were performed within the five vertebrate groups (fish, amphibians, reptiles, mammals and birds) instead of across all host species. These findings agree with the classic isolationist-interactive continuum of parasite communities that has become widely accepted in parasite ecology. They also suggest that parasite communities are not saturated with species, and that the addition of new species will result in increased total parasite biovolume per host. If the number of parasite species exploiting a host population is not regulated by processes arising from within the parasite community, external factors such as host characteristics may be the main determinants of parasite diversity.     

Relating parasite communities to host environmental conditions using phylogenetic tools

There are many tools available for analysing parasite communities, either based on the proportions or presence/absence of species. These analyses rely on phylogenetic distances, and analyses of actual characters (e.g. species). The phylogenetic analysis (Wanger parsimony) was compared to a cluster analysis (UPGMA) and correspondence analyses of two real helminth communities in sheep (one farm and with repeated sampling along time) or goats (several farms, each sampled once). The cladograms obtained using Wagner parsimony provided a clearer structuring of the helminth communities than classical analyses. The homogeneous groups of parasite communities on goat farms were significantly related (Fisher' exact test) to the environmental characteristics. The evolution along time pattern of change in the sheep infection of sheep was not the same for in all the animals, and two groups of communities could be distinguished in the last lamb cohorts. Phylogenetic analyses provide an effective performing tool to for interpreting the change in evolution of helminth communities with environmental conditions.     

Taxonomic partitioning shedding light on the diversification of parasite communities

Power relations were used for 297 parasite communities of fish, bird and mammal hosts between the number of genera (G) and the number of species (S) per community to test for the relative importance of different processes in their diversification. For the bird hosts the relation was G∝S^0.92, and for fish hosts it was G∝S^0.97, but for mammal hosts, the number of parasite genera increases more slowly as a function of species richness (G∝S^0.83), suggesting, among other possibilities, a higher rate of within-host parasite speciation in mammals than in other vertebrates.     

Compositional turnover in host and parasite communities does not change network structure

Decreasing similarity between ecological communities with increasing geographic distance (i.e. distance‐decay) is a common biogeographical observation in free‐living communities, and a slightly less common observation for parasite communities. Ecological networks of interacting species may adhere to a similar pattern of decreasing interaction similarity with increasing geographic distance, especially if species interactions are maintained across space. We extend this further, examining if host–parasite networks – independent of host and parasite species identities – become more structurally dissimilar with increasing geographic distance. Utilizing a global database of helminth parasite occurrence records, we find evidence for distance‐decay relationships in host and parasite communities at both regional and global scales, but fail to detect similar relationships in network structural similarity. Host and parasite community similarity were strongly related, and both decayed rapidly with increasing geographic distance, typically resulting in complete dissimilarity after approximately 2500 km. Our failure to detect a decay in network structural similarity suggests the possibility that different host and parasite species are filling the same functional roles in interaction networks, or that variation in network similarity may be better explained by other geographic variables or aspects of host and parasite ecology.     

Fish parasite communities in tropical reservoirs along the Perak River, Malaysia

The parasite communities of fish in three reservoirs (Temengor, Kenering and Cenderuh) along the Perak River, as well as in the lower Perak, are compared. A total of 36 species, 51 species, 61 species and 58 species of metazoan parasites from six types of fishes common in all studied locations, were obtained in Temengor, Kenering, Cenderuh Reservoirs, and downstream Perak River, respectively. The various criteria (prevalence, mean intensity, diversity index, similarity index and evenness) of the parasite community were highest at the Cenderuh Reservoir, followed by the downstream river, Kenering, and Temengor Reservoirs. Monogeneans were the most common parasites in all species of fish examined from all study sites. Fish of the same species showed a high degree of similarity of its parasite fauna regardless of study site, but different hosts had a low similarity of their parasite fauna, even within the same study site. This revised version was published online in August 2006 with corrections to the Cover Date.