The Evolution of Taxonomic Diversity in Helminth Assemblages of Mammalian Hosts

Several studies have searched for the key forces behind the diversification of parasite assemblages over evolutionary time. All of these studies have used parasite species richness as their measure of diversity, thus ignoring the relatedness among parasite species and the taxonomic structure of the assemblages. This information is essential, however, if we want to elucidate which processes have caused an assemblage of parasites to acquire new species. Here, we performed a comparative analysis across 110 species of mammalian hosts in which we evaluated the effects of four host traits (body mass, population density, geographic range, and basal metabolic rate) on the diversity of their assemblages of helminth endoparasites. As measures of diversity, we used parasite species richness, as well as the average taxonomic distinctness of the assemblage and its variance; the latter measures are based on the taxonomic distance between two parasite species, computed across all possible species pairs in an assemblage. Unlike parasite species richness, both the average taxonomic distinctness and its variance were unaffected by the number of hosts examined. These two measures of parasite diversity also proved highly repeatable among host populations of the same mammalian species; in contrast, parasite species richness was unreliable as a species character, as it varied as much within a host species than among different host species. Using phylogenetically independent contrasts, and correcting for potential confounding variables, we found that host population density correlated positively with parasite species richness. There were, however, no other relationships between any of the four host traits investigated and either of our measures of parasite diversity. The processes facilitating the taxonomic diversification of parasite assemblages thus remain unclear, but their elucidation will be necessary if we are to fully understand parasite evolution.     

Community ecology of the metazoan parasites of namorado sandperches, Pseudopercis numida Miranda-Ribeiro, 1903 and P. semifasciata Cuvier, 1829 (Perciformes: Pinguipedidae), from the coastal zone of the State of Rio de Janeiro, Brazil

One hundred and twenty-eight specimens of namorado sandperches, 62 P. numida and 66 P. semifasciata, collected between October 2002 and June 2003 off the Cabo Frio, Rio de Janeiro, Brazil (Lat 23 degrees S and Long 42 degrees W), were examined to study their metazoan parasites. Parasite communities of these fish were composed basically of endoparasites, mainly digenean and cestodes species, with low prevalence and abundance but having high parasite species richness values (at the component community level). Among these values, that found for P. numida is the highest so far recorded for marine fishes from the Neotropical Region. Thirty-nine species of metazoan parasites were collected: 36 from P. numida and 28 from P. semifasciata. Twenty-five parasite species were common to both species of namorado sandperches. Pseudopercis numida and P. semifasciata are new host records for all parasite species collected, with the exception of Microcotyle pseudopercis. Choanodera sp., Leurodera decora, Neolebouria georgenascimentoi, and Proctoeces sp. which were recorded for the first time in the South American Atlantic Ocean. Gnathia sp. from P. numida and Scolex pleuronectis from P. semifasciata were the species having the greatest dominance frequency. Parasite abundance in P. numida and P. semifasciata were positively correlated with the host total length. Only in P. numida was parasite species richness correlated positively with the host total length. No significant differences between endoparasite infracommunities of P. numida and P. semifasciata were detected. The ectoparasites of P. numida had higher values for parasite abundance, parasite richness, Brillouin index, evenness index, and Berger-Parker index than those of the ectoparasites of P. semifasciata. Comparisons among all ecto- and endoparasites showed the ectoparasites of P. numida as the most heterogeneous group. Low similarity values were observed among the three types of parasite infracommunities of the two hosts.     

Community ecology of metazoan parasites of the anchovy Anchoa tricolor (Osteichthyes: Engraulidae) from the coastal zone of the State of Rio de Janeiro, Brazil.

Between October 2001 and March 2002, 103 specimens of A. tricolor from Angra dos Reis (23 degrees 01' S, 44 degrees 19' W), in the coastal zone of the State of Rio de Janeiro, Brazil, were analyzed in order to study their metazoan parasite infracommunities. Ten species of metazoan parasites were collected: 4 digeneans, 1 cestode, 1 acantocephalan, 2 nematodes, 1 copepod, and 1 hirudinean; 77.7% of the fishes were parasitized by one or more metazoan, with a mean of 3.5 +/- 6.2 parasite/fish. Digenean was the most dominant with 4 species that accounted for 53.2% of the total parasites collected; Ergasilus sp. was the most abundant species. Abundance and prevalence of Parahemiurus merus (Linton, 1910) were positively correlated with the total length of host. Relationships between total body length of fish and both total parasite abundance and mean parasite species richness were observed. Mean parasite diversity of species was correlated to host's total length, with significant differences found between male and female fishes. Two pairs of larval species showed significant positive association and covariation. The metazoan parasite infracommunities of A. tricolor presented dominance of larval endoparasites; correlation of parasite abundance, diversity, and species richness with host total length; and low number of parasite interspecific relationships. The parasite community of A. tricolor showed some similarities with the parasite community of another South American Atlantic engraulid.     

Structure of the parasite communities of a coral reef fish assemblage (Labridae): testing ecological and phylogenetic host factors

The role of ecological and phylogenetic processes is fundamental to understanding how parasite communities are structured. However, for coral reef fishes, such information is almost nonexistent. In this study, we analyzed the structure of the parasite communities based on composition, richness, abundance, and biovolume of ecto- and endoparasites of 14 wrasse species (Labridae) from Lizard Island, Great Barrier Reef, Australia. We determine whether the structure of the parasite communities from these fishes was related to ecological characteristics (body size, abundance, swimming ability, and diet) and/or the phylogenetic relatedness of the hosts. We examined 264 fishes from which almost 37,000 individual parasites and 98 parasite categories (types and species) were recorded. Gnathiid and cestode larvae were the most prevalent and abundant parasites in most fishes. Mean richness, abundance, and biovolume of ectoparasites per fish species were positively correlated with host body size only after controlling for the host phylogeny, whereas no such correlation was found for endoparasites with any host variable. Because most ectoparasites have direct transmission, one possible explanation for this pattern is that increased space (host body size) may increase the colonization and recruitment of ectoparasites. However, endoparasites generally have indirect transmission that can be affected by many other variables, such as number of prey infected and rate of parasite transmission.     

Drivers of parasite community structure in fishes of the continental shelf of the Western Mediterranean: the importance of host phylogeny and autecological traits

We explored the relationships between features of host species and their environment, and the diversity, composition and structure of parasite faunas and communities using a large taxonomically consistent dataset of host-parasite associations and host-prey associations, and original environmental and host trait data (diet, trophic level, population density and habitat depth vagility) for the most abundant demersal fish species off the Catalonian coast of the Western Mediterranean. Altogether 98 species/taxa belonging to seven major parasite groups were recovered in 683 fish belonging to 10 species from seven families and four orders. Our analyses revealed that (i) the parasite fauna of the region is rich and dominated by digeneans; (ii) the host parasite faunas and communities exhibited wide variations in richness, abundance and similarity due to a strong phylogenetic component; (iii) the levels of host sharing were low and involved host generalists and larval parasites; (iv) the multivariate similarity pattern of prey samples showed significant associations with hosts and host trophic guilds; (v) prey compositional similarity was not associated with the similarity of trophically transmitted parasite assemblages; and (vi) phylogeny and fish autecological traits were the best predictors of parasite community metrics in the host-parasite system studied.     

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.     

Community ecology of the metazoan parasites of white croaker, Micropogonias furnieri (Osteichthyes: Sciaenidae), from the coastal zone of the State of Rio de Janeiro, Brazil

One hundred specimens of white croakers, Micropogonias furnieri (Desmarest 1823) (Osteichthyes: Sciaenidae) collected from Pedra de Guaratiba (23 degrees 01'S, 43 degrees 38'W), State of Rio de Janeiro, Brazil, from September 1997 to August 1999, were necropsied to study their parasites. The majority of the fish (95%) were parasitized by metazoan. Twenty-eight species of parasites were collected. The nematodes were the 40.5% of the total number of parasites specimens collected. Dichelyne elongatus was the most dominant species. Lobatostoma ringens, Pterinotrematoides mexicanum, Corynosoma australe, D. elongatus, and Caligus haemulonis showed a positive correlation between the host's total length and parasite prevalence and abundance. The monogenean P. mexicanum had differences in the prevalence and abundance in relation to sex of the host. The mean diversity in the infracommunities of M. furnieri was H=0.499+/-0.411, with correlation with the host's total length and without differences in relation to sex of the host. One pair of ectoparasites showed positive covariation, and two pairs of endoparasites showed positive association and covariation between their prevalences and abundances, respectively. Negative association or covariations were not found. The dominance of endoparasites in the croakers parasite infracommunities reinforced the differences found in sciaenids from the South American Pacific Ocean, in which the ectoparasites are dominant.     

Community ecology of the metazoan parasites of white sea catfish, Netuma barba (Osteichthyes: Ariidae), from the coastal zone of the state of Rio De Janeiro, Brazil.

Between March 2000 and April 2001, 63 specimens of N. barba from Angra dos Reis, coastal zone of the State of Rio de Janeiro (23 degrees 0' S, 44 degrees 19' W), Brazil, were necropsied to study their infracommunities of metazoan parasites. Fifteen species of metazoan parasites were collected: 2 digeneans, 1 monogenean, 2 cestodes, 1 acantocephalan, 2 nematodes, 6 copepods, and 1 hirudinean. Ninety-six percent of the catfishes were parasitized by at least one metazoan parasite species. A total of 646 individual parasites was collected, with mean of 10.3 +/- 16.6 parasites/fish. The copepods were 37.5% of the total parasite specimens collected. Lepeophtheirus monacanthus was the most dominant species and the only species with abundance positively correlated with the host total length. Host sex did not influence parasite prevalence or mean abundance of any species. The mean diversity in the infracommunities of N. barba was H = 0.130 +/- 0.115 with no correlation with host's total length and without differences in relation to sex of the host. One pair of endoparasites (Dinosoma clupeola and Pseudoacanthostomum floridensis) showed positive association and covariation between their abundances and prevalences. The parasite community of N. barba from Rio de Janeiro can be defined as a complex of species with low prevalence and abundance and with scarcity of interspecific associations. However, because of both the presence of assemblages of sympatric ariid species as well as the spawning behavior characteristic of these fishes, additional comparative studies of the parasite component communities of ariids are necessaries to elucidate this pattern.     

Vulnerability and diet breadth predict larval and adult parasite diversity in fish of the Bothnian Bay

Recent studies of aquatic food webs show that parasite diversity is concentrated in nodes that likely favour transmission. Various aspects of parasite diversity have been observed to be correlated with the trophic level, size, diet breadth, and vulnerability to predation of hosts. However, no study has attempted to distinguish among all four correlates, which may have differential importance for trophically transmitted parasites occurring as larvae or adults. We searched for factors that best predict the diversity of larval and adult endoparasites in 4105 fish in 25 species studied over a three-year period in the Bothnian Bay, Finland. Local predator–prey relationships were determined from stomach contents, parasites, and published data in 8,229 fish in 31 species and in seals and piscivorous birds. Fish that consumed more species of prey had more diverse trophically transmitted adult parasites. Larval parasite diversity increased with the diversity of both prey and predators, but increases in predator diversity had a greater effect. Prey diversity was more strongly associated with the diversity of adult parasites than with that of larvae. The proportion of parasite species present as larvae in a host species was correlated with the diversity of its predators. There was a notable lack of association with the diversity of any parasite guild and fish length, trophic level, or trophic category. Thus, diversity is associated with different nodal properties in larval and adult parasites, and association strengths also differ, strongly reflecting the life cycles of parasites and the food chains they follow to complete transmission.     

Spatial variation in species diversity and composition of flea assemblages in small mammalian hosts: geographical distance or faunal similarity?

Aim Spatial variation in the diversity of fleas parasitic on small mammals was examined to answer three questions. (1) Is the diversity of flea assemblages repeatable among populations of the same host species? (2) Does similarity in the composition of flea assemblages among populations of the same host species decay with geographical distance, with decreasing similarity in the composition of local host faunas, or with both? (3) Does the diversity of flea assemblages correlate with climatic variables? Location The study used previously published data on 69 species of small mammals and their fleas from 24 different regions of the Holarctic. Methods The diversity of flea assemblages was measured as both species richness and the average taxonomic distinctness of their component species. Similarity between flea assemblages was measured using both the Jaccard and Morisita–Horn indices, whereas similarity in the composition of host faunas between regions (host ‘faunal’ distance) was quantified using the Jaccard index. Where appropriate, a correction was made for the potentially confounding influence of phylogeny using the independent contrasts method. Results Flea species richness varied less within than among host species, and is thus a repeatable host species character; the same was not true of the taxonomic distinctness of flea assemblages. In almost all host species found in at least five regions, similarity in flea assemblages decreased with increases in either or both geographical and faunal distance. In most host species, the diversity of flea assemblages correlated with one or more climatic variable, in particular mean winter temperature. Main conclusions Spatial variation in flea diversity among populations of the same mammal species is constrained by the fact that it appears to be a species character, but is also driven by local climatic conditions. The results highlight how ecological processes interact with co‐evolutionary history to determine local parasite biodiversity.     

Are there general rules governing parasite diversity? Small mammalian hosts and gamasid mite assemblages

Parasite biodiversity varies on several scales, and in particular among different host species. Previous attempts at finding relationships between host features and the diversity of the parasite assemblages they harbour have yielded inconsistent results, suggesting strongly that any patterns might be taxon-specific. Here, we examined the potential of three host characteristics (host body mass, basal metabolic rate, and area of the geographical range) as determinants of parasite diversity in one group of ectoparasites, gamasid mites (superfamily Dermanyssoidea), using data from 63 species of small mammalian hosts. Our analyses used three measures of parasite diversity (species richness, the Shannon diversity index, and average taxonomic distinctness), and controlled for sampling effort and phylogenetic influences. Although several significant relationships were observed, they depended entirely on which diversity measure was used, or on which host taxon was investigated (insectivores vs. rodents and lagomorphs). In addition, the present results on patterns of mite diversity were not consistent with those of an earlier study involving roughly the same host taxa and the same biogeographical area, but a different group of ectoparasites, i.e. fleas. Thus, there appears to be no universal determinant of parasite diversity, and associations between host features and parasite diversity probably evolve independently in different host–parasite systems.     

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.     

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.     

Determinants of the parasite community of clariid fishes from Lake Victoria, Tanzania

The factors that determine parasite assemblages among the clariid fishes of Lake Victoria, Tanzania were studied between August 2003 and February 2005. Six hundred and fifty-six fish belonging to seven species were necropsied and examined for parasites, from which 31 species of metazoan parasites were recorded. The community was dominated by the nematodes both in species and numbers. Most species were generalists with only two trematodes, Diplostomum mashonense and Tylodelphys species, being specialists of Clarias gariepinus. Ten species were considered core and predictable. Parasite species richness, number of individuals per host and Shannon-Wiener diversity indices were generally high. At the compound community level, a mean number of 7.8 parasites were shared among different species of fish and the maximum number of parasites species per fish at the infracommunity level was seven. Levels of similarity in parasite species richness at the component community level ranged from 29.6 to 61.5%. The study concludes that parasite communities in clariid fishes of Lake Victoria are structured by ecological factors. At the infracommunity level, host size, diet and vagility promoted a richer parasite community. At the compound level, two factors were crucial, namely the intermixing of the waters in the lake and the predominant and mobile C. gariepinus.     

The functional traits of host fish can act as good predictors for parasite composition in a neotropical floodplain

Parasite diversity can be influenced by the interaction of environmental factors and host traits, but understanding which traits can be decisive for the establishment of the parasite may provide subsidies for a better understanding of the host-parasite relationship. In this study, we investigated whether functional traits, diet, and host phylogeny can predict the similarity of the endoparasite composition of a fish assemblage in a Brazilian floodplain. Of the three evaluated components, the host's diet was the factor that showed the greatest influence on the composition and similarity of endoparasites, demonstrating the highest value of the explanation. The functional traits and phylogeny, despite presenting significant values (unique effect and global effect), showed low explainability in the composition of the endoparasites. When analyzing the joint effects, all components showed significant influence. Hosts that live in the same environment that are phylogenetically related and have a similar ecology have a certain degree of homogeneity in their parasite assemblages and, because they are endoparasites (which are acquired trophically along the chain), diet is the main driver of parasite richness and similarity. Overall, host traits can be one of the main determinants of parasite composition, so studies that address the functional traits of the host provide a representation of local diversity and define the possible patterns of these parasite communities.     

Host introductions and the geography of parasite taxonomic diversity

Aim Geographical variation in parasite diversity is examined among populations of fish in their original heartland and in areas where they have been introduced. The diversity in heartland and introduced populations is contrasted, and also compared with the expectations of a null model. Location Data on the parasite communities of two salmonid fish species were obtained: the rainbow trout Oncorhynchus mykiss in its British Columbia heartland and in introduced populations in North America, Great Britain, South America and New Zealand; and the brown trout Salmo trutta in heartland populations from Great Britain, and in introduced populations in North America, South America and New Zealand. Methods The average taxonomic distinctness and its variance were computed for each parasite community, and used as measures of the taxonomic diversity of parasite species in each fish population. Observed values of taxonomic distinctness were also compared with those expected if each community was a random selection from the world list of parasite species known for each of the two host species. Results Few parasite communities departed from the expectations of the null model, i.e. few had a taxonomic diversity of parasites greater or lower than that expected from a random selection of parasite species. However, these departures were not more or less likely among heartland fish populations than among introduced ones. In both fish species, parasite communities in introduced populations tended to be a little more taxonomically diverse than in the heartland populations. Main conclusions Overall, the results suggest that the accumulation of parasite species in introduced hosts over short (ecological) periods of time can result in parasite assemblages that are just as, or even more, taxonomically diverse than those developed over much longer (evolutionary) time frames in the host species geographical heartland. This finding highlights the importance of ecological factors in parasite biodiversity in addition to coevolutionary processes.     

Host-specialization and species diversity in fish parasites: phylogenetic conservatism?

The pattern of parasite species diversification and specialization, appreciated by host range, is investigated in fish parasites. We test whether host range is linked with phylogeny at a high taxonomic level, and if there is a relationship between host range and host species diversification. For this purpose we used two sets of data, one on macro-parasites of marine fishes of the Mediterranean Sea and the other on macro-parasites of marine and freshwater fishes of Canada. Similar patterns of host range among parasitic groups were found. Our findings suggest that habitat (marine vs freshwater) and geographic localization (Canada vs Mediterranean region) play little role in determining the observed patterns of host range. We highlight the potential influence of phylogeny (high-taxonomic level) on the level host range in parasites. We find that parasites with free-swimming larval stages and with direct life cycles have a narrower range of host species than do parasites with indirect life cycle, even if we cannot control for phylogenetic effects because of the lack of variation of life cycles within each parasitic group. Finally, a positive relationship was found between the number of known hosts and parasite species diversity in the case of Mediterranean parasite species. The relationship between host range and species diversification should be related to the mechanism of cospeciation.     

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.