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.     

Parasite species richness in New Zealand fishes: a grossly underestimated component of biodiversity?

Estimates of total parasite species richness, for given host groups in given geographical areas, are always much higher than the numbers of known parasite species on which they are based. The discrepancy is a reflection of our limited current knowledge of parasite diversity. This is illustrated by a comparison of the parasite faunas of New Zealand fish species with those of Canadian fish; the latter have been well studied by fish parasitologists, and provide a standard for comparisons. More parasite species are known per host species for Canadian fish than for New Zealand fish, for both marine and freshwater fishes. This difference remains after correcting for differences in study effort, i.e. in the number of published studies per fish species. There are also more parasite species per fish species in Canada than in New Zealand when parasite species richness is expressed as number of species per unit of host body length. For freshwater fish, the difference can be explained by the restricted phylogenetic origins and geographical isolation of New Zealand fish species. For marine fish, however, there is no a priori reason to expect a difference in parasite species richness between fish in New Zealand and Canadian waters, and the observed difference probably results from a lack of appropriate parasitological surveys in New Zealand. If the true species richness of the parasite faunas of New Zealand marine fish species approaches that of their Canadian counterparts, then most of the diversity and ecosystem function of fish parasites in New Zealand remains unknown.     

Linking ecology with parasite diversity in Neotropical fishes

A comparative analysis was performed to seek large-scale patterns in the relationships between a set of fish species traits (body size, type of environment, trophic level, schooling behaviour, depth range, mean habitat temperature, geographical range, ability to enter brackish waters and capability of migration) and the diversity of their metazoan parasite assemblages among 651 Neotropical fish species. Two measurements of parasite diversity are used: the species richness and the taxonomic distinctness of a fish's parasite assemblage, including all metazoan parasites, ectoparasites only, or endoparasites only. The results showed that, on this scale, the average taxonomic distinctness of parasite assemblages was clearly more sensitive to the influence of host traits than parasite species richness. Differences in the taxonomic diversification of the parasite assemblages of different fish species were mainly related to the fish's environment (higher values in benthic–demersal species), trophic level (positive correlation with increasing level), temperature (positive correlation with temperature in marine ectoparasites, negative in endoparasites; positive for all groups of parasites in freshwater fishes) and oceanic distribution (higher values in fish species from the Pacific Ocean than those of the Atlantic). The results suggest that, among Neotropical fish species, only certain key host traits have influenced the processes causing the taxonomic diversification of parasite assemblages.     

Comparison of the parasitic fauna of Aplocheilus panchax and A. melastigma

The metazoan parasite fauna of two species of freshwater fishes Aplocheilus panchax and A. melastigma collected from a stream at Waltair is compared; 17 parasite species were found. Aplocheilus panchax served as a host to 13 parasite species and A. melastigma to 10 parasite species. Of the 17 parasites collected, 12 were larval helminths to which the fishes act as intermediate and paratenic hosts. This has been attributed to the interaction between terrestrial birds, mammals and fishes in determining the parasite fauna in the biocoenosis. The parasite fauna of these fishes is divided into typical and less typical according to their frequencies. Among less typical there are peripheral division parasites which are abundant in other fishes in the stream. Only six parasite species occurred in both A. panchax and A. melastigma and both fish shared most of their parasite fauna with other fishes. Differences in the parasite fauna of these fishes are attributed to the morphological, behavioural or ecological features of these fishes.     

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.     

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.     

Aggregation and species coexistence of ectoparasites of marine fishes.

Interspecific interaction may lead to species exclusion but there are several ways in which species can coexist. One way is by reducing the overall intensity of competition via aggregated utilisation of fragmented resources. Known as the 'aggregation model of coexistence', this system assumes saturation and an equilibrium number of species per community. In this study we tested the effects of interspecific aggregation on the level of intraspecific aggregation among ectoparasites of marine fishes (36 communities of gill and head ectoparasite species). If parasite species are distributed in a way that interspecific aggregation is reduced relative to intraspecific aggregation then species coexistence is facilitated. We found a positive relationship between parasite species richness and fish body size, controlling for host phylogeny. A positive relationship between infracommunity species richness and total parasite species richness was also found, providing no evidence for saturation. This result supports the view that infracommunities of parasites are not saturated by local parasite residents. The observed lack of saturation implies that we are far from a full exploitation of the fish resource by parasites. Ectoparasites were aggregated at both population and species levels. However, only half of the ectoparasite communities were dominated by negative interspecific aggregation. We found that infracommunity parasite species richness was positively correlated with the level of intraspecific aggregation versus interspecific aggregation. This means that intraspecific aggregation increases compared with interspecific aggregation when total parasite species richness increases, controlling fish size and phylogeny. This supports one assumption of the 'aggregation model of coexistence', which predicts that interspecific interactions are reduced relative to intraspecific interactions, facilitating species coexistence.     

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.     

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.     

Host population density as the major determinant of endoparasite species richness in floodplain fishes of the upper Paraná River, Brazil

A comparative analysis of parasite species richness was performed across 53 species of fish from the floodplain of the upper Paraná River, Brazil. Values of catch per unit effort, CPUE (number of individuals of a given fish species captured per 1000 m(2) of net during 24 h) were used as a rough measure of population density for each fish species in order to test its influence on endoparasite species richness. The effects of several other host traits (body size, social behaviour, reproductive behaviour, spawning type, trophic category, feeding habits, relative position in the food web, preference for certain habitats and whether the fish species are native or exotic) on metazoan endoparasite species richness were also evaluated. The CPUE was the sole significant predictor of parasite species richness, whether controlling for the confounding influences of host phylogeny and sampling effort or not. The results suggest that in the floodplain of the upper Paraná River (with homogeneous physical characteristics and occurrence of many flood pulses), population density of different host species might be the major determinant of their parasite species richness.     

Host preference and specialization in Gnathia sp., a common parasitic isopod of coral reef fishes

A gnathiid species (Crustacea: Isopoda; one of the most common ectoparasites of coral reef fishes) from the Great Barrier Reef, Australia, was allowed to choose among fishes from three different families to feed on (using two species of fishes per family). Gnathiids showed a strong preference for labrids, rarely feeding on pomacentrids or apogonids. In a separate experiment, gnathiid host preference did not vary among three labrid fish species. Gnathiids that fed on labrids had higher survival than those that fed on apogonids. Male gnathiids that fed on labrids also moulted to the adult stage more quickly. This suggests that host specialization and local adaptation might be occurring between these ectoparasites and their host fishes at the host fish family level.     

Zoogeography of the shorefish fauna of Clipperton Atoll

One hundred and fifteen species of fishes (14 oceanic, plus 101 shore and nearshore species) are known from Clipperton Island, a small, remote coral atoll in the tropical eastern Pacific (TEP). This fish fauna includes only 14% of the region's shallow-water species, and also is depauperate relative to the fish faunas of other isolated tropical islands. The island's isolation, small size, reduced habitat diversity, and oceanic environment contribute to this paucity of species.Fifty-two species at Clipperton can be identified as TEP; these include 37 widespread species, six species shared only with the Revillagigedo Islands [the nearest (950 km) offshore shoals], and eight endemic to Clipperton. Endemics species apparently have a mix of west and east Pacific origins. Sixty-three species are transpacific; they include three new records (of Naso surgeonfishes) that maybe vagrants recruited > 4,000 km from Oceania.Clipperton is situated at the juncture between the TEP and Oceania. Its fish fauna contains about equal numbers of TEP and transpacific species. This faunal structure reflects the relative influence of surface currents from Oceania and the TEP. Although most of Clipperton's transpacific shorefishes are widespread in eastern Oceania, the Clipperton fauna has specific affinities to the fauna of the Line Islands, which are located within the main eastbound current from Oceania. Clipperton may therefore be a major stepping stone for dispersal between Oceania and the remainder of the TEP. About 50% of the non-oceanic, tropical transpacific fishes occur there, and at least 75 % of those species apparently have resident populations at the island.     

Species diversity and abundance of freshwater fishes in irrigation ditches around rice fields

The relationships between environmental variables, distribution of freshwater fishes and their diet were investigated at 40 sites on irrigation ditches for rice fields in central Japan. Multivariate analyses showed that fish species richness and diversity in ditches was high when fishes were able to easily invade the rice fields. Natural stream beds not covered by concrete had greater total number and biomass of fishes in irrigation ditches. The connection between ditches and rice fields was of secondary importance. Canonical correlation analysis indicated that the two principal fish community variables, abundance and diversity, were respectively represented by the presence of the minnow, Gnathopogon elongatus elongatus, and the absence of the loach, Misgurnus anguillicaudatus. Most fishes in the irrigation ditches predominantly preyed upon aquatic insects such as ephemeropteran nymphs, chironomid larvae and trichopteran larvae, but aerial insects and benthic algae were also fed upon by a few species. Small fishes (<4cm SL) preyed more on chironomid and less on trichopteran larvae than large (4cm SL) fishes. The diet overlap between species was extremely high for small fishes in ditches weakly connected with rice fields. The recent changes in rice fields and irrigation ditches to increase production efficiency has led to a decrease in fish diversity. For the coexistence of rice production and fish diversity in rice areas, a new irrigation system, where fishes can easily invade rice fields and where plenty of invertebrates are available for fishes, should be developed.     

West African rivers as biogeographic islands: species richness of fish communities

Summary Some factors influencing the species richness of West African fish communities were studied in a sample of 26 rivers using four habitat and hydrologic variables. Analysis of a larger sample of 39 rivers showed that species richness was positively related to area. A power function with an exponent of 0.32 gave the best fit. As the surface area used was that of the catchment area and not that (unknown) of the river, the biological significance of this relationship and the possibilities of comparison were limited. Ridge regression analysis and forward stepwise selection indicated that a model that explained ln(species richness) as a function of ln(mean annual discharge) and ln-(catchment surface area) was best, accounting for 90% of the variance of the dependent variable. The combination of surface area and discharge was presumed to act through the volume of water available for the fishes and habitat productivity. Habitat diversity, measured by the diversity of the terrestrial vegetation covering the catchment area, had no significant positive effect when surface area was used in the regression. Rivers (islands) should have fewer species than tributaries of similar size since, for fishes within a river system (continent), there is free circulation between all its branches. The model derived from the river data underestimated the species richness of a sample of 11 tributaries. This was compatible with the hypothesis of higher population extinction rates in insular biotopes. The residuals of the linear model did not show random geographical distribution; the rivers in some areas had more species than expected. The possibility that historical factors, especially Quaternary climatic variations, might cause this distribution is discussed.     

Helminth communities of native and introduced fishes in Lake Pátzcuaro, Michoacán, México

In Lake Pátzcuaro in the Mesa Central of México, a total of 19 species of helminths was found in 598 fishes and comprised five digeneans, two monogeneans, four cestodes, one acanthocephalan and seven nematodes, of which ten species were represented by larval or immature states. The richest and most diverse helminth communities were found in the native carnivorous goodeid Alloophorus robustus. In general, the helminth communities in the different fish species were not particularly species rich and the parasite assemblages were numerically dominated by larvae of the bird trematode, Posthodiplostomum minimum. Patterns of helminth community richness and diversity were similar to those previously observed in north-temperate freshwater fishes. Most enteric helminths occurred with low abundance and only a small proportion of the gut helminth communities was numerically dominated by any one species. Helminths dominating their enteric communities showed some level of host specificity. Helminth communities in carnivorous fish species were generally richer than those in herbivores and detritivores, with the exception of the predominantly herbivorous Goodea atripinnis. The helminth fauna of introduced fishes, Cyprinus carpio, Micropterus salmoides and Oreochromis niloticus , consisted of either few or no host-specific adult helminth(s) translocated from their original geographical areas and by larval stages of helminths of piscivorous birds. Based on the geological history of the area and the biogeography of the endemic fish fauna, it is hypothesized that host-switching and relationships with the nearctic fauna have been fundamental in determining the helminth fauna of the endemic fish hosts.     

Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals

Epidemiological theory predicts positive correlations between host population density or body mass and species richness among parasite communities. Here I test these predictions by a comparative study of communities of directly transmitted mammalian parasites, gastrointestinal strongylid nematodes. I use data from 45 species of mammals, representing examination of 17 200 individual hosts. The variable studied was the average number of gastrointestinal strongylid nematode species per host population, and three different methods were used to obtain estimates of parasite species richness that are unbiased by number of host individuals examined. Analyses were done using the phylogenetically independent contrast method. Host population density and parasite species richness were strongly positively correlated when the effects of host body weight had been controlled for. Controlling for other variables did not change this, and the relationship was found regardless of method used to correct for uneven sampling effort among host species. A positive relationship between parasite species richness and host body weight was also found, but the effect of host densities had to be controlled for to see this. These relationships between host traits and species richness of directly transmitted parasites are stronger than patterns found using data on indirectly transmitted mammalian parasites, and suggests that links between host traits and parasite species richness are stronger than previously suggested. The results are consistent with parasite species richness being positively linked to pathogen transmission rates and reductions in transmission rates possibly increasing extinction probabilities in parasite populations. The results also suggest that parasites may exert a cost of increases in rate of population energy usage, and thus show that pathogens may be important in generating independence between body mass and rate of population energy usage among host species.     

Comparing the richness of metazoan ectoparasite communities of marine fishes: controlling for host phylogeny

Parasite communities are the product of acquisitions and losses of parasite species during the evolutionary history of their host. When comparing the parasite communities of different host species to assess the role of ecological variables as determinants of parasite species richness, a correction must be made for the possible phylogenetic inheritance of parasites from ancestral hosts independent of host ecology. We performed a comparative analysis of the metazoan ectoparasite communities on the heads and gills of 111 species of marine fish. The influences of host body size, host schooling behaviour and water temperature were tested after controlling for both sampling and phylogenetic effects. Overall, water temperature correlated positively with both parasite species richness and abundance, whereas fish size only correlated with parasite abundance. The correlation across all fish species between water temperature and parasite species richness was dependent on an outlier point. The results, however, generally held when fish from different biogeographical areas (Pacific and Atlantic) were analysed separately. In all analyses, parasite species richness always correlated strongly with parasite abundance. There was no evidence that schooling fish taxa harboured richer or more abundant ectoparasite communities than their non-schooling sister taxa, possibly because of the small number of contrasts available for that test. Overall, whereas both water temperature and host size affect the number of parasite individuals that can be harboured by a fish, only temperature appears important as a determinant of ectoparasite community richness. Received: 30 May 1996 / Accepted: 23 October 1996     

Macroecology of a host-parasite relationship

The larvae of freshwater mussels are obligate ectoparasites on fishes while adults are sedentary and benthic. Dispersal of mussels is dependent on the movement of fish hosts, a regional process, but growth and reproduction should be governed by local processes. Thus, mussel assemblage attributes should be predictable from the regional distribution and abundance of fishes. At a broad spatial scale in the Red River drainage, USA, mussel species richness and fish species richness were positively associated; maximum mussel richness was limited by fish richness, but was variable beneath that constraint. Measured environmental variables and the associated local fish assemblages each significantly accounted for the regional variation in mussel assemblages. Furthermore, mussel assemblages showed strong spatial autocorrelation. Variation partitioning revealed that pure fish effects accounted for 15.4% of the variation in mussel assemblages; pure spatial and environmental effects accounted for 16.1% and 7.8%, respectively. Shared variation among fish, space and environmental variables totaled 40%. Of this shared variation, 36.8% was associated with the fish matrix. Thus, the variation in mussel assemblages that was associated with the distribution and abundance of fishes was substantial (> 50%), indicating that fish community structure is an important determinant of mussel community structure. Although animals commonly disperse plants and, thus, influence the structure of plant communities, our results show a strong macroecological association between two disparate animal groups with one strongly affecting the assemblage structure of the other.     

The evolutionary transition to coloniality promotes higher blood parasitism in birds

Parasitism has been argued as one of the major costs of breeding sociality in birds. However, there is no clear evidence for an increased parasite pressure associated with the evolutionary transition from solitary to colonial breeding. I used the pairwise comparative method to test whether colonial bird species incur in a greater risk of infection and if they must to face with a greater diversity of blood parasites (Haematozoa), by comparing pairs of congeners that included one solitary and one colonial breeding species. The richness, both in terms of number of species and number of genera, as well as the prevalence of blood parasites resulted higher in colonial species than in their solitary breeding sisters, while controlling for differences in research effort and other potentially confounding effects. These results point towards higher transmission rates of blood parasites among colonial hosts. Given the detrimental effects of blood parasites on their host fitness, the higher risk of infection and the exposition to a more diverse parasite fauna may have imposed an important cost associated to the evolution of avian coloniality. This may help to explain why colonial species have larger immune system organs, as well as to explore differences in other host life history traits potentially shaped by blood parasites.