The functional importance of parasites in animal communities: many roles at many levels?

Past research on parasites and community ecology has focussed on two distinct levels of the overall community. First, it has been shown that parasites can have a role in structuring host communities. They can have differential effects on the different hosts that they exploit, they can directly debilitate a host that itself is a key structuring force in the community, or they can indirectly alter the phenotype of their host and change the importance of the host for the community. Second, certain parasite species can be important in shaping parasite communities. Dominant parasite species can directly compete with other parasite species inside the host and reduce their abundance to some extent, and parasites that alter host phenotype can indirectly make the host more or less suitable for other parasite species. The possibility that a parasite species simultaneously affects the structure of all levels of the overall community, i.e. the parasite community and the community of free-living animals, is never considered. Given the many direct and indirect ways in which a parasite species can modulate the abundance of other species, it is conceivable that some parasite species have functionally important roles in a community, and that their removal would change the relative composition of the whole community. An example from a soft-sediment intertidal community is used to illustrate how the subtle, indirect effects of a parasite species on non-host species can be very important to the structure of the overall community. Future community studies addressing the many potential influences of parasites will no doubt identify other functionally important parasite species that serve to maintain biodiversity.     

Linking community assembly and structure across scales in a wild mouse parasite community

Understanding what processes drive community structure is fundamental to ecology. Many wild animals are simultaneously infected by multiple parasite species, so host–parasite communities can be valuable tools for investigating connections between community structures at multiple scales, as each host can be considered a replicate parasite community. Like free‐living communities, within‐host–parasite communities are hierarchical; ecological interactions between hosts and parasites can occur at multiple scales (e.g., host community, host population, parasite community within the host), therefore, both extrinsic and intrinsic processes can determine parasite community structure. We combine analyses of community structure and assembly at both the host population and individual scales using extensive datasets on wild wood mice (Apodemus sylvaticus) and their parasite community. An analysis of parasite community nestedness at the host population scale provided predictions about the order of infection at the individual scale, which were then tested using parasite community assembly data from individual hosts from the same populations. Nestedness analyses revealed parasite communities were significantly more structured than random. However, observed nestedness did not differ from null models in which parasite species abundance was kept constant. We did not find consistency between observed community structure at the host population scale and within‐host order of infection. Multi‐state Markov models of parasite community assembly showed that a host's likelihood of infection with one parasite did not consistently follow previous infection by a different parasite species, suggesting there is not a deterministic order of infection among the species we investigated in wild wood mice. Our results demonstrate that patterns at one scale (i.e., host population) do not reliably predict processes at another scale (i.e., individual host), and that neutral or stochastic processes may be driving the patterns of nestedness observed in these communities. We suggest that experimental approaches that manipulate parasite communities are needed to better link processes at multiple ecological scales.     

Communities of parasites of freshwater fish of Jersey, Channel Islands

The parasite faunas of 12 species of freshwater fish from 17 localities on the island of Jersey were examined. Comparison of the species composition, number, diversity and equitability of the parasite fauna of each species of fish in each locality revealed that community diversity was always low, that most communities were dominated by a single species of parasite, and that community similarity between host species, and often between sites, was generally low. This was not related to unavailability or distribution of potential, invertebrate, intermediate host species, but appeared to be due to chance colonization events. With two exceptions, little exchange of parasites took place between host species, despite vacant niches in the parasite communities and the absence of competitors, and normal parasite specificity was maintained. Comparison of the parasite communities with those on other oceanic islands suggests that they are poorer than would be predicted by island biogeographical theory, and that this is not a very good predictor of parasite community richness on oceanic islands.     

The life-history impact and implications of multiple parasites for bumble bee queens

Most studies of the consequences of parasitism on fitness have examined single host–parasite systems. However, parasitological studies show that most hosts are constantly challenged by a complex parasite community. Thus, neither the response of hosts to individual parasite species nor the individual impact of these parasite species is likely to be as unconstrained as studies of single host–parasite systems might suggest. In this study, the parasite community structure in spring queens of the common European bumble bee, Bombus pratorum, was assessed. By capturing queens and allowing them to rear colonies in the laboratory, the relative impact of different parasite species on fitness across the annual host life-cycle could be examined. Of 160 queens, 67% were parasitised by one or more members of a five-species parasite community. The impact of parasites varied from being highly virulent to undetectable under benign laboratory conditions. The majority of multi-parasite infections involved a high impact parasite, which resulted in the removal of associated parasites from the host population. This study shows that, whilst multiple infections occur within individual hosts, most parasites act individually on their hosts. However, multiple parasite species in the host population may constrain the host population’s ability to adapt to single parasite species.     

Halfway up the trophic chain: development of parasite communities in the sparid fish Boops boops

We examined the patterns of composition and structure of parasite communities in the Mediterranean sparid fish Boops boops along a gradient of fish sizes, using a large sample from a single population. We tested the hypothesis that species forming the core of the bogue parasite fauna (i.e. species which have a wide geographical range and are responsible for recognizable community structure) appear early in the fish ontogeny. The sequential community development observed supported the prediction that core species appear in the fish population earlier than rare and stochastic species. There was also a strong correlation between the order of 'arrival' of the species and their overall prevalence. Six key species were responsible for recognizable community structure across size/age cohorts; the addition to this baseline community of key parasite species resulted in a nested structure that is linked to differential species abundance rather than fish size. Information on the life-cycles, distribution and host range of the parasites is used to explain the observed patterns of parasite community structure. We conclude that the small mouth size of B. boops coupled with suction feeding may provide a setting for passive sampling as a mechanism leading to non-random parasite community structure.     

Seasonal dynamics of the component community structure of parasites of the minnow Phoxinus phoxinus (L.)

The material represented by 75 specimens of minnow of the age 2-2(+) was collected according to the standard technique in the Chovju River (tributary of the Vychegda River, a region of the settlement Nizniy Chov, district of Syktyvkar town) during the period June-September 2000. The quantitative estimation of the structure of the component parasite communities was performed by calculating errors of the equation of regression for each species group separately, with subsequent summarizing of means of errors by all parasite groups comprising the community (Dorovskikh, 2001 6; 2002 B). In order to have a possibility to get data complementing each other, the calculation of variety indexes and other indexes have been made for metazoan parasites only and for the whole community, including the protozoan parasites. In both cases, i.e. considering only metazoan parasites and the whole composition of parasite species, three states of the component parasite community have been recognised: the formed community (June), the community in destroying (July and August), the community in the process of formation (September). In the course of working on the total species composition we recorded the beginning of community destroying on 30th of June, and the beginning of community formation in August. Considering only the metazoan parasites, the community is defined (after: Pugachev, 1999) as the mature (balanced) one in June, while in July, August and September, it was unmature (off-balance) by its characteristics. Regarding the protozoan parasites, the community in June, August and September was characterized as the mature one based on indices of parasite biomass, and as unripe one based on the number of parasite individuals; however in July, both groups of indices allowed to refer it to the unripe state. However, these unripe states are essentially different. In July, it is the result of dieing out the parasites of the past generation; in August and September, it is the result of the appearances of new generations. Therefore we recognise three states of parasite community named above. Considering the whole species composition of parasites we noted the greater difference of index values based on the parasite specimen numbers and their conventional biomass, that was in the case of the metazoan parasites only. It is particularly noticeable in the middle of the June, in the period of the formed community. This fact, together with high errors of the equations of regression and the presence of the high number of Apiosoma, points to the disturbance in the structure of component parasite community in the minnow from the Chovju River. This is easily explicable, because the Chovju River is the polluted reservoir, and pollution comes from agricultural fields, Verhny-Chov settlement, pigsties and cow-sheds. The pollution is a seasonal factor here. The most powerful pollution was noted at May-June, and then it decreased along the beginning of rains in the end of August; in September it increased again. It is important to point out that the monitoring of the metazoan parasites only allows to reveal the general dynamics of the community during the period of observation, but does not allow to catch the beginning of its destroying and developing and to notice possible disturbances in the community structure caused by pollution of reservoirs, particularly, if this pollution is a seasonal factor as in the Chovju River. Three named states of the component community of the fish parasites take place in other periods of year than this observed in the intestional parasite communities of fish helminths of the temperate climate zone. The developing of parasite communities of the intestinal helminths of the Anguilla anguilla in England (Kennedy, 1997) and of Leuciscus idus from the Rybinsk reservoir (Zhohov, 2003) starts in the beginning of summer. In May, their species diversity is minimal and in August is maximal. In conditions of the middle stream of the Vychegda River, the species diversity of parasite community associated with the minnow is maximal in June and minimal in August, when it only begins developing.     

An examination of the infracommunities and component communities from impala (Aepyceros melampus) in the Kruger National Park, South Africa

The intestinal helminth parasites of the impala from the Kruger National Park, South Africa, were examined to describe the parasite community structure. Demographic variation and the associated differences in behavior were used to further investigate the patterns of community composition. Monte Carlo simulations were performed to test for differences in species richness and mean abundance between the various demographic groups, and nonmetric multidimensional scaling ordination was used to compare community composition. Seventeen species of nematodes, totaling more than 1.3 million worms, were recovered. Males harbored a greater number of nematode species than did females, but adult females were more heavily infected than their male counterparts. Lambs acquired infections early in life, and their parasite community composition rapidly approached that of the older animals. The parasite community in the juvenile and adult males was significantly different from the community of the adult females. These data suggest that social and feeding behavior of the different age-sex classes structure the parasite component community of impala. Additionally, the distinction between common and rare parasites, and their classification in other herbivores, implies complex transmission dynamics that includes extensive species sharing within the Kruger National Park.     

Eutrophication,biodiversity loss,and species invasions modify the relationship between host and parasite richness during host community assembly

Host and parasite richness are generally positively correlated, but the stability of this relationship in response to global change remains poorly understood. Rapidly changing biotic and abiotic conditions can alter host community assembly, which in turn, can alter parasite transmission. Consequently, if the relationship between host and parasite richness is sensitive to parasite transmission, then changes in host composition under various global change scenarios could strengthen or weaken the relationship between host and parasite richness. To test the hypothesis that host community assembly can alter the relationship between host and parasite richness in response to global change, we experimentally crossed host diversity (biodiversity loss) and resource supply to hosts (eutrophication), then allowed communities to assemble. As previously shown, initial host diversity and resource supply determined the trajectory of host community assembly, altering post‐assembly host species richness, richness‐independent host phylogenetic diversity, and colonization by exotic host species. Overall, host richness predicted parasite richness, and as predicted, this effect was moderated by exotic abundance—communities dominated by exotic species exhibited a stronger positive relationship between post‐assembly host and parasite richness. Ultimately, these results suggest that, by modulating parasite transmission, community assembly can modify the relationship between host and parasite richness. These results thus provide a novel mechanism to explain how global environmental change can generate contingencies in a fundamental ecological relationship—the positive relationship between host and parasite richness.     

The parasites of Anolis lizards the northern Lesser Antilles

Summary The communities of parasitic helminths from ten species of lizards on seven islands in the Caribbean were examined to ascertain the relative importance of predictable deterministic factors and unpredicatable colonization or extinction events in determining the structure of the parasite community. A simple graphical model of community structure is used as a null model to describe the features of a community that are dependent only upon the size of the host population and features of the life histories of the constituent parasite species. This model predicts that parasite species will exhibit a nested pattern of local and global relative abundance. The observed data correspond fairly well to this pattern. The absences of individual parasite species from communities where they might be expected to be present emphasizes the role of stochastic colonization and extinction events in delineating the constituent members of the community on any island.Statistical analysis of the distribution of parasite species per host illustrates that this pattern is random in habitats where parasite species diversity is low, but decreasingly variable in habitats where more diverse parasite communities occur. Increased parasite diversity also leads to an increase in the proportion of hosts that contain mixed species infections. Comparisons of worm burdens from single and mixed species infections within individual hosts suggest that interactions between parasite species only rarely leads to reduced worm burdens.     

Parasite establishment and host extinction in model communities

Studies of host–parasite dynamics usually consider one, or at most two, host species, neglecting the possible effects of other species on the focal hosts and vice versa. To explore the interaction of community structure with host–parasite dynamics, we model the invasion of stable communities of varying size by a parasite. The communities are generated with random interaction coefficients and connectance 0.5. Each community is invaded by parasites with different values of virulence (disease-induced host mortality rate), specificity and transmission rate. The result of each invasion is determined by numerically simulating the dynamics of the community. We classify the outcomes by whether the parasite successfully establishes in the focal host population(s), and, if so, by the proportion of host and non-host species that go extinct as a result of the parasite's introduction. We discuss how the structure of the community and the interaction between hosts and other species affect several important processes of disease ecology: the density threshold for parasite invasion, extinction cascades caused by the parasite, and the frequency of extinctions of hosts and non-hosts. In our simulated communities, non-host species went extinct more frequently than hosts, suggesting the importance of the community context of disease. In some cases, the parasite's invasion induced regular population cycles in the previously stable community.     

Climate,host phylogeny and the connectivity of host communities govern regional parasite assembly

Aim

Identifying barriers that govern parasite community assembly and parasite invasion risk is critical to understand how shifting host ranges impact disease emergence. We studied regional variation in the phylogenetic compositions of bird species and their blood parasites (Plasmodium and Haemoproteus spp.) to identify barriers that shape parasite community assembly.

Location

Australasia and Oceania.

Methods

We used a data set of parasite infections from >10,000 host individuals sampled across 29 bioregions. Hierarchical models and matrix regressions were used to assess the relative influences of interspecies (host community connectivity and local phylogenetic distinctiveness), climate and geographic barriers on parasite local distinctiveness and composition.

Results

Parasites were more locally distinct (co‐occurred with distantly related parasites) when infecting locally distinct hosts, but less distinct (co‐occurred with closely related parasites) in areas with increased host diversity and community connectivity (a proxy for parasite dispersal potential). Turnover and the phylogenetic symmetry of parasite communities were jointly driven by host turnover, climate similarity and geographic distance.

Main conclusions

Interspecies barriers linked to host phylogeny and dispersal shape parasite assembly, perhaps by limiting parasite establishment or local diversification. Infecting hosts that co‐occur with few related species decreases a parasite's likelihood of encountering related competitors, perhaps increasing invasion potential but decreasing diversification opportunity. While climate partially constrains parasite distributions, future host range expansions that spread distinct parasites and diminish barriers to host shifting will likely be key drivers of parasite invasions.     

Downstream changes in the composition of the parasite community of fishes in an Appalachian stream

The spatial distribution of 6 parasite species (Myxobolus sp., Dactylogyrus sp., Sterliadochona ephemeridarum, Plagioporus sinitsini, Allopodocotyle chiliticorum, Allocreadium lucyae) was studied in 5 species of fishes (Oncorhynchus mykiss, Clinostomus funduloides, Notropis chiliticus, Rhinichthys atratulus, Semotilus atromaculatus) in Basin Creek, an Appalachian stream in North Carolina. Nonmetric multidimensional scaling and vector fitting were used to determine if the proximity of sampling sites was related to community similarity. Position along Basin Creek was significantly related to parasite community structure. Breaks in parasite community composition were imposed by waterfalls at upstream areas of Basin Creek that restricted distributions of C. funduloides, N. chiliticus, and S. atromaculatus and at the downstream limit of the study area by a break in the distribution of S. ephemeridarum coincident with the existence of a dam but were independent of suitable piscine host distributions. These discontinuities in parasite community composition imply that the relationship between proximity of sites and community similarity is predictive because distance between sites is related to the probability that fish at different sampling sites recruit parasites from different species pools. This relationship is not the same for all component communities.     

Examining the area effect for parasite communities of bluegill x green sunfish hybrids in five constructed ponds in Kansas

The parasite communities of bluegill x green sunfish hybrids were examined from 5 constructed ponds in Kansas in an attempt to evaluate the separate effects of habitat area and habitat heterogeneity on parasite community structure. Characterization of fish community structure and collection of hybrid fishes was conducted using an electrofishing boat. Benthic invertebrates were sampled, and substrate types examined at 30 evenly spaced points in each pond. Nonmetric multidimensional scaling of the parasite infracommunities, in concert with an analysis of similarities, indicated significant clustering of infracommunities by locality. The number and diversity of habitat types, and the richness and diversity of both fishes and benthic invertebrates, were positively correlated with the first axis of the infracommunity ordination. Pond surface area, parasite richness, and stocking pressure were negatively correlated with the first axis of the infracommunity ordination, suggesting that pond area, stocking pressure, or both was a stronger determinant of parasite community structure in these systems than habitat and host heterogeneity.     

The influence of a parasite community on the dynamics of a host population: a longitudinal study on willow ptarmigan and their parasites

Despite the fact that most host populations are infected by a community of different parasite species, the majority of empirical studies have focused on the interaction between the host and a single parasite species. Here, we explore the hypothesis that host population dynamics are affected both by single parasite species and by the whole parasite community. We monitored population density and breeding productivity of two populations of willow ptarmigan ( Lagopus lagopus ) in northern Norway for 8 and 11 years, respectively, and sampled eukaryotic endoparasites. We found that increasing abundances of the cestode Hymenolepis microps was associated with increased breeding mortality and reduced annual growth rate of the host population in both areas, and reduced host body mass and body condition in the area where such data were available. In one of the areas, the abundance of the nematode Trichostrongylus tenuis was associated with reductions in host body mass, body condition and breeding mortality and the filaroid nematode Splendidofilaria papillocerca was negatively related to host population growth rates. The parasite community was also negatively related to host fitness parameters, suggesting an additional community effect on host body mass and breeding mortality, although none of the parasites had a significant impact on their own. The prevalence of parasites with very different taxonomical origins tended to covary within years, suggesting that variability in the parasite community was not random, but governed by changes in host susceptibility or environmental conditions that affected exposure to parasites in general. Other variables including climate, plant production and rodent densities were not associated with the recorded demographic changes in the host population.     

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.     

Patterns of parasite community dissimilarity: the significant role of land use and lack of distance‐decay in a bat–helminth system

Increasing community dissimilarity across geographic distance has been described for a wide variety of organisms and understanding its underlying causes is key to understanding mechanisms driving patterns of biodiversity. Both niche‐based and neutral processes may produce a distance decay relationship; however, disentangling their relative influence requires simultaneous examination of multiple potential drivers. Parasites represent a unique opportunity in which to study distance decay because community dissimilarity may depend on environmental requirements and dispersal capability of parasites as well also those of their hosts. We used big brown bats Eptesicus fuscus and their intestinal helminths to investigate: 1) independent contributions of geographic and environmental distances on dissimilarity of intestinal helminth component communities between populations of big brown bats; 2) which environmental variables best explained variation in community dissimilarity; and 3) whether similar patterns of decay with geographic or environmental distance were observed for within‐host population and within‐individual host parasite communities. We used compositional measures of community dissimilarity to examine how parasite communities may change with geographic distance and varying environmental conditions. Non‐spatial variables strongly influenced compositional parasite community dissimilarity over multiple community scales, and we observed little evidence for spatial processes such as distance decay. Environment surrounding roost sites better predicted helminth community dissimilarity than any other class of variables and landcover classes representing anthropogenic modification consistently explained variation in community structure. Our results indicate that human disturbance drives significant patterns of parasite community dissimilarity, most likely by changing the presence or abundance of intermediate hosts in an area.     

Host traits associated with species roles in parasite sharing networks

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

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.     

Parasites in marine protected areas: success and specificity of monogeneans

The effect of a marine protected area on the Lamellodiscus spp. monogenean community was tested by comparing the communities of parasites of Diplodus sargus inside and outside of the area. A total of 104 D. sargus were dissected harbouring 1280 monogeneans from the genus Lamellodiscus and belonging to 11 species. No modification in the global parasite community linked with the protection of the host populations was revealed. The most abundant and less specific parasite species, Lamellodiscus elegans , however, increased its abundance in the protected area. A significant relationship was found between parasite host range and the percentage of infected hosts. A significant relationship also occurred between epidemiological and genetic distances for the parasite species found. The results are discussed in term of parasite success and specificity and the importance of taking into account parasitism in the biological conservation of hosts.