Distribution and abundance of parasite nematodes: ecological specialisation,phylogenetic constraint or simply epidemiology?

We investigate the patterns of abundance‐spatial occupancy relationships of adult parasite nematodes in mammal host populations (828 populations of nematodes from 66 different species of terrestrial mammals). A positive relationship between mean parasite abundance and host occupancy, i.e. prevalence, is found which suggests that local abundance is linked to spatial distribution across species. Moreover, the frequency distribution of the parasite prevalence is bimodal, which is consistent with a core‐satellite species distribution. In addition, a strong positive relationship between the abundance (log‐transformed) and its variance (log‐transformed) is observed, the distribution of worm abundance being lognormally distributed when abundance values have been corrected for host body size.
Hanski et al. proposed three distinct hypotheses, which might account for the positive relationship between abundance and prevalence in free and associated organisms: 1) ecological specialisation, 2) sampling artefact, and 3) metapopulation dynamics. In addition, Gaston and co‐workers listed five additional hypotheses. Four solutions were not applicable to our parasitological data due to the lack of relevant information in most host‐parasite studies. The fifth hypothesis, i.e. the confounded effects exerted by common history on observed patterns of parasite distributions, was considered using a phylogeny‐based comparison method. Testing the four possible hypotheses, we obtained the following results: 1) the variation of parasite distribution across host species is not due to phylogenetic confounding effects; 2) the positive relationship between mean abundance and prevalence of nematodes may not result from an ecological specialisation, i.e. host specificity, of these parasites; 3) both a positive abundance‐prevalence relationship and a negative coefficient of variation of abundance‐prevalence relationship are likely to occur which corroborates the sampling model developed by Hanski et al. We argue that demographic explanations may be of particular importance to explain the patterns of bimodality of prevalence when testing Monte‐Carlo simulations using epidemiological modelling frameworks, and when considering empirical findings. We conclude that both the bimodal distribution of parasite prevalence and the mean‐variance power function simply result from demographic and stochastic patterns (highlighted by the sampling model), which present compelling evidence that nematode parasite species might adjust their spatial distribution and burden in mammal hosts for simple epidemiological reasons.     

Searching for generality in the patterns of parasite abundance and distribution: Ectoparasites of a South African rodent, Rhabdomys pumilio

We studied abundance and distribution of seven ectoparasite species (fleas Chiastopsylla rossi and Dynopsyllus ellobius, a louse Polyplax arvicanthis, mites Androlaelaps fahrenholzi and Laelaps giganteus and two ticks Haemaphysalis elliptica and Hyalomma truncatum) exploiting the same populations of the rodent host Rhabdomys pumilio in South Africa. We considered three general patterns of abundance and distribution, namely (i) aggregated distribution of parasites amongst individual hosts; (ii) positive relationships between mean parasite abundance and their prevalence; and (iii) applicability of a simple epidemiological model based on mean parasite abundance and its variance to predict the observed patterns of prevalence. Our aims were to evaluate the relative role of host- versus parasite-associated factors by looking at similarity amongst different parasites in these patterns. In general, all parasites demonstrated strong similarity in each of the three patterns of abundance and distribution. However, the strength of these patterns differed amongst parasite species. We conclude that these patterns are driven mainly by hosts, but differences are caused by differences between various life-history traits of parasite species. Our results support the idea that general laws apply to parasite population ecology.     

Distribution of fleas (Siphonaptera) among small mammals: mean abundance predicts prevalence via simple epidemiological model

We used data on the abundance and distribution of fleas parasitic on small mammals in Slovakia and aimed: (i) to confirm a positive relationship between abundance and distribution fleas within and across host species; and (ii) to test if prevalence of fleas can be reliably predicted from a simple epidemiological model that takes into account flea mean abundance and its variance. Prevalence of a flea species increased with an increase in its mean abundance both within and across host species. We calculated prevalences both for each flea-host association and for each flea species across all hosts. Observed prevalences did not differ significantly from those predicted by the epidemiological model using parameters of Taylor's power relationship between mean abundance of fleas and its variance. Regressions of predicted prevalences against observed prevalences produced slope values that did not differ significantly from unity and were independent of scale (within or across host species). Our results demonstrated that up to 96% of variance in flea prevalence can be explained solely by their mean abundance. We concluded that, in general, there is no need to invoke other, more complex factors for the explanation of the variation in flea prevalence.     

Invasive parasites are detectable by their abundance-occupancy relationships: the case of helminths from Liza haematocheilus (Teleostei: Mugilidae)

The biogeographic patterns of abundance and prevalence of helminths from Liza haematocheilus were studied across its native (Sea of Japan) and introduced (Sea of Azov) distribution ranges. Abundance-occupancy relationships (AORs) were tested for the core-satellite and enemy release (ERH) species hypotheses in eight and 14 host samples from the native and introduced host ranges, respectively. The AOR model fitted parasite data extremely well, irrespective of whether the host or the parasite species were native or invasive. Except for co-introduced monogeneans, species were less abundant and prevalent in the introduced host population than in the native one, which agrees well with the ERH. Two occupancy patterns were observed. A unimodal, right-skewed distribution of prevalence frequency was common for the acquired groups of helminth parasites in the introduced range, whereas a bimodal distribution was more common in the native range. Core species in the native range were monogeneans, adult and larval digeneans, whereas host-specific, co-introduced monogeneans were the only core species in the introduced range. Acquired grey-mullet specialists and host generalists infected only a small portion of the introduced host population with low mean abundance. These results indicate that strict host specificity, together with a direct life cycle, are the traits that enabled helminth species to entirely occupy the invasive host population. The AORs showed that parasite individuals tend to accumulate in a relatively small fraction of susceptible introduced hosts, probably as an adaptation to enhance mating opportunities, thereby providing a mechanistic explanation of the ERH. All this evidence suggests that co-introduced and acquired species use the introduced host population in very different ways. Therefore, we posit that the examination of AORs can be instrumental in understanding the role of co-introduced parasites in invasion theory.     

Spatial variation in population density across the geographical range in helminth parasites of yellow perch Perca flavescens

The abundance of a species is not constant across its geographical range; it has often been assumed to decrease from the centre of a species’ range toward its margins. The central assumption of this “favourable centre” model is tested for the first time with parasites, using different species of helminth parasites exploiting fish as definitive hosts. Data on prevalence (percentage of hosts that are infected) and abundance (mean no. parasites per host) were compiled for 8 helminth species occurring in 23 populations of yellow perch Perca flavescens, from continental North America. For each parasite species, correlations were computed between latitude and both local prevalence and abundance values. In addition, the relationships between the relative prevalence or abundance in one locality and the distance between that locality and the one where the maximum value was reported, were assessed separately for each species to determine whether abundance tends to decrease away from the presumed centre of the range, where it peaks. For both the cestode Proteocephalus pearsei and the acanthocephalan Leptorhynchoides thecatus, there was a positive relationship between prevalence or abundance and the latitude of the sampled population. There was also a significant negative relationship between relative prevalence and the distance from the locality showing the maximum value in P. pearsei, but no such pattern was observed for the other 7 parasite species. Since this single significant decrease in prevalence with increasing distance from the peak value may be confounded by a latitudinal gradient, it appears that the distribution of abundance in parasites of perch does not follow the favourable centre model. This means that the environmental variables affecting the density of parasites (host availability, abiotic conditions) do not show pronounced spatial autocorrelation, with nearby sites not necessarily providing more similar conditions for the growth of parasite populations than distant sites.     

Mammal density and patterns of ectoparasite species richness and abundance

Patterns of species richness, prevalence and abundance of ectoparasites have rarely been investigated at both the levels of populations and species of hosts. Here, we investigated the effects in changes in small mammal density on species richness, abundance and prevalence of ectoparasitic fleas. The comparative analyses were conducted for different small mammal species and among several populations during a long-term survey. We tested the hypothesis that an increase in host density should be linked with an increase in parasite species richness both among host species and among populations within host species, as predicted by epidemiological models. We also used host species density data from literature. We found that host density has a major influence on the species richness of ectoparasite communities of small mammals among host populations. We found no relationship between data of host density from the literature and parasite species richness. In contrast with epidemiological hypotheses, we found no relationships between abundance, or prevalence, and host density, either among host species or among host populations. Moreover, a decrease in abundance of fleas in relation with an increase in host density was observed for two mammal species (Apodemus agrarius and A. flavicollis). The decrease or the lack of increase in flea abundance in relation with an increase in host density suggests anti-parasitic behavioural activities such as grooming.     

The intra- and interspecific relationships between abundance and distribution in helminth parasites of birds

1. Positive correlations between local abundance and distribution on a larger spatial scale are commonly observed among related species.
2. Within parasite species, the same relationship may be expected between prevalence and intensity of infection across host species used. Across parasite species, a positive relationship is expected between average abundance in a host population and the number of host species that can be exploited based on the resource breadth hypothesis. Trade-offs between the ability to exploit many host species and the potential for heavy infections, however, could result in a negative relationship.
3. Intraspecifically, using data on 51 helminth species parasitic in birds, prevalence and intensity of infection among host species used are generally only weakly correlated. Only in nematodes is there an overall positive relationship between prevalence and intensity.
4. A comparative analysis was performed on data from 389 species of cestodes, trematodes and nematodes parasitic in birds to determine how host specificity covaries interspecifically with abundance, measured both as prevalence and intensity of infection.
5. After controlling for phylogenetic influences and sampling effort, the number of host species used correlated positively with prevalence in all three parasite taxa, and with intensity of infection in trematodes only.
6. These results do not support the existence of a trade-off between abundance and the use of many host species, as has been found for fish parasites. Instead, whatever makes helminth parasites of birds abundant within a host population may facilitate their successful colonization of new host species.     

Parasitization of bats by bat flies (Streblidae) in fragmented habitats

Parasites represent a large fraction of the world's biodiversity. They control host population sizes and contribute to ecosystem functioning. However, surveys on species diversity rarely include parasitic species. Bats often present traits favoring parasite diversity, such as large home ranges, long life spans, and large colonies. The most conspicuous bat parasites are the highly host-specific, blood-sucking bat flies (Diptera: Streblidae, Nycteribiidae). Recent studies have found a direct effect of habitat alteration on the abundance of bat species. We expected, therefore, that changes in the host community in response to anthropogenic habitat modification will also result in changes in the associated parasite community. We captured bats in three different habitats in Central Panama between 2013 and 2015. We recorded information on prevalence and intensity of bat fly parasitization of the seven most commonly captured bat species. Prevalence and intensity were both significantly influenced by roost type, abundance, and host sex and age. We found that habitat variables and matrix type significantly influenced the prevalence and intensity of parasitization, while the direction of the responses was host species- and parasite species-specific. In general, roosting conditions and behavior of host bats appear to be fundamental in explaining changes in prevalence and intensity of parasitization between different habitat types, as bat flies are bound to the roost during their reproductive cycle. Habitat alterations affect next to the host community composition also the availability of possible roost structures as well as microclimatic conditions, which all three reflect in parasitization.     

Metazoan parasites of freshwater cyprinid fish ( Leuciscus cephalus): testing biogeographical hypotheses of species diversity

The diversity and similarity of parasite communities is a result of many determinants widely considered in parasite ecology. In this study, the metazoan parasite communities of 15 chub populations (Leuciscus cephalus) were sampled across a wide geographical range. Three hypotheses of biogeographical gradients in species diversity were tested: (1) latitudinal gradient, (2) a 'favourable centre' versus 'local oasis' model, and (3) decay of similarity with distance. We found that the localities in marginal zones of chub distribution showed lower parasite species richness and diversity. A latitudinal gradient, with increasing abundance of larvae of Diplostomum species, was observed. There was a general trend for a negative relationship between relative prevalence or abundance and the distance from the locality with maximum prevalence or abundance for the majority of parasite species. However, statistical support for a 'favourable centre' model was found only for total abundance of Monogenea and for larvae of Diplostomum species. The phylogenetic relatedness of host populations inferred an important role when the 'favourable centre' model was tested. Testing of the hypothesis of 'decay of similarity with geographical distance' showed that phylogenetic distance was more important as a determinant of similarity in parasite communities than geographical distance between host populations.     

Distribution patterns and microhabitat segregation in gastrointestinal helminths of Sorex shrews

We studied the distribution patterns and microhabitat use in gastrointestinal helminths of the shrews Sorex araneus and S. caecutiens in Finland. The distribution of species prevalences was bimodal, and in S. araneus the abundance (mean intensity) was positively associated with commonness (prevalence), as assumed by the core-satellite species hypothesis (Hanski 1982). However, the positive correlation between prevalence and intensity was observed only when the effects of helminth body size and taxonomic group (cestodes vs nematodes) on intensity were controlled for. The nematodes of the genus Longistriata occurred predictably as core species, whereas the identity of the core cestodes was more variable between host species and regions. Helminth body size and taxonomic group were not related to the degree of aggregation in shrew populations, but helminth body size seemed to explain the differences in the distribution patterns of helminths between shrews and voles. The core species did not show more segregation in microhabitat use than randomly selected species. In fact, the two core nematodes showed largely overlapping intestinal distributions. We conclude that linear intestinal space is not a key resource for shrew nematodes, but it may be for shrew cestodes.     

The effect of habitat on the helminth parasites of an island population of the Polynesian rat (Rattus exulans)

Differences in helminth faunal composition, distribution and abundance were studied in three habitats on an island on which the Polynesian rat, Rattus exulans (Peale), is the only rodent present. The effects of season and of host age and sex were also included in the analysis. Habitat had a statistically significant effect on the prevalence and/or abundance of all seven parasites included in this study. Season influenced four species (Brachylaima apoplania, Capillaria sp., Heterakis spumosa and Mastophorus muris) but had little or no detectable effect on the remaining three (Capillaria hepatica, Hymenolepis diminuta and Syphacia muris) . Of the two intrinsic variables, age but not sex was found to have an effect. A comparison of the effects of each variable on parasite prevalence confirmed that habitat was the most important of the four variables. In a prior study on the influence of habitat on host population dynamics on this island, between-habitat differences were shown to include adult longevity, total population density and the seasonal availability and abundance of various food types. These factors, together with physical differences in the microhabitat and the parasite's life cycle, help to provide explanations for the observed results.     

Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections.

Helminth parasites were studied in the wood mouse, Apodemus sylvaticus, in southern England in September of each of four successive years (1994-1997). Nine species of helminths were recorded: five nematodes (Heligmosomoides polygyrus, Syphacia stroma, Pelodera strongyloides, Trichuris muris, Capillaria murissylvatici), two cestodes (Microsomacanthus crenata, Taenia taeniaeformis) and two trematodes (Corrigia vitta, Brachylaemus recurvum). In total, 134 mice were examined and 91.8% carried at least one species of helminth. The majority of mice carried two to three species (60.5%) and the highest combination was six of the nine species recorded in the study. The patterns of between-year variations in the prevalence and abundance of infection were different for each of the six species for which sufficient quantitative data were available to enable statistical analysis. For H. polygyrus, the most important source of variation arose from between-year differences, host age and the interaction of these factors: abundance increased with host age but in 1995 the age pattern was markedly different from that in the remaining years. The abundance of C. vitta also varied significantly between years but additionally there was a strong independent age effect. For M. crenata, the year x age interaction was significant, indicating that abundance among different age cohorts varied from year to year but there was also a weak significant main effect of age arising from the youngest age cohort carrying no parasites and the oldest age cohort the heaviest infections. For P. strongyloides the only significant factor was between-year variation with 1995 being a year of exceptionally low prevalence and abundance of infection. No significant between-year variation was detected for S. stroma but there was a strong sex effect (males carrying heavier infections) and an age effect (older mice of both sexes carrying heavier infections). The abundance of Trichuris muris varied only in relation to host age, worm burdens growing in intensity with increasing age, but there was also a significant interaction between year and host sex with respect to prevalence. For the remaining three species, the prevalence of infections was too low (< 8.2%) to enable any meaningful interpretation. This analysis emphasizes the need for carefully controlled statistical procedures in aiding the interpretation and the prioritization of the factors affecting worm burdens in wild rodents.     

Uncorrelated mistletoe infection patterns and mating success with local host specialization in <Emphasis Type="Italic">Psittacanthus calyculatus</Emphasis> (Loranthaceae)

Mistletoe infection between conspecific and interspecific hosts can be restricted by seed dispersal, host-mistletoe compatibility and abiotic factors, yet no studies have linked mistletoe infection patterns and pollination together for understanding mistletoe distribution at a local scale. Psittacanthus calyculatus (Loranthaceae) is a hemiparasitic plant with a broad host range across its geographic distribution. The potential for local host adaptation has been shown using cross-inoculation experiments, in which plants of mistletoe seeds collected from a given host are more likely to survive when they are inoculated on conspecific host trees compared with those inoculated on other host provenances. Here we evaluate host adaptation by describing the local patterns of infection (prevalence and intensity) of P. calyculatus mistletoes on three native host tree species (Alnus acuminata, Quercus crassipes, Salix bonplandiana) and one introduced species (Populus alba) and carried out cross-pollination experiments to examine how pollination affects infection patterns of different host species. Mistletoe infection prevalence (proportion of infection) and infection intensity (mean number of mistletoes per tree) were in general disproportional with respect to the availability of native host tree species but higher to that of non-native host tree species. Cross-pollination experiments showed higher mating success on the native host tree species, suggesting higher local adaptation to specially Q. crassipes. The observed spatial distribution of host tree species and mistletoe infection along with the non-random mating could contribute to local genetic structuring of mistletoe populations.     

Diversity of avian haemosporidians in arid zones of northern Venezuela

Arid zones of northern Venezuela are represented by isolated areas, important from an ornithological and ecological perspective due to the occurrence of restricted-range species of birds. We analysed the prevalence and molecular diversity of haemosporidian parasites of wild birds in this region by screening 527 individuals (11 families and 20 species) for parasite mitochondrial DNA. The overall prevalence of parasites was 41%, representing 17 mitochondrial lineages: 7 of Plasmodium and 10 of Haemoproteus. Two parasite lineages occurred in both the eastern and western regions infecting a single host species, Mimus gilvus. These lineages are also present throughout northern and central Venezuela in a variety of arid and mesic habitats. Some lineages found in this study in northern Venezuela have also been observed in different localities in the Americas, including the West Indies. In spite of the widespread distributions of some of the parasite lineages found in northern Venezuela, several, including some that are relatively common (e.g. Ven05 and Ven06), have not been reported from elsewhere. Additional studies are needed to characterize the host and geographical distribution of avian malaria parasite lineages, which will provide a better understanding of the influence of landscape, vector abundance and diversity, and host identity on haemosporidian parasite diversity and prevalence.     

Distribution of the cestode Caryophyllaeides fennica (Cestoda: Lytocestidae) in the population of cyprinid fish in the Rybinsk water reservoir

The distribution of the cestode Caryophyllaeides fennica in populations of the ide, roach, white bream and bream from the Rybinsk reservoir has been analyzed in regard to fish age. The relative abundance of C. fennica in populations of each host species was calculated as product of the helminthes abundance by the fish number in age groups. The highest prevalence and abundance of cestodes was found in the ide. All age classes of this species were infected, with the maximum in fishes of the age 3+ ... 5+. The roach is infected with C. fennica till only 10-year age; brean is infected till the age 4+. In the white bream C. fennica is an occasional parasite. The cestode number among hosts was as follows: bream--68%; roach--26%, ide--5%, white bream--1%. Different approaches to the estimation of the parasite abundance distribution among several host species (in terms of mean prevalence and intensity of the relative abundance of parasites) are discussed.     

Parasites of Perccottus glenii Dybowski, 1877 (Actinopterygii: Odontobutidae) in the native and the introduced host range: Abundance–occupancy and abundance–variance relationships

The Chinese sleeper Perccottus glenii Dybowski, 1877 is an invasive fish species rapidly expanding in Siberia and Europe. Its native range encompasses the Far East region of Russia, northeastern China and northern North Korea. We studied species composition, prevalence, mean abundance and variance of mean abundance of macroparasites of the Chinese sleeper in the native and the introduced range. The species composition of the parasite component communities differed considerably in the native and the introduced range. The frequency distributions of prevalence, mean abundance and variance of mean abundance of the parasites did not demonstrate any significant differentiation between the two parts of the host range. However, an analysis of the abundance–occupancy and the abundance–variance relationships revealed that the parasite component communities in the two parts of the host range were quite distinct. In the native range, prevalence increased faster and variance increased more slowly with the increasing abundance of the parasites than in the introduced range. These features are mostly associated with considerably increased prevalence, abundance and aggregation of the host-specific cestode Nippotaenia mogurndae in recipient water bodies as compared with the native habitats.     

Ectomycorrhizal communities in a productive Tuber aestivum Vittad. orchard: composition, host influence and species replacement

Truffles (Tuber spp.) and other ectomycorrhizal species form species-rich assemblages in the wild as well as in cultivated ecosystems. We aimed to investigate the ectomycorrhizal communities of hazels and hornbeams that are growing in a 24-year-old Tuber aestivum orchard. We demonstrated that the ectomycorrhizal communities included numerous species and were phylogenetically diverse. Twenty-nine ectomycorrhizal taxa were identified. Tuber aestivum ectomycorrhizae were abundant (9.3%), only those of Tricholoma scalpturatum were more so (21.4%), and were detected in both plant symbionts with a variation in distribution and abundance between the two different hosts. The Thelephoraceae family was the most diverse, being represented by 12 taxa. The overall observed diversity represented 85% of the potential one as determined by a jackknife estimation of richness and was significantly higher in hazel than in hornbeam. The ectomycorrhizal communities of hornbeam trees were closely related phylogenetically, whereas no clear distribution pattern was observed for the communities in hazel. Uniform site characteristics indicated that ectomycorrhizal relationships were host mediated, but not host specific. Despite the fact that different plant species hosted diverse ectomycorrhizal communities and that the abundance of T. aestivum differed among sites, no difference was detected in the production of fruiting bodies.     

Epidemiological prediction of the distribution of insects of medical significance: comparative distributions of fleas and sucking lice on the rat host Rattus norvegicus in Yunnan Province, China

Determining the distribution patterns of ectoparasites is important for predicting the spread of vector-borne diseases. A simple epidemiological model was used to compare the distributions of two different taxa of ectoparasitic insects, sucking lice (Insecta: Siphonaptera) and fleas (Insecta: Anoplura), on the same rodent host, Rattus norvegicus Berkenhout (Rodentia: Muridae), in Yunnan Province, China. Correlations between mean abundance and prevalence were determined. Both fleas and sucking lice were aggregated on their hosts, and sucking lice showed a higher degree of aggregation than fleas. The prevalence of both fleas and sucking lice increased with log-transformed mean abundance and a highly linear correlation and modelling efficiency of predicted prevalence against observed prevalence were obtained. The results demonstrate that prevalence can be explained simply by mean abundance.     

Host characteristics do not affect community structure of ectoparasites on the fishing bat Noctilio leporinus (L., 1758) (Mammalia: Chiroptera)

Patterns of parasite abundance and prevalence are thought to be influenced by several host characteristics such as size, sex, developmental stage, and seasonality. We examined two obligatory ectoparasites of the bat Noctilio leporinus (L.) (Chiroptera, Noctilionidae) to test whether prevalence and abundance of Noctiliostrebla aitkeni Wenzel and Paradyschiria fusca Speiser (Diptera, Streblidae) are influenced by the host characteristics. During this survey, 2110 flies were collected. The total abundance was 1150 N. aitkeni and 950 P. fusca. The prevalence of both species was shown to be superior to 75% and neither host size, sex, reproductive stage nor season influenced significantly the variation of the observed values. N. aitkeni were more abundant than P. fusca in all seasons except winter. Both flies showed a significant seasonal variation in terms of abundance but host biological characteristics (host size, sex, and reproductive stage) did not play a significant role as structuring factors of the batflies component community.