Parasite Assemblages Research Articles

Stocks and seasonal migrations of the flounder Xystreurys rasile as indicated by its parasites

The aims of this study were (1) to compare the structure and composition of parasite assemblages of the flounder Xystreurys rasile in two regions of the Argentine Sea in order to evaluate the hypothesis for the existence of different stocks, and (2) to test the hypothesis for X. rasile migration from the Argentine-Uruguayan Common Fishing Zone (AUCFZ) towards more southern waters during spring. Parasitological evidence shows that at least two stocks of X. rasile inhabit the coastal and shelf waters of the northern Argentine Sea, one in El Rincón and the other in the AUCFZ. These stocks should be considered as discrete entities in management plans to ensure a sustainable use of these resources. The results also confirm the existence of migratory patterns in the northern stock.

Introduction of Steven A. Nadler, Recipient of the Henry Baldwin Ward Medal for 2013

Introduction of Steven A. Nadler, Recipient of the Henry Baldwin Ward Medal for 2013

A Metabolic and Body-Size Scaling Framework for Parasite Within-Host Abundance, Biomass, and Energy Flux

Energetics may provide a useful currency for studying the ecology of parasite assemblages within individual hosts. Parasite assemblages may also provide powerful models to study general principles of ecological energetics. Yet there has been little ecological research on parasite-host energetics, probably due to methodological difficulties. However, the scaling relationships of individual metabolic rate with body or cell size and temperature may permit us to tackle the energetics of parasite assemblages in hosts. This article offers the foundations and initial testing of a metabolic theory of ecology (MTE) framework for parasites in hosts. I first provide equations to estimate energetic flux through observed parasite assemblages. I then develop metabolic scaling theory for parasite abundance, energetics, and biomass in individual hosts. In contrast to previous efforts, the theory factors in both host and parasite metabolic scaling, how parasites use host space, and whether energy or space dictates carrying capacity. Empirical tests indicate that host energetic flux can set parasite carrying capacity, which decreases as predicted considering the scaling of host and parasite metabolic rates. The theory and results also highlight that the phenomenon of "energetic equivalence" is not an assumption of MTE but a possible outcome contingent on how species partition resources. Hence, applying MTE to parasites can lend mechanistic, quantitative, predictive insight into the nature of parasitism and can inform general ecological theory.

Evolution of parasite island syndromes without long‐term host population isolation: parasite dynamics in Macaronesian blackcaps Sylvia atricapilla

AbstractAimThe study of parasite biogeography on islands is important for our understanding of both the processes involved in the evolution of parasite assemblages worldwide and the ecology and conservation of insular communities. By studying the haemosporidian blood parasites of a bird that has recently colonized a number of oceanic islands, we were able to test hypotheses relating to the processes of parasite colonization and community assembly prior to the permanent isolation of host species on islands.LocationThe Atlantic Ocean archipelagos of Madeira and the Canary Islands.MethodsWe used cytochrome b DNA sequences to determine the prevalence and richness of parasites of the genera Haemoproteus, Plasmodium and Leucocytozoon in blackcaps, Sylvia atricapilla, a widespread passerine that colonized these archipelagos during the Last Glacial Maximum. We compared insular blackcap parasite assemblages with those observed in 37 blackcap populations sampled on mainland Europe.ResultsThe insular parasite assemblage was impoverished, containing c. 10% of the parasites found on the continent. None of the parasites observed on the islands were blackcap specific. Some of the observed parasites appear to have switched from blackcaps to other Macaronesian host species, whereas others were of Afrotropical origin and were acquired after blackcaps colonized the islands. The prevalence of parasites in the island populations of blackcaps was lower than in mainland blackcap populations and parasite richness decreased with increasing island distance to the continent.Main conclusionsMacaronesian blackcaps do not face the strong parasite load encountered by their mainland counterparts despite the fact that blackcap migration from the continent may directly transport mainland blackcap parasites to the islands. This supports the idea that normal mainland host–parasite associations are compromised on islands and that parasite island syndromes (low richness, frequent host‐switching and reduced specialization) evolve even before insular host populations become completely isolated from their mainland counterparts.

Parasites in subyearling Chinook salmon (Oncorhynchus tshawytscha) suggest increased habitat use in wetlands compared to sandy beach habitats in the Columbia River estuary

Many estuaries in the Pacific Northwest have been severely altered reducing wetlands habitat and resulting in an interest in their importance as rearing areas for juvenile salmon. To examine differences in habitat use during residency in the Columbia River estuary, we examined parasite communities acquired through food web interactions in subyearling Chinook salmon (Oncorhynchus tshawytscha) collected from four different habitat types in May and July of 2004 and 2005. Collections were made from two sandy bottom habitat types in the tidal freshwater and marine mixing areas of the estuary. These were compared to two wetlands types: one composed of scrub and shrub vegetation and another with emergent vegetation. Parasite assemblages differed among habitats suggesting differences in salmon feeding opportunities and rearing behaviors. In both years, the nematode, Hysterothylacium aduncum and the acanthocephalan, Echinorhynchus lageniformis, which use intermediate hosts found in the estuary, were more prevalent in lower wetlands suggesting increased feeding by salmon in these habitats. The differences in parasite assemblages among habitats suggests a variety of rearing and migration patterns through the Columbia River estuary and the increased prevalences of some parasites in the wetlands show that these habitats can be important feeding grounds for salmon.

Evaluating the role of regional and local processes in structuring a larval trematode metacommunity of Helisoma trivolvis

Metacommunity theory has advanced our understanding of how local and regional processes affect the structure of ecological communities. While parasites have largely been omitted from metacommunity research, parasite communities can provide the large sample sizes and discrete boundaries often required for evaluating metacommunity patterns. Here, we used assemblages of flatworm parasites that infect freshwater snails (Helisoma trivolvis) to evaluate three questions: 1) what factors affect individual host infections within ponds? 2) Is the parasite metacommunity structured among ponds? And 3) what is the relative role of local versus regional processes in determining metacommunity structure and species richness among ponds? We examined 10 821 snails from 96 sites in five park complexes in the San Francisco Bay area, California, and found 953 infections from six parasite groups. At the within‐pond level, infection status of host snails correlated positively with individual snail size and pond infection prevalence for all six parasite groups. Using an ordination method to test for metacommunity structure, we found that the parasite metacommunity was organized in a non‐random pattern with species responding individually along an environmental gradient. Based on a model selection approach involving local and regional predictors, parasite species richness and metacommunity structure correlated with both local abiotic (pH and total dissolved nitrogen) and biotic (non‐host mollusk density, and H. trivolvis biomass) factors, with little support for regional predictors. Overall, this trematode metacommunity most closely followed the predictions from the species sorting or mass effects metacommunity paradigm, in which community diversity is filtered by local site characteristics.

Endemism in host–parasite interactions among island populations of an endangered species

AbstractAimImplicit in conserving interactions is the idea that species behave differently throughout their range, resulting in functionally dissimilar populations of the same species. Host–parasite interactions are a useful system to explore the pervasiveness of these ecological phenotypes. Here, we investigated whether the role of an endangered, endemic species to provide habitat for ectoparasites varies throughout the geographic distribution of the host.LocationChannel Islands, California.MethodsWe captured island foxes (Urocyon littoralis sp.) from three populations: Santa Catalina (n = 72), Santa Rosa (n = 79) and San Miguel (n = 83). We compared the extent to which variation in parasite attributes were due to differences among individuals or populations. As a measure of the latter, we used discriminant function analysis to determine whether individuals from the same population ‘cluster’ together when comparing patterns of intensity in various ectoparasites.ResultsWe identified eight ectoparasite species that included at least six new parasite records for island foxes. We found that ectoparasite attributes including diversity and intensity varied among host populations. More importantly, we show that knowing the parasite composition of the host can identify its population of origin, due to unique host–parasite interactions. Overall, we correctly ‘assigned’ 72% of island foxes to their actual, respective populations, although there were inconsistencies among populations.Main conclusionsIf foxes generally have the same parasite assemblage regardless of their respective populations, then conservation of a single population likely maintains all necessary species interactions and discriminate function analysis is uninformative in discerning population assignments of individuals. Our findings highlight the importance of conserving populations to maintain endemic interactions and caution against extrapolating the ecology (i.e. known species associations) of a species to other locations within their range.

Can the studies at a spatial scale of 100s meters detect the spatiotemporal fluctuations of a parasite assemblage?

The importance of small-scale heterogeneity in local factors which overrides that of larger-scales factors, suggest that local factors play a major role in determining the richness and prevalence of larval digeneans in intertidal gastropods. The restricted distribution of the snail Heleobia australis along a 500 m transect in Cangrejo creek (Mar Chiquita, Argentina) provides a good opportunity to test the assumption that a study at spatial scale of 100s meters can detect spatiotemporal fluctuations of a larval digenean assemblage. To analyze that, 3600 specimens of H. australis were collected seasonally during the year 2011. A quantitative variation and a space-time interaction between sampling points and seasons of the year for the total prevalence of larval digeneans and snail's densities were found, as well as a positive correlation with abiotic factors. These results revealed that the fluctuations in the community of larval digeneans of the snail H. australis can be detected at small spatial scale, using its natural distribution of 500 m. This study also highlights the importance of seasonality as a factor that must be considered in studies focused on the search for patterns structuring the communities of larval digeneans, at medium and large scales.

Patterns of variation in parasite component communities and infracommunities of a littoral fish species from the northern coast of Chile

The structure and similarity of the parasite communities of fish can be evaluated at the component community (CC) and infracommunity (IC) levels. Both hierarchical levels have been used to assess parasite variations in fish at large (biogeographic) scales. However, studies evaluating the consistency between these two hierarchical levels at smaller geographical scales are scarce. In this study, the parasite assemblages of 124 Paralabrax humeralis collected by local fishermen by spear fishing at four sites (El Fierro, EF; P. Angamos, PA; Santa María, ISM; San Jorge, BSJ) in northern Chile were compared to assess the variability (or similarity) of their CCs and ICs at a limited geographical scale using multivariate analysis. At the IC level, discriminant analyses showed that P. humeralis parasite communities varied significantly among sites; 70% of ectoparasite ICs were correctly assigned to each site, but only 55% of helminth parasite ICs were correctly classified. At the CC level, the composition of parasite communities as assessed by correspondence analyses varied significantly between sites. Tagia sp., Neobenedenia sp. and Philometra sp. were associated with BSJ, ISM and PA, respectively; Corynosoma sp. and most digeneans were associated with both ISM and EF. Analysis of similarities (ANOSIM) showed significant variations in the degree of similarity between P. humeralis CCs from different sites, but not between ICs. Variations between CCs from different sites reflect fish population processes (e.g., population age, reproductive segregation) and the particular conditions of their respective habitats, whereas ICs reflect individual host movements. This study demonstrated that, when examined at a limited geographical scale, IC is better than CC at capturing the local pool of parasite assemblages when host populations are spatially segregated. Therefore, in this study, it is demonstrated that at a small geographic scale, CC variations are not reflected by IC, when host population is spatially segregated.

Blood Parasite Infestation and the Leukocyte Profiles in Adult and Immature Reed Warblers (Acrocephalus scirpaceus) and Sedge Warblers (Acrocephalus schoenobaenus) During Autumn Migration

Haemoparasites prevalence in birds can vary among species, age and sex groups and ecological conditions. To comprehend the host—parasite assemblages, it is important to investigate physiological mechanisms underlying the interactions in wild bird species. Here, using blood smears we investigated how leukocyte profiles in reed warblers (Acrocephalus scirpaceus) and sedge warblers (Acrocephalus schoenobaenus) vary in relation to the heamoparasite presence with respect to the host's age and sex. We sampled the birds during their autumn migration in 2008 at a stopover site in northern Poland. We found a significant relationship between the leukocyte profiles and parasite infection. Parasite infection was associated with elevated relative number of heterophils with simultaneous lowered relative number of lymphocytes. These opposite pattern resulted in an elevated H/L ratio in infected birds. Total leukocytes, lymphocytes and heterophils counts were elevated in birds infected with blood parasites as compared with those of non-infected ones. Leukocyte profiles of parasitized birds were similar regardless of individual age. However, non-infected adults had lower total leukocyte counts and values of H/L than non-infected immatures.

Ontogenetic changes in heterogeneity of parasite communities of fish: disentangling the relative role of compositional versus abundance variability

In order to determine how much of the variability in parasite assemblages is driven by differences in composition or in abundance we used multivariate dispersions (average distance from infracommunities to their size class centroid in the multivariate space) as a measurement of β-diversity in infracommunities of Conger orbignianus, applying a set of dissimilarity measures with different degrees of emphasis on composition versus relative abundance information. To evaluate comparatively the rate of such changes, we also analysed the effect of host size by regressing differences in β-diversity among size classes against differences in mean fish size. Multivariate dispersions varied along an ontogenetic gradient, its significance depending on the measurement used. Larger fish showed higher richness and abundance; however, smaller fish displayed lower variations in abundance but higher in composition. This could be caused by stochastic encounters at low densities due to the overdispersion of parasites in previous hosts. As fish grow, the composition of their parasite assemblages becomes homogenized by repeated exposure, with abundance thus arising as the main source of variability. Both variables act at different rates, with the exponential decay in the compositional variability as differences in fish size increase being about twice as steep as the decay in abundance variability, indicating that compositional homogeneity is reached faster than abundance heterogeneity as fish grow. Discerning between both variables is crucial in order to understand how community structure is formed by size-dependent variability of host populations.

The influence of host ecology and biogeography on the helminth species richness of freshwater fishes in Mexico

Freshwater fish helminths, the most well known Mexican vertebrate parasites, include approximately 260 species (platyhelminthes, acanthocephalans, nematodes, and hirudineans). The distribution patterns of adult helminth diversity (throughout parasite and host groups and hydrological regions) are described and the effects of host traits and environmental and geographical factors on diversity are evaluated. Adult helminths include 160 species, parasitizing 149 fish species of 23 families distributed in 21 regions. Nematoda was the most species-rich (>50 species). Cichlidae harboured rich helminth assemblages, with widespread parasites. By contrast, Atherinopsidae and Goodeidae showed relatively poor helminth assemblages, including specific parasites with narrow distribution. Helminth richness in southeastern Mexico was higher than northern or central regions. Non-parametric richness estimators were used to avoid confusion in comparisons with unequal sampling efforts. Bootstrap values, the method with the best performance, indicated that estimated richness shows the same distribution pattern that observed richness. Non-phylogenetic and phylogenetic analyses were used to determine the role of different factors in the parasite diversification. The distribution range was the most important richness predictor (widespread fishes harbour richer parasite assemblages), although interactions between this variable and others such as trophic level, latitude, habitat temperature and precipitation are also important. Likewise, biogeographical factors can also affect parasite diversity.

Nematode community structure in the brush-tailed rock-wallaby, Petrogale penicillata: Implications of captive breeding and the translocation of wildlife

Despite an increasing appreciation of the disease risks associated with wild-life translocations, the effects which captive breeding programs exert on parasite communities remain understudied. This may be attributed, in part, to the current lack of rapid and cost-effective techniques for comparing parasite assemblages between host populations. Terminal restriction fragment length polymorphism (T-RFLP) analysis of the rDNA region encompassing the internal transcribed spacers (ITS-1 and ITS-2) and 5.8S rRNA gene was used to characterise bursate nematode communities (suborder Strongylida) across two captive and two non-captive colonies of the threatened brush-tailed rock-wallaby, Petrogale penicillata. A clone library was constructed and a restriction enzyme selected to differentiate the predominant operational taxonomic units (OTUs) by the unique peak profiles they generated. The prevalence, intensity of infection and comparative structure of strongylid assemblages was evaluated for each of the host colonies. Compared to wild conspecifics, captive wallabies exhibited a reduced prevalence of infection and significantly lower faecal egg counts. T-RFLP revealed that a high proportion of the OTUs co-occurred across three of the four study locations. Despite this, the composition of strongylid assemblages was significantly different between the colonies, even when host translocation events had occurred. These results suggest that captive breeding programs may exert a profound impact on parasitic helminth assemblages. Developing efficient techniques for characterising community dynamics in potentially pathogenic organisms is critical to the long term success of species recovery efforts worldwide.

Patterns of diversity and abundance of fleas and mites in the Neotropics: host‐related, parasite‐related and environment‐related factors

The effects of host-related, parasite-related and environmental factors on the diversity and abundance of two ectoparasite taxa, fleas (Insecta: Siphonaptera) and mites (Acari: Mesostigmata), parasitic on small mammals (rodents and marsupials), were studied in different localities across Brazil. A stronger effect of host-related factors on flea than on mite assemblages, and a stronger effect of environmental factors on mite than on flea assemblages were predicted. In addition, the effects of parasite-related factors on flea and mite diversity and abundance were predicted to manifest mainly at the scale of infracommunities, whereas the effects of host-related and environmental factors were predicted to manifest mainly at the scale of component and compound communities. This study found that, in general, diversity and abundance of flea and mite assemblages at two lower hierarchical levels (infracommunities and component communities) were affected by host-related, parasite-related and environmental factors, and compound communities were affected mainly by host-related and environmental factors. The effects of factors differed between fleas and mites: in fleas, community structure and abundance depended on host diversity to a greater extent than in mites. In addition, the effects of factors differed among parasite assemblages harboured by different host species.

Parasites as indicators of movement and population connectivity of a non‐diadromous, tropical estuarine teleost: king threadfin Polydactylus macrochir

Temporal and spatial patterns in parasite assemblages were examined to evaluate the degree of movement and connectivity of post-recruitment life-history stages of a large, non-diadromous tropical estuarine teleost, king threadfin Polydactylus macrochir, collected from 18 locations across northern Australia. Ten parasites types (juvenile stages of two nematodes and seven cestodes, and adults of an acanthocephalan) were deemed to be suitable for use as biological tags, in that they were considered to have a long residence time in the fish, were relatively easy to find and were morphologically very different to each other which aided discrimination. Univariate and discriminant function analysis of these parasites revealed little difference in temporal replicates collected from five locations, suggesting that the parasite communities were stable over the timeframes explored. Univariate, discriminant function, and Bray-Curtis similarity analyses indicated significant spatial heterogeneity, with Bray-Curtis classification accuracies ranging from 55 to 100% for locations in north-western and northern Australia, 24 to 88% in the Gulf of Carpentaria, and 39 to 88% on the east coast of Queensland. Few differences were observed among locations separated by <200 km. The observed patterns of parasite infection are in agreement with concurrent studies of movement and connectivity of P. macrochir in that they indicate a complex population structure across northern Australia. These results should be considered when reviewing the management arrangements for this species.

Parasite diversity and coinfection determine pathogen infection success and host fitness

While the importance of changes in host biodiversity for disease risk continues to gain empirical support, the influence of natural variation in parasite diversity on epidemiological outcomes remains largely overlooked. Here, we combined field infection data from 2,191 amphibian hosts representing 158 parasite assemblages with mechanistic experiments to evaluate the influence of parasite richness on both parasite transmission and host fitness. Using a guild of larval trematode parasites (six species) and an amphibian host, our experiments contrasted the effects of parasite richness vs. composition, observed vs. randomized assemblages, and additive vs. replacement designs. Consistent with the dilution effect hypothesis extended to intrahost diversity, increases in parasite richness reduced overall infection success, including infections by the most virulent parasite. However, the effects of parasite richness on host growth and survival were context dependent; pathology increased when parasites were administered additively, even when the presence of the most pathogenic species was held constant, but decreased when added species replaced or reduced virulent species, emphasizing the importance of community composition and assembly. These results were similar or stronger when community structures were weighted by their observed frequencies in nature. The field data also revealed the highly nested structure of parasite assemblages, with virulent species generally occupying basal positions, suggesting that increases in parasite richness and antagonism in nature will decrease virulent infections. Our findings emphasize the importance of parasite biodiversity and coinfection in affecting epidemiological responses and highlight the value of integrating research on biodiversity and community ecology for understanding infectious diseases.

Geographical Patterns of Parasite Infracommunities in the Rough Scad, Trachurus lathami Nichols, in the Southwestern Atlantic Ocean

We assessed temporal variability in parasite infections of rough scad (Trachurus lathami) in 3 samples from Miramar (MI) in 2008, separated by periods of 1 mo, and 2 samples from Villa Gesell (VG), 1 each in 2008 and 2009 (Buenos Aires Province, Argentina), respectively. A sample was also obtained from Cabo Frio (CF) (Brazil) in 2009 to compare differences in parasite communities between fish from this locality and each Argentinean locality. All rough scad were parasitized by at least 1 of 27 parasite species. Similarity-based multivariate analysis revealed significant differences between localities, but temporal homogeneity in each Argentinean locality. Overall, prevalence and abundance of parasite species were most similar between samples from MI and VG, while the greatest differences occurred between samples from MI and CF. A canonical analysis of principal coordinates showed significant differences among samples. Grillotia carvajalregorum was the most important species in determining the position of Argentinean samples, especially those from MI, while Ectenurus virgulus , Raphidascaris sp., and Hysterothylacium sp. were the most important species related to fish from CF. The parasite assemblage of T. lathami showed a notable temporal persistence within the same locality and a high variability at the spatial scale, suggesting the existence of 3 independent stocks of T. lathami in South Atlantic waters.

The role of immigration and in‐situ radiation in explaining blood parasite assemblages in an island bird clade

Parasite communities on islands are assembled through multiple immigrations and/or in-situ diversification. In this study, we used a phylogenetic approach to investigate the role of such processes in shaping current patterns of diversity in Leucocytozoon, a group of haemosporidian blood parasites infecting whites eyes (Zosterops) endemic to the Mascarene archipelago (south-western Indian Ocean). We found that this parasite community arose through a combination of multiple immigrations and in-situ diversification, highlighting the importance of both processes in explaining island diversity. Specifically, two highly diverse parasite clades appear to have been present in the Mascarenes for most of their evolutionary history and have diversified within the archipelago, while another lineage apparently immigrated more recently, probably with human-introduced birds. Interestingly, the evolutionary histories of one clade of parasites and Indian Ocean Zosterops seem tightly associated with a significant signal for phylogenetic congruence, suggesting that host-parasite co-divergence may have occurred in this system.

Metazoan parasites on the gills of the skipjack tuna Katsuwonus pelamis (Osteichthyes: Scombridae) from the Alboran Sea (western Mediterranean Sea)

The gills of 31 skipjack tuna Katsuwonus pelamis (L.) caught in the Alboran Sea (western Mediterranean Sea) were examined for metazoan parasites, and the gills of 4 specimens from the Balearic Sea (also western Mediterranean Sea) were analysed for comparative purposes. Nine -species of parasites were found, including 8 didymozoid trematodes (Atalostrophion cf. bio-varium, Didymocylindrus filiformis, Didymocylindrus simplex, Didymocystis reniformis, Didymoproblema fusiforme, Didymozoon longicolle, Koellikeria sp. and Lobatozoum multisacculatum) and 1 caligid copepod (Caligus bonito). Koellikeria sp. and L. multisacculatum were not recorded in the Balearic Sea. Most of the parasites (79.2% of all specimens) were didymozoids. Didymozoon longicolle was the dominant species; A. cf. biovarium, D. simplex, D. fusiforme and L. multisacculatum are reported from the Mediterranean Sea for the first time. No correlation was found between the intensity of infection of any parasite species and host size or sex. Most of the parasites, particularly didymozoids, showed a high site-specificity. Significant differences were found between the parasite assemblages of K. pelamis from the Alboran Sea and from the Atlantic Ocean. D. fusiforme, D. longicolle and L. multisacculatum are suggested as potential tags to follow skipjack tuna migrations between the Atlantic Ocean and Mediterranean Sea.

Compositional and phylogenetic dissimilarity of host communities drives dissimilarity of ectoparasite assemblages: geographical variation and scale-dependence

We tested the hypothesis that compositional and/or phylogenetic dissimilarity of host assemblages affect compositional and/or phylogenetic dissimilarity of parasite assemblages, to different extents depending on scale, using regional surveys of fleas parasitic on small mammals from 4 biogeographical realms. Using phylogenetic community dissimilarity metric, we calculated the compositional and phylogenetic dissimilarity components between all pairs of host and parasite communities within realms and hemispheres. We then quantified the effect of compositional or phylogenetic dissimilarity in host regional assemblages, and geographical distance between assemblages, on the compositional or phylogenetic dissimilarity of flea regional assemblages within a realm, respectively. The compositional dissimilarity in host assemblages strongly affected compositional dissimilarity in flea assemblages within all realms and within both hemispheres. However, the effect of phylogenetic dissimilarity of host assemblages on that of flea assemblages was mostly confined to the Neotropics and Nearctic, but was detected in both the Old and New World at the higher scale, possibly because of phylogenetic heterogeneity in flea and host faunas between realms. The clearer effect of the compositional rather than the phylogenetic component of host community dissimilarity on flea community dissimilarity suggests important roles for host switching and ecological fitting during the assembly history of flea communities.