[Show abstract][Hide abstract] ABSTRACT: Parasites often have direct impacts on their host physiology or function, which can in turn have indirect effects on interspecific interactions and ecosystem structure. The present study investigates the effect of trematode parasite infection on the ecologically and commercially important venerid clam Austrovenus stutchburyi. Although the indirect impacts of clam infection on the broader benthic community, mediated by impaired burrowing of parasitized clams, have been well documented before, the more direct impacts on the clam itself remain poorly studied. The consequence of parasite infection on clam growth rate, mortality, body condition and foot length was quantified in a three-month laboratory experiment, in which juvenile clams were infected with varying levels of the echinostome trematode Curtuteria australis. Although mortality was unaffected by parasite infection, greater numbers of parasites deleteriously affected the growth rate, body condition and foot length of clams. This may result in delayed maturity and a lower filtration rate for infected individuals, as well as a reduced ability to bury into the sediment. Consequently, increased parasite infection not only has subsequent broader impacts on the surrounding ecological community, but can also affect the clam host directly and lower its value as a harvested species.
Journal of Experimental Marine Biology and Ecology 01/2016; 474:23 - 28. DOI:10.1016/j.jembe.2015.09.012 · 1.87 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Variations in levels of parasitism among individuals in a population of hosts underpin the importance of parasites as an evolutionary or ecological force. Factors influencing parasite richness (number of parasite species) and load (abundance and biomass) at the individual host level ultimately form the basis of parasite infection patterns. In fish, diet range (number of prey taxa consumed) and prey selectivity (proportion of a particular prey taxon in the diet) have been shown to influence parasite infection levels. However, fish diet is most often characterized at the species or fish population level, thus ignoring variation among conspecific individuals and its potential effects on infection patterns among individuals. Here, we examined parasite infections and stomach contents of New Zealand freshwater fish at the individual level. We tested for potential links between the richness, abundance and biomass of helminth parasites and the diet range and prey selectivity of individual fish hosts. There was no obvious link between individual fish host diet and helminth infection levels. Our results were consistent across multiple fish host and parasite species and contrast with those of earlier studies in which fish diet and parasite infection were linked, hinting at a true disconnect between host diet and measures of parasite infections in our study systems. This absence of relationship between host diet and infection levels may be due to the relatively low richness of freshwater helminth parasites in New Zealand and high host-parasite specificity.
[Show abstract][Hide abstract] ABSTRACT: Host-parasite checklists are essential resources in ecological parasitology, and are regularly used as sources of data in comparative studies of parasite species richness across host species, or of host specificity among parasite species. However, checklists are only useful datasets if they are relatively complete, that is, close to capturing all host–parasite associations occurring in a particular region. Here, we use three approaches to assess the completeness of 25 checklists of metazoan parasites in vertebrate hosts from various geographic regions. First, treating checklists as interaction networks between a set of parasite species and a set of host species, we identify networks with a greater connectance (proportion of realized host–parasite associations) than expected for their size. Second, assuming that the cumulative rise over time in the number of known host–parasite associations in a region tends toward an asymptote as their discovery progresses, we attempt to extrapolate the estimated total number of existing associations. Third, we test for a positive correlation between the number of published reports mentioning an association and the time since its first record, which is expected because observing and reporting host–parasite associations are frequency-dependent processes. Overall, no checklist fared well in all three tests, and only three of 25 passed two of the tests. These results suggest that most checklists, despite being useful syntheses of regional host–parasite associations, cannot be used as reliable sources of data for comparative analyses.
[Show abstract][Hide abstract] ABSTRACT: The ability to manipulate host behaviour is among the most fascinating and best-studied adaptations of parasites. In this opinion article, we highlight trends and biases in the study of this phenomenon that may cloud or limit our understanding of its evolution. For instance, reviews and theoretical studies have shown a disproportionately sharp increase in the past decade relative to empirical studies. We also discuss taxonomic biases in the host-parasite systems investigated, as well as recent declines in the use of experimental infections and in the proportion of these systems in which fitness benefits for the parasites have been confirmed. We finish this opinion article by offering recommendations for the continued success of research in this area.
Trends in Parasitology 10/2015; DOI:10.1016/j.pt.2015.07.002 · 6.20 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Species of Apatemon Szidat, 1928 and Australapatemon Sudarikov, 1959 are reported from New Zealand for the first time, and their life cycles are resolved using molecular sequence data (28S and ITS rDNA regions and mitochondrial COI). The metacercaria of Apatemon sp. 'jamiesoni' ex Gobiomorphus cotidianus and its cercaria ex Potamopyrgus antipodarum are described in detail. Its adult, found in Anas platyrhynchos and Phalacrocorax punctatus, is identified by molecular sequence data. Apatemon sp. 'jamiesoni' uses a different species of snail host, exhibits consistent differences in the genetic markers examined and its single described adult differs from known species so as to be considered distinct, but its formal description awaits additional adult specimens. Australapatemon niewiadomski n. sp. is described from Anas platyrhynchos. It is distinguished morphologically by the absence of a ringnapf and its overall smaller size compared to most other Australapatemon spp. except Au. magnacetabulum and Au. minor, which are smaller in nearly all features than the new species. Au. niewiadomski n. sp. metacercaria and its intermediate host (Barbronia weberi) are identified via matching of molecular sequence data. The status of Apatemon and Australapatemon as distinct genera is confirmed based on their respective monophyly, and genetic divergence between them is comparable to other well-established genera in the Strigeidae. The diagnosis of Australapatemon is emended. Life history data, accurate patterns of host specialisation and distribution, alongside concurrent molecular and morphological evidence would be useful for an integrative taxonomical approach towards the elucidation of species diversity in this group.
Parasitology Research 09/2015; DOI:10.1007/s00436-015-4744-0 · 2.10 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: When hosts experience environmental stress, the quantity and quality of resources they provide for parasites may be diminished, and host longevity may be decreased. Under stress, parasites may adopt alternative strategies to avoid fitness reductions. Trematode parasites typically have complex life cycles, involving asexual reproduction in a gastropod first intermediate host. A rare phenomenon, briefly mentioned in the literature, and termed 'precocious encystment' involves the next stage in the parasites' life cycle (metacercarial cyst) forming within the preceding stage (redia), while still inside the snail. In the trematode Parorchis sp. NZ using rocky shore snails exposed to long periods outside water, we hypothesised this might be an adaptive strategy against desiccation, preventing parasite emergence from the snail. To test this, we first investigated the effect of prolonged desiccation on the survival of two species of high intertidal snails. Secondly, we measured the reproductive output (cercarial production) of the parasite under wet and dry conditions. Finally, we quantified the influence of desiccation stress on the occurrence of precocious encystment. Snail mortality was higher under dry conditions, indicating stress, and it was somewhat exacerbated for infected snails. Parasite reproductive output differed between wet and dry conditions, with parasites of snails kept in dry conditions producing more cercariae when placed in water. Little variation was observed in the occurrence of precocious encystment, although some subtle patterns emerged. Given the stresses associated with living in high intertidal environments, we discuss precocious encystment as a possible stress response in this trematode parasite.
Parasitology International 09/2015; 64(6). DOI:10.1016/j.parint.2015.09.001 · 1.86 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: In many host–parasite systems, infection risk can be reduced by high local biodiversity, though the mitigating effects of diversity are context dependent and not universal.In aquatic ecosystems, local fauna can reduce the transmission success of parasite free-swimming infective stages by preying on them, acting as decoy hosts, or physically interfering with transmission. However, most prior research has focused on the effect of a single non-host organism at a time and/or has been performed under simplified and artificial conditions.Here, using data on 11 trematode species sampled in different New Zealand lakes, we test whether local biodiversity affects infection risk in target second intermediate hosts, as well as total parasite population size (number of parasites per m2), under natural conditions. We considered four components of local biodiversity: total biomass of non-host fish species, diversity (Simpson index) of non-host benthic invertebrates, total density of zooplankton and macrophyte biomass. Our analyses also accounted for host density, a known determinant of parasite prevalence, intensity of infection and total parasite population density.The only influence of local biodiversity we detected was a negative effect of the diversity of non-host benthic invertebrates on the prevalence achieved by trematodes in their second intermediate hosts: that is, the proportion of individual hosts that are infected. Interestingly, this effect was discernible in all 11 trematode species considered here, even if very weak within some species.Our findings suggest that higher non-host benthic diversity may generally decrease infection risk for target hosts including snails, arthropods and fish. However, reduced infection success did not automatically mean smaller overall parasite population size, as other factors can maintain the parasite population in the face of high local diversity of non-hosts.
[Show abstract][Hide abstract] ABSTRACT: The standing crop biomass of different populations or trophic levels reflects patterns of energy flow through an ecosystem. The contribution of parasites to total biomass is often considered negligible; recent evidence suggests otherwise, although it comes from a narrow range of natural systems. Quantifying how local parasite biomass, whether that of a single species or an assemblage of species sharing the same host, varies across localities with host population biomass, is critical to determine what constrains parasite populations. We use an extensive dataset on all free-living and parasitic metazoan species from multiple sites in New Zealand lakes to measure parasite biomass and test how it covaries with host biomass. In all lakes, trematodes had the highest combined biomass among parasite taxa, ranging from about 0.01 to 0.25 g m−2, surpassing the biomass of minor free-living taxa. Unlike findings from other studies, the life stage contributing the most to total trematode biomass was the metacercarial stage in the second intermediate host, and not sporocysts or rediae within snail first intermediate hosts, possibly due to low prevalence and small snail sizes. For populations of single parasite species, we found no relationship between host and parasite biomass for either juvenile or adult nematodes. In contrast, all life stages of trematodes had local biomasses that correlated positively with those of their hosts. For assemblages of parasite species sharing the same host, we found strong relationships between local host population biomass and the total biomass of parasites supported. In these host–parasite biomass relationships, the scaling factor (slope in log-log space) suggests that parasites may not be making full use of available host resources. Host populations appear capable of supporting a little more parasite biomass, and may be open to expansion of existing parasites or invasion by new ones.
[Show abstract][Hide abstract] ABSTRACT: Within any parasite species, abundance varies spatially, reaching higher values in certain localities than in others, presumably reflecting the local availability of host resources or the local suitability of habitat characteristics for free-living stages. In the absence of strong interactions between two species of helminths with complex life cycles, we might predict that the degree to which their abundances covary spatially is determined by their common resource requirements, i.e. how many host species they share throughout their life cycles. We test this prediction using five trematode species, all with a typical three-host cycle, from multiple lake sampling sites in New Zealand's South Island: Stegodexamene anguillae, Telogaster opisthorchis, Coitocaecum parvum, Maritrema poulini, and an Apatemon sp. Pairs of species from this set of five share the same host species at either one, two, or all three life cycle stages. Our results show that when two trematode species share the same host species at all three life stages, they show positive spatial covariation in abundance (of metacercarial and adult stages) across localities. When they share hosts at two life stages, they show positive spatial covariation in abundance in some cases but not others. Finally, if two trematode species share only one host species, at a single life stage, their abundances do not covary spatially. These findings indicate that the extent of resource sharing between parasite species can drive the spatial match-mismatch between their abundances, and thus influence their coevolutionary dynamics and the degree to which host populations suffer from additive or synergistic effects of multiple infections.
Parasitology Research 06/2015; 114(10). DOI:10.1007/s00436-015-4590-0 · 2.10 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Zooplankton and phytoplankton communities play host to a wide diversity of parasites, which have been found to play a significant role in a number of ecosystem processes, such as facilitating energy transfer and promoting species succession through altering interspecific competition. Yet we know little about the mechanisms that drive parasite dynamics in aquatic ecosystems. Recent mathematical models have shown how habitat can shape parasite dynamics through influencing the efficacy of parasite transmission; however, these predictions have yet to be tested at larger ecological scales. Here, we present a comparative analysis of parasitism in planktonic communities, assembling data from a range of host and parasite taxa, habitat types, and geographic regions. Our results suggest that the prominent depth-prevalence relationship observed in studies on Daphnia in temperate lakes of North America is applicable to a wide range of aquatic habitats, hosts, and parasites; however, differences in transmission strategies between parasites can lead to considerable variation in parasite dynamics. Observational studies which incorporate a diversity of habitat types will be important in uncovering the mechanisms which underlie this relationship. In particular, more experimental work on transmission stage survivability and infectivity in aquatic environments will be necessary before we can make accurate predictive models of parasite spread in these ecosystems.
[Show abstract][Hide abstract] ABSTRACT: Theory predicts the bottom–up coupling of resource and consumer densities, and epidemiological models make the same prediction for host–parasite interactions. Empirical evidence that spatial variation in local host density drives parasite population density remains scarce, however. We test the coupling of consumer (parasite) and resource (host) populations using data from 310 populations of metazoan parasites infecting invertebrates and fish in New Zealand lakes, spanning a range of transmission modes. Both parasite density (no. parasites per m2) and intensity of infection (no. parasites per infected hosts) were quantified for each parasite population, and related to host density, spatial variability in host density and transmission mode (egg ingestion, contact transmission or trophic transmission). The results show that dense and temporally stable host populations are exploited by denser and more stable parasite populations. For parasites with multi-host cycles, density of the ‘source’ host did not matter: only density of the current host affected parasite density at a given life stage. For contact-transmitted parasites, intensity of infection decreased with increasing host density. Our results support the strong bottom–up coupling of consumer and resource densities, but also suggest that intraspecific competition among parasites may be weaker when hosts are abundant: high host density promotes greater parasite population density, but also reduces the number of conspecific parasites per individual host.
[Show abstract][Hide abstract] ABSTRACT: The fundamental assumption underpinning the evolution of numerous adaptations shown by parasites with complex life cycles is that huge losses are incurred by infective stages during certain transmission steps. However, the magnitude of transmission losses or changes in the standing crop of parasites passing from upstream (source) to downstream (target) hosts have never been quantified in nature. Here, using data from 100 pairs of successive upstream–downstream life stages, from distinct populations representing 10 parasite species, we calculated the total density per m
of successive life stages. We show that clonal amplification of trematodes in their first intermediate host leads to an average 4-fold expansion of numbers of individuals at the next life stage, when differences in the longevity of successive life stages are taken into account. In contrast, trophic transmission to the definitive host results in almost no numerical change for trematodes, but possibly in large decreases for acanthocephalans and nematodes, though a correction for longevity was not possible for the latter groups. Also, we only found a positive association between upstream and downstream stage densities for transmission involving free-swimming cercariae in trematodes, suggesting a simple output-recruitment process. For trophic transmission, there was no coupling between downstream and upstream parasite densities. These first quantitative estimates of ontogenetic rises and falls in numbers under natural conditions provide new insights into the selective pressures acting on parasites with complex cycles.
[Show abstract][Hide abstract] ABSTRACT: How do the lifestyles (free-living unparasitized, free-living parasitized, and parasitic) of animal species affect major ecological power-law relationships? We investigated this question in metazoan communities in lakes of Otago, New Zealand. In 13,752 samples comprising 1,037,058 organisms, we found that species of different lifestyles differed in taxonomic distribution and body mass and were well described by three power laws: a spatial Taylor's law (the spatial variance in population density was a power-law function of the spatial mean population density); density-mass allometry (the spatial mean population density was a power-law function of mean body mass); and variance-mass allometry (the spatial variance in population density was a power-law function of mean body mass). To our knowledge, this constitutes the first empirical confirmation of variance-mass allometry for any animal community. We found that the parameter values of all three relationships differed for species with different lifestyles in the same communities. Taylor's law and density-mass allometry accurately predicted the form and parameter values of variance-mass allometry. We conclude that species of different lifestyles in these metazoan communities obeyed the same major ecological power-law relationships but did so with parameters specific to each lifestyle, probably reflecting differences among lifestyles in population dynamics and spatial distribution.
Proceedings of the National Academy of Sciences 12/2014; 112(6). DOI:10.1073/pnas.1422475112 · 9.67 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Despite their very different historical origins as scientific disciplines, parasitology and marine ecology have already combined successfully to make important contributions to our understanding of the functioning of natural ecosystems. For example, robust assessments of the contribution of parasites to ecosystem biomass and energetics, and of their impact on community-wide biodiversity and food web structure, have all been made for the first time in marine systems. Nevertheless, for the marriage between parasitology and marine ecology to remain fruitful, several challenges must first be overcome. We discuss seven such challenges on the road to a greater synergy between these disciplines: (1) Raising awareness of parasitism as an ecological force by increasing the proportion of articles about parasites and diseases in marine ecology journals; (2) Making greater use of theory and conceptual frameworks from marine ecology to guide parasitological research; (3) Speeding up or at least maintaining the current rate at which marine parasites are found and described; (4) Elucidating a greater proportion of life cycles in all major groups of marine parasites; (5) Increasing the number of host-parasite model systems on which our knowledge is based; (6) Extending parasitological research offshore and into ocean depths; (7) Developing, as needed, new epidemiological theory and transmission models for the marine environment. None of these challenges is insurmountable, and addressing just a few of them should guarantee that parasitology and marine ecology will continue to join forces and make further substantial contributions.
Journal of Sea Research 11/2014; in press(on-line). DOI:10.1016/j.seares.2014.10.019 · 1.99 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: 1. Meta-analysis has become a standard way of summarizing empirical studies in many fields, including ecology and evolution. In ecology and evolution, meta-analyses comparing two groups (usually experimental and control groups) have almost exclusively focused on comparing the means, using standardized metrics such as Cohen's / Hedges’ d or the response ratio.2. However, an experimental treatment may not only affect the mean but also the variance. Investigating differences in the variance between two groups may be informative, especially when a treatment influences the variance in addition to or instead of the mean.3. In this paper, we propose the effect size statistic, lnCVR (the natural logarithms of the ratio between the coefficients of variation, CV, from two groups), which enables us to meta-analytically compare differences between the variability of two groups. We illustrate the use of lnCVR with examples from ecology and evolution.4. Further, as an alternative approach to the use of lnCVR, we propose the combined use of (the log standard deviation) and (the log mean) in a hierarchical (linear mixed) model. The use of with overcomes potential limitations of lnCVR and it provides a more flexible, albeit more complex, way to examine variation beyond two group comparisons. Relevantly, we also refer to the potential use of and lnCV (the log CV) in the context of comparative analysis.5. Our approaches to compare variability could be applied to already published meta-analytic datasets that compare two-group means to uncover potentially overlooked effects on the variance. Additionally, our approaches should be applied to future meta-analyses, especially when one suspects a treatment has an effect not only on the mean, but also on the variance. Notably, the application of the proposed methods extends beyond the fields of ecology and evolution.This article is protected by copyright. All rights reserved.
Methods in Ecology and Evolution 11/2014; 6(2). DOI:10.1111/2041-210X.12309 · 6.55 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Littorinid snails are one particular group of gastropods identified as important intermediate hosts for a wide range of digenean parasite species, at least throughout the Northern Hemisphere. However nothing is known of trematode species infecting these snails in the Southern Hemisphere. This study is the first attempt at cataloguing the digenean parasites infecting littorinids in New Zealand. Examination of over 5,000 individuals of two species of the genus Austrolittorina Rosewater, A. cincta Quoy & Gaimard and A. antipodum Philippi, from intertidal rocky shores, revealed infections with four digenean species representative of a diverse range of families: Philophthalmidae Looss, 1899, Notocotylidae Lühe, 1909, Renicolidae Dollfus, 1939 and Microphallidae Ward, 1901. This paper provides detailed morphological descriptions of the cercariae and intramolluscan stages of these parasites. Furthermore, partial sequences of the 28S rRNA gene and the mitochondrial gene cytochrome c oxidase subunit 1 (cox1) for varying numbers of isolates of each species were obtained. Phylogenetic analyses were carried out at the superfamily level and along with the morphological data were used to infer the generic affiliation of the species.
[Show abstract][Hide abstract] ABSTRACT: For rocky shore gastropods, attachment strength is a key determinant of survival, as getting dislodged by wave action or predators has negative consequences. Yet little is known of the factors that cause inter-individual variation in attachment strength among conspecifics. Here, we test the influence of trematode infection on the suction-mediated attachment strength of periwinkles from two New Zealand species, Austrolittorina cincta and A. antipodum. Using a standardised experimental protocol, we measured both the strength of attachment of individual snails to the substrate, and its repeatability, i.e. the consistency of measurements taken on different occasions on the same individuals. We then compared the attachment of snails infected with a philophthalmid trematode with that of their uninfected conspecifics. First, we found that for a given snail mass, infected snails were easier to detach from the substrate than the uninfected ones, although this pattern was only significant for A. cincta, the larger of the two snail species. Second, the repeatability of attachment strength measurements per individual snail did not differ between infected and uninfected conspecifics, for either of the two periwinkle species. Our findings show that parasitism can weaken snail attachment, and indirectly increase snail mortality, on exposed rocky shores, suggesting a new way in which parasites can affect host population dynamics.
Journal of Experimental Marine Biology and Ecology 09/2014; 458:1–5. DOI:10.1016/j.jembe.2014.04.022 · 1.87 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: SUMMARY Host specificity is a fundamental component of a parasite's life history. However, accurate assessments of host specificity, and the factors influencing it, can be obscured by parasite cryptic species complexes. We surveyed two congeneric species of intertidal snail intermediate hosts, Zeacumantus subcarinatus and Zeacumantus lutulentus, throughout New Zealand to identify the number of genetically distinct echinostome trematodes infecting them and determine the levels of snail host specificity among echinostomes. Two major echinostome clades were identified: a clade consisting of an unidentified species of the subfamily Himasthlinae and a clade consisting of five species of the genus Acanthoparyphium. All five Acanthoparyphium species were only found in a single snail species, four in Z. subcarinatus and one in Z. lutulentus. In contrast, the Himasthlinae gen. sp. was found in both hosts, but was more prevalent in Z. lutulentus (97 infections) than Z. subcarinatus (10 infections). At least two of the Acanthoparyphium spp. and the Himasthlinae gen. sp. are widespread throughout New Zealand, and can therefore encounter both snail species. Our results suggest that host specificity is determined by host-parasite incompatibilities, not geographic separation, and that it can evolve in different ways in closely related parasite lineages.