Impacts of crustacean invasions on parasite dynamics in aquatic ecosystems: A plea for parasite-focused studies

While there is considerable interest in, and good evidence for, the role that parasites play in biological invasions, the potential parallel effects of species introduction on parasite dynamics have clearly received less attention. Indeed, much effort has been focused on how parasites can facilitate or limit invasions, and positively or negatively impact native host species and recipient communities. Contrastingly, the potential consequences of biological invasions for the diversity and dynamics of both native and introduced parasites have been and are still mainly overlooked, although successful invasion by non-native host species may have large, contrasting and unpredictable effects on parasites. This review looks at the links between biological invasions and pathogens, and particularly at crustacean invasions in aquatic ecosystems and their potential effects on native and invasive parasites, and discusses what often remains unknown even from well-documented systems. Aquatic crustaceans are hosts to many parasites and are often invasive. Published studies show that crustacean invasion can have highly contrasting effects on parasite dynamics, even when invasive host and parasite species are phylogenetically close to their native counterparts. These effects seem to be dependent on multiple factors such as host suitability, parasite life-cycle or host-specific resistance to parasitic manipulation. Furthermore, introduced hosts can have drastically contrasting effects on parasite standing crop and transmission, two parameters that should be independently assessed before drawing any conclusion on the potential effects of novel hosts on parasites and the key processes influencing disease dynamics following biological invasions. I conclude by calling for greater recognition of biological invasions’ effects on parasite dynamics, more parasite-focused studies and suggest some potential ways to assess these effects. Keywords: Invasive species, Spillover, Spillback, Crustacean, Amphipod, Complex life cycle, Parasite transmissio

Effects of temperature on persistence times of native and invasive gammarid species in the stomachs of Cottus gobio.

5 pagesInternational audienc

Data from: Bottom-up regulation of parasite population densities in freshwater ecosystems

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

Data from: The scaling of parasite biomass with host biomass in lake ecosystems: are parasites limited by host resources?

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

Evolution, phylogenetic distribution and functional ecology of division of labour in trematodes

Abstract Division of labour has evolved in many social animals where colonies consist of clones or close kin. It involves the performance of different tasks by morphologically distinct castes, leading to increased colony fitness. Recently, a form of division of labour has been discovered in trematodes: clonal rediae inside the snail intermediate host belong either to a large-bodied reproductive caste, or to a much smaller and morphologically distinct ‘soldier’ caste which defends the colony against co-infecting trematodes. We review recent research on this phenomenon, focusing on its phylogenetic distribution, its possible evolutionary origins, and how division of labour functions to allow trematode colonies within their snail host to adjust to threats and changing conditions. To date, division of labour has been documented in 15 species from three families: Himasthlidae, Philophthalmidae and Heterophyidae. Although this list of species is certainly incomplete, the evidence suggests that division of labour has arisen independently more than once in the evolutionary history of trematodes. We propose a simple scenario for the gradual evolution of division of labour in trematodes facing a high risk of competition in a long-lived snail host. Starting with initial conditions prior to the origin of castes (size variation among rediae within a colony, size-dependent production of cercariae by rediae, and a trade-off between cercarial production and other functions, such as defence), maximising colony fitness (R 0) can lead to caste formation or the age-structured division of labour observed in some trematodes. Finally, we summarise recent research showing that caste ratios, i.e. relative numbers of reproductive and soldier rediae per colony, become more soldier-biased in colonies exposed to competition from another trematode species sharing the same snail, and also respond to other stressors threatening the host’s survival or the colony itself. In addition, there is evidence of asymmetrical phenotypic plasticity among individual caste members: reproductives can assume defensive functions against competitors in the absence of soldiers, whereas soldiers are incapable of growing into reproductives if the latter’s numbers are reduced. We conclude by highlighting future research directions, and the advantages of trematodes as model systems to study social evolution

Data from: Save your host, save yourself? caste-ratio adjustment in a parasite with division of labor and snail host survival following shell damage

Shell damage and parasitic infections are frequent in gastropods, influencing key snail host life-history traits such as survival, growth, and reproduction. However, their interactions and potential effects on hosts and parasites have never been tested. Host–parasite interactions are particularly interesting in the context of the recently discovered division of labor in trematodes infecting marine snails. Some species have colonies consisting of two different castes present at varying ratios; reproductive members and nonreproductive soldiers specialized in defending the colony. We assessed snail host survival, growth, and shell regeneration in interaction with infections by two trematode species, Philophthalmus sp. and Maritrema novaezealandense, following damage to the shell in the New Zealand mud snail Zeacumantus subcarinatus. We concomitantly assessed caste-ratio adjustment between nonreproductive soldiers and reproductive members in colonies of the trematode Philophthalmus sp. in response to interspecific competition and shell damage to its snail host. Shell damage, but not parasitic infection, significantly increased snail mortality, likely due to secondary infections by pathogens. However, trematode infection and shell damage did not negatively affect shell regeneration or growth in Z. subcarinatus; infected snails actually produced more new shell than their uninfected counterparts. Both interspecific competition and shell damage to the snail host induced caste-ratio adjustment in Philophthalmus sp. colonies. The proportion of nonreproductive soldiers increased in response to interspecific competition and host shell damage, likely to defend the parasite colony and potentially the snail host against increasing threats. These results indicate that secondary infections by pathogens following shell damage to snails both significantly increased snail mortality and induced caste-ratio adjustments in parasites. This is the first evidence that parasites with a division of labor may be able to produce nonreproductive soldiers according to environmental factors other than interspecific competition with other parasites

Mean Biomass of parasitic and free-living taxa from 4 lakes

Mean Biomass of all metazoan parasitic and free-living taxa from 4 lakes in New Zealan

Variations in infection levels and parasite-induced mortality among sympatric cryptic lineages of native amphipods and a congeneric invasive species: Are native hosts always losing?

Shared parasites can strongly influence the outcome of competition between congeneric, sympatric hosts, and thus host population dynamics. Parasite-mediated competition is commonly hypothesized as an important factor in biological invasion success; invasive species often experience lower infection levels and/or parasite-induced mortality than native congeneric hosts. However, variation in infection levels among sympatric hosts can be due to contrasting abilities to avoid infection or different parasite-induced mortality rates following infection. Low parasite infection levels in a specific host can be due to either factor but have drastically different implications in interaction outcomes between sympatric hosts.We assessed acanthocephalan infection levels (prevalence and abundance) among cryptic molecular taxonomic units (MOTU) of the native G. pulex/G. fossarum species complex from multiple populations where they occur in sympatry. We concomitantly estimated the same parameters in the invasive Gammarus roeseli commonly found in sympatry with G. pulex/G. fossarum MOTUs. We then tested for potential differences in parasite-induced mortality among these alternative hosts. As expected, the invasive G. roeseli showed relatively low infection level and was not subject to parasite-induced mortality. We also found that both acanthocephalan infection levels and parasite-induced mortality varied greatly among cryptic MOTUs of the native amphipods. Contrary to expectations, some native MOTUs displayed levels of resistance to their local parasites similar to those observed in the invasive G. roeseli. Overall, cryptic diversity in native amphipods coupled with high levels of variability in infection levels and parasite-induced mortality documented here may strongly influence inter-MOTU interactions and native population dynamics as well as invasion success and population dynamics of the congeneric invasive G. roeseli. Keywords: Biological invasion, Cryptic diversity, Gammarus fossarum/Gammarus pulex species complex, Gammarus roeseli, Acanthocephalan parasites, Infection levels, Parasite-induced mortalit

Cryptic diversity, mate discrimination and cannibalism among amphipod lineages: if you can’t mate with them, eat them!

International audienc

Manipulative parasites may not alter intermediate host distribution but still enhance their transmission: field evidence for increased vulnerability to definitive hosts and non-host predator avoidance.

8 pagesInternational audienceBehavioural alterations induced by parasites in their intermediate hosts can spatially structure host populations, possibly resulting in enhanced trophic transmission to definitive hosts. However, such alterations may also increase intermediate host vulnerability to non-host predators. Parasite-induced behavioural alterations may thus vary between parasite species and depend on each parasite definitive host species. We studied the influence of infection with 2 acanthocephalan parasites (Echinorhynchus truttae and Polymorphus minutus) on the distribution of the amphipod Gammarus pulex in the field. Predator presence or absence and predator species, whether suitable definitive host or dead-end predator, had no effect on the micro-distribution of infected or uninfected G. pulex amphipods. Although neither parasite species seem to influence intermediate host distribution, E. truttae infected G. pulex were still significantly more vulnerable to predation by fish (Cottus gobio), the parasite's definitive hosts. In contrast, G. pulex infected with P. minutus, a bird acanthocephalan, did not suffer from increased predation by C. gobio, a predator unsuitable as host for P. minutus. These results suggest that effects of behavioural changes associated with parasite infections might not be detectable until intermediate hosts actually come in contact with predators. However, parasite-induced changes in host spatial distribution may still be adaptive if they drive hosts into areas of high transmission probabilities