Global analysis of seasonal changes in trematode infection levels reveals weak and variable link to temperature.

Seasonal changes in environmental conditions drive phenology, i.e., the annual timing of biological events ranging from the individual to the ecosystem. Phenological patterns and successional abundance cycles have been particularly well studied in temperate freshwater systems, showing strong and predictable synchrony with seasonal changes. However, seasonal successional changes in the abundance of parasites or their infection levels in aquatic hosts have not yet been shown to follow universal patterns. Here, using a compilation of several hundred estimates of spring-to-summer changes in infection by trematodes in their intermediate and definitive hosts, spanning multiple species and habitats, we test for general patterns of seasonal (temperature) driven changes in infection levels. The data include almost as many decreases in infection levels from spring to summer as there are increases, across different host types. Our results reveal that the magnitude of the spring-to-summer change in temperature had a weak positive effect on the concurrent change in prevalence of infection in first intermediate hosts, but no effect on the change in prevalence or abundance of infection in second intermediate or definitive hosts. This was true across habitat types and host taxa, indicating no universal effect of seasonal temperature increase on trematode infections. This surprising variation across systems suggests a predominance of idiosyncratic and species-specific responses in trematode infection levels, at odds with any clear phenological or successional pattern. We discuss possible reasons for the minimal and variable effect of seasonal temperature regimes, and emphasise the challenges this poses for predicting ecosystem responses to future climate change.

Molecular quantification of parasitic sea louse larvae depends on species and life stage.

Sea lice cause substantial economic and environmental harm to Norway's aquaculture industry and wild salmonid populations. Rapid, accurate quantification of lice larval densities in coastal waters remains the greatest bottleneck for providing empirical data on infestation risk within wild salmon habitats and aquaculture production regions. We evaluated the capability of droplet digital PCR (ddPCR) as an absolute quantification method for the planktonic stages of two parasitic louse species, Lepeophtheirus salmonis (Krøyer) and Caligus elongatus (von Nordman). Results demonstrated linear relationships between the DNA quantity measured and the number of spiked larvae for both species and life stages. However, L. salmonis contained a significantly greater number of DNA copies than C. elongatus individuals and for C. elongatus, nauplii displayed a significantly higher number of DNA copies than copepodids. Our results suggest that ddPCR can effectively enumerate louse larvae, but interpreting ddPCR results differ between the two louse species. Obtaining larval abundance estimates from marine plankton samples will depend on the nauplii to copepodid ratio for C. elongatus, but not for L. salmonis.

Temporal stability of polymorphic Arctic charr parasite communities reflects sustained divergent trophic niches.

Polymorphic Arctic charr Salvelinus alpinus populations frequently display distinct differences in habitat use, diet, and parasite communities. Changes to the relative species densities and composition of the wider fish community have the potential to alter the habitat niche of sympatric Arctic charr populations. This study evaluated the temporal stability of the parasite community, diet, and stable isotopes (δ13C, δ15N) of three sympatric Arctic charr morphs (piscivore, benthivore, and planktivore) from Loch Rannoch, Scotland, in relation to changes to the fish community. All Arctic charr morphs displayed distinct differences in parasite communities, diet, and stable isotope signatures over time, despite the establishment of four new trophically transmitted parasite taxa, and increased fish and zooplankton consumption by the piscivorous and planktivore morphs, respectively. Native parasite prevalence also increased in all Arctic charr morphs. Overall, Loch Rannoch polymorphic Arctic charr morph populations have maintained their distinct trophic niches and parasite communities through time despite changes in the fish community. This result indicates that re-stocking a native fish species has the potential to induce shifts in the parasite community and diet of Arctic charr morphs.

Factors influencing return rate and marine residence duration in sea trout populations in Central Norway.

Brown trout (Salmo trutta) display extensive plasticity in marine migratory behaviours, with marine migrations considered to be an adaptive strategy which enables sea trout to maximize growth and reproductive potential. However, marine migrations are not without associated costs, including threats posed by ever-increasing salmon lice (Lepeophtheirus salmonis) infestations. In the present study, we used passive integrated transponder technology to characterize variability in sea trout migration behaviour amongst three catchments situated in a region of intensive salmon farming in central Norway. Specifically, we investigate how lice infestation, out-migration date and body size alter sea trout return rate and marine residence duration during the first out-migration to sea from each catchment. Distinct catchment-specific differences in sea trout out-migration size and the number of cohorts were observed, but larger body size did not guarantee the successful return of migrating trout. The marine residence duration of individuals that successfully returned to freshwater was positively correlated with lice infestation risk, suggesting for these individuals the lethal infestation threshold had not been reached. Our results also suggest that sea trout populations from lotic-dominated catchments are potentially at greater risk from size-related threats to their survival encountered during their marine migrations than sea trout from lentic-dominated catchments. The variability in sea trout migratory behaviour amongst catchments observed here emphasizes the challenges fisheries managers face when deciding the best actions to take to protect the anadromous portion of brown trout populations.

Cercarial behaviour alters the consumer functional response of three-spined sticklebacks.

Free-living parasite life stages may contribute substantially to ecosystem biomass and thus represent a significant source of energy flow when consumed by non-host organisms. However, ambient temperature and the predator's own infection status may modulate consumption rates towards parasite prey. We investigated the combined effects of temperature and predator infection status on the consumer functional response of three-spined sticklebacks towards the free-living cercariae stages of two common freshwater trematode parasites (Plagiorchis spp., Trichobilharzia franki). Our results revealed genera-specific functional responses and consumption rates towards each parasite prey: Type II for Plagiorchis spp. and Type III for T. franki, with an overall higher consumption rate on T. franki. Elevated temperature (13°C) increased the consumption rate on Plagiorchis spp. prey for sticklebacks with mild cestode infections (<5% fish body weight) only. High consumption of cercarial prey by sticklebacks may impact parasite population dynamics by severely reducing or even functionally eliminating free-living parasite life stages from the environment. This supports the potential role of fish as biocontrol agents for cercariae with similar dispersion strategies, in instances where functional response relationships have been established. Our study demonstrates how parasite consumption by non-host organisms may be shaped by traits inherent to parasite transmission and dispersal, and emphasises the need to consider free-living parasite life stages as integral energy resources in aquatic food webs.

Temperature does not influence functional response of amphipods consuming different trematode prey.

Direct consumption on free-living cercariae stages of trematodes by non-host organisms interferes with trematode transmission and leads to reduced infections in the next suitable hosts. Consumer functional responses provide a useful tool to examine relationships between consumption rates and ecologically relevant prey densities, whilst also accounting for abiotic factors that likely influence consumption rates. We investigated how temperature influences the consumer functional response of the amphipod Gammarus lacustris towards the cercariae of three freshwater trematodes (Diplostomum, Apatemon and Trichobilharzia). Amphipods displayed different functional responses towards the parasites, with Type II responses for Diplostomum and Type I responses for Apatemon prey. Temperature did not alter the consumption rate of the amphipod predator. Trichobilharzia was likely consumed at similar proportions as Diplostomum; however, this could not be fully evaluated due to low replication. Whilst Type II responses of invertebrate predators are common to various invertebrate prey types, this is the first time a non-filter feeding predator has been shown to exhibit Type I response towards cercarial prey. The prey-specific consumption patterns of amphipods were related to cercarial distribution in the water column rather than to the size of cercariae or temperature influence. The substantial energy flow into food webs by non-host consumer organisms highlights the importance of understanding the mechanisms that modulate functional responses and direct predation in the context of parasitic organisms.

Alpine bullhead (Cottus poecilopus Heckel): a potential refuge for Gyrodactylus salaris Malmberg, 1957 (Monogenea).

The notifiable freshwater pathogen Gyrodactylus salaris Malmberg, 1957 tends to be a generalist in contrast to other monogeneans. Whilst it causes most damage to its primary host, the Atlantic salmon (Salmo salar Linnaeus), transport and reservoir hosts likely play a key role in maintaining the parasite in the environment. Here, we tested the ability of G. salaris (strain River Lierelva, southern Norway) to infect and reproduce on a population of wild caught alpine bullhead (Cottus poecilopus Heckel). Exposure of alpine bullhead yearlings (0+) to G. salaris for 24 h at low (6.5 °C) or high temperature (11.5 °C) resulted in the establishment of 1 to 104 parasites per fish. Eight to nine days post-infection at high temperature, the infection of G. salaris was eliminated, indicative of innate host immunity. In contrast, at low temperature G. salaris infections persisted for 47-48 days. The relative lengthy infection of alpine bullhead with G. salaris compared to other non-salmonids tested may be due to low temperature and high initial infection load in combination with an epibiont infection. The present results suggest that this non-salmonid may function as a temperature-dependent transport or reservoir host for G. salaris.

Predicting invasive species impacts: a community module functional response approach reveals context dependencies.

Predatory functional responses play integral roles in predator-prey dynamics, and their assessment promises greater understanding and prediction of the predatory impacts of invasive species. Other interspecific interactions, however, such as parasitism and higher-order predation, have the potential to modify predator-prey interactions and thus the predictive capability of the comparative functional response approach. We used a four-species community module (higher-order predator; focal native or invasive predators; parasites of focal predators; native prey) to compare the predatory functional responses of native Gammarus duebeni celticus and invasive Gammarus pulex amphipods towards three invertebrate prey species (Asellus aquaticus, Simulium spp., Baetis rhodani), thus, quantifying the context dependencies of parasitism and a higher-order fish predator on these functional responses. Our functional response experiments demonstrated that the invasive amphipod had a higher predatory impact (lower handling time) on two of three prey species, which reflects patterns of impact observed in the field. The community module also revealed that parasitism had context-dependent influences, for one prey species, with the potential to further reduce the predatory impact of the invasive amphipod or increase the predatory impact of the native amphipod in the presence of a higher-order fish predator. Partial consumption of prey was similar for both predators and occurred increasingly in the order A. aquaticus, Simulium spp. and B. rhodani. This was associated with increasing prey densities, but showed no context dependencies with parasitism or higher-order fish predator. This study supports the applicability of comparative functional responses as a tool to predict and assess invasive species impacts incorporating multiple context dependencies.

Relative competence of native and exotic fish hosts for two generalist native trematodes.

Exotic fish species frequently acquire native parasites despite the absence of closely related native hosts. They thus have the potential to affect native counterparts by altering native host-parasite dynamics. In New Zealand, exotic brown trout Salmo trutta and rainbow trout Oncorhynchus mykiss have acquired two native trematodes (Telogaster opisthorchis and Stegodexamene anguillae) from their native definitive host (the longfin eel Anguilla dieffenbachii). We used a combination of field surveys and experimental infections to determine the relative competence of native and exotic fish hosts for these native parasites. Field observations indicated that the longfin eel was the superior host for both parasites, although differences between native and exotic hosts were less apparent for S. anguillae. Experimental infections indicated that both parasites had poorer establishment and survival in salmonids, although some worms matured and attained similar sizes to those in eels before dying. Overall, the field surveys and experimental infections indicate that these exotic salmonids are poor hosts of both native trematodes and their presence may decrease native parasite flow to native hosts.

Introduced brown trout alter native acanthocephalan infections in native fish.

1. Native parasite acquisition provides introduced species with the potential to modify native host-parasite dynamics by acting as parasite reservoirs (with the 'spillback' of infection increasing the parasite burdens of native hosts) or sinks (with the 'dilution' of infection decreasing the parasite burdens of native hosts) of infection. 2. In New Zealand, negative correlations between the presence of introduced brown trout (Salmo trutta) and native parasite burdens of the native roundhead galaxias (Galaxias anomalus) have been observed, suggesting that parasite dilution is occurring. 3. We used a multiple-scale approach combining field observations, experimental infections and dynamic population modelling to investigate whether native Acanthocephalus galaxii acquisition by brown trout alters host-parasite dynamics in native roundhead galaxias. 4. Field observations demonstrated higher infection intensity in introduced trout than in native galaxias, but only small, immature A. galaxii were present in trout. Experimental infections also demonstrated that A. galaxii does not mature in trout, although parasite establishment and initial growth were similar in the two hosts. Taken together, these results support the hypothesis that trout may serve as an infection sink for the native parasite. 5. However, dynamic population modelling predicts that A. galaxii infections in native galaxias should at most only be slightly reduced by dilution in the presence of trout. Rather, model exploration indicates parasite densities in galaxias are highly sensitive to galaxias predation on infected amphipods, and to relative abundances of galaxias and trout. Hence, trout presence may instead reduce parasite burdens in galaxias by either reducing galaxias density or by altering galaxias foraging behaviour.