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Mounting evidence suggests that the transmission of certain parasites is facilitated by increasing temperatures, causing their host population to decline. However, no study has yet addressed how temperature and parasitism may combine to shape the functional structure of a whole host community in the face of global warming. Here, we apply an outdoor mesocosm approach supported by field surveys to elucidate this question in a diverse intertidal community of amphipods infected by the pathogenic microphallid trematode, Maritrema novaezealandensis. Under present temperature (17°C) and level of parasitism, the parasite had little impact on the host community. However, elevating the temperature to 21°C in the presence of parasites induced massive structural changes: amphipod abundances decreased species-specifically, affecting epibenthic species but leaving infaunal species largely untouched. In effect, species diversity dropped significantly. In contrast, four degree higher temperatures in the absence of parasitism had limited influence on the amphipod community. Further elevating temperatures (19-25°C) and parasitism, simulating a prolonged heat-wave scenario, resulted in an almost complete parasite-induced extermination of the amphipod community at 25°C. In addition, at 19°C, just two degrees above the present average, a similar temperature-parasite synergistic impact on community structure emerged as seen at 21°C under lower parasite pressure. The heat-wave temperature of 25°C per se affected the amphipod community in a comparable way: species diversity declined and the infaunal species were favoured at the expense of epibenthic species. Our experimental findings are corroborated by field data demonstrating a strong negative relationship between current amphipod species richness and the level of Maritrema parasitism across 12 sites. Hence, owing to the synergistic impact of temperature and parasitism, our study predicts that coastal amphipod communities will deteriorate in terms of abundance and diversity in face of anticipated global warming, functionally changing them to be dominated by infaunal species., (© 2018 John Wiley & Sons Ltd.)

Parasitism is believed to play an important role in maintaining species diversity, for instance by facilitating coexistence between competing host species. However, the possibility that environmental factors may govern the outcome of parasite-mediated competition has rarely been considered. The closely related amphipods Corophium volutator and Corophium arenarium both serve as second intermediate host for detrimental trematodes. Corophium volutator is the superior competitor of the two, but also suffers from higher mortality when exposed to infective trematode stages. Here, we report parasite-mediated competitive release of C. arenarium in an intertidal habitat, in part triggered by unusually high temperatures linked to the North Atlantic climate oscillation (NAO). The elevated temperatures accelerated the transmission of cercariae from sympatric first intermediate hosts (mud snails) to amphipods, causing a local collapse of the parasite-sensitive C. volutator population and concordant increase in the abundance of the competitively inferior C. arenarium.

Besides the direct impact on the general performance of individual organisms, the ecological consequences of climate change in terrestrial and marine ecosystems are expected to be determined by complex cascading effects arising from modified trophic interactions and competitive relationships. Recently, the synergistic effect of parasitism and climate change has been emphasised as potentially important to host population dynamics and community structure, but robust empirical evidence is generally lacking. The amphipod Corophium volutator is an ecologically important species in coastal soft-bottom habitats of the temperate North Atlantic, and commonly serves as host to microphallid trematodes that cause intensity-dependent and temperature-dependent mortality in the amphipod population. Using a simulation model parameterised with experimental and field data, we demonstrate that a 3.8 degrees C increase in ambient temperature will likely result in a parasite-induced collapse of the amphipod population. This temperature increase is well within the range predicted to prevail by the year 2075 in the International Wadden Sea region from where the model data are obtained. Due to the amphipods' ecological importance, their population decline may impact the coastal ecosystem as a whole.

The abundant amphipod Corophium volutator is an ecosystem engineer in soft-bottom intertidal communities due to its grazing and bioturbation activity. However, the amphipod commonly serves as second intermediate host for detrimental microphallid trematodes. This host-parasite association is potentially very sensitive to climate change as the transmission rate of larval trematodes (cercariae) from first intermediate hosts (mud snails) to amphipods, and hence infection intensity-dependent amphipod mortality, generally accelerates with increasing temperature. Given the ecosystem engineering role of C. volutator, we hypothesized that elevated temperature, indirectly through increased parasite-induced amphipod mortality, significantly affects the structure of the surrounding benthic community. To test this, we performed a three-month outdoor mesocosm experiment exposing a natural soft-bottom community of benthic plants and animals to four different treatments: relatively low mean water temperature (18 °C) with low (< 4%) and high (c. 31%) trematode prevalence in the snail population, and relatively high mean water temperature (22 °C) with low and high trematode prevalence. Both temperature and snail parasitism had a significant impact on amphipod abundance and resulted in their almost complete eradication at the warm temperature with high parasitism. Aside from the amphipod hosts, increased temperature affected the abundance of eight faunal species out of 22 in total (36%), whereas increased level of parasitism or the parasite-temperature interaction influenced the density of three species (14%). The treatment-determined Corophium abundance played an isolated role for several species, particularly the polychaetes Hediste diversicolor (positive) and Polydora ligni (negative). Regarding primary producers, the overall frequency distribution of 21 species of benthic diatoms differed between all four treatments. Species-specific effects were few and weak, however, and microalgal abundance (chlorophyll-a) was statistically unaffected by treatments, together suggesting a rather resilient plant community towards the experimental perturbations. At the community level, the non-host macrofaunal diversity decreased with temperature in the low parasitism treatments whereas it increased with temperature in the high parasitism treatments. This suggests that sufficiently high levels of parasitism may turn a negative effect of elevated temperature on macrofaunal biodiversity into a positive effect. Hence, our experiment demonstrates that the synergy between parasitism and a relevant temperature increase, e.g. in lieu of climate oscillations or global warming, may have broad ecological consequences for the organization and function of soft-bottom communities, in part through elevated parasite-induced mortality of a central community member. [ABSTRACT FROM AUTHOR]