Population‐level effects of parasitism on a freshwater ecosystem engineer, the unionid mussel Anodonta anatina

Abstract

Parasites can negatively affect hosts at individual, population, and species‐level scales. However, the link between individual‐ and population‐level impacts is often poorly understood. In particular, the population‐level response to parasitism may alter wider ecosystem dynamics if animals with ecosystem engineering capabilities are infected. Here, we examine the effects of parasitism on a freshwater ecosystem engineer, the unionid mussel Anodonta anatina, at two different sites. We study three common parasites: the digenean trematode Rhipidocotyle campanula; the unionicolid mite Unionicola intermedia; and the ectoparasitic invasive zebra mussel Dreissena polymorpha. As well as demonstrating the individual‐level effects of parasitism on the native host mussel, we construct a simple model to estimate the reduction in population‐level reproductive output caused by parasites. We show that both infection prevalence and intensity were population‐specific, with one site having more than three times as many native mussels infected by trematodes and mites than the other, but more than four times fewer mussels afflicted by invasive zebra mussels. Negative reproductive consequences for individual host mussels were documented as a result of parasitism, with trematodes causing castration at both sites. Mites were also correlated with a reduction in the viability of larval offspring (glochidia) by more than 25%, but only at one site, suggesting some potential impacts of parasitism may be population specific. The population‐level model shows that parasitism alone reduces larval output of the two populations by 10% and 13%, respectively. Our study takes the important step of scaling individual‐level effects of parasitism to population‐level processes, and highlights the influence that parasites may have in the population dynamics of unionid mussels. Given the ecosystem engineering capabilities of A. anatina, such effects may have important impacts on the wider biota. Even at relatively low prevalences, the observed effects of parasites on native mussel populations suggests that parasitism must be considered in the conservation of freshwater mussels, one of the world's most globally imperilled faunal groups. Further, understanding how the effects of parasitism on individual hosts scales to the ecosystem level is a crucial and unaddressed question in freshwater biology.

Parasitism dramatically alters the ecosystem services provided by freshwater mussels

“…While R. campanula prevalence may vary (Taskinen et al, 1997), infection rates remain >10% throughout the year in this river (Brian et al, 2021; Brian & Aldridge, 2021a), and so we expect a qualitative effect regardless of sampling time, even if prevalence changes. Furthermore, we have also left aside the temporal density‐mediated effect of parasitism; for example, trematodes can increase unionid mussel mortality under stressful conditions (Jokela et al, 2005) and reduce population‐level reproductive capacity (Brian et al, 2021). Incorporating such effects into models of ecosystem function requires understanding how reproductive limitation influences long‐term population dynamics.…”

“…However, as we emphasise the proportional change rather than absolute values, as long as the effect of parasites on individual mussels is reasonably consistent through the year, our results should be broadly translatable to other seasons. While R. campanula prevalence may vary (Taskinen et al, 1997), infection rates remain >10% throughout the year in this river (Brian et al, 2021; Brian & Aldridge, 2021a), and so we expect a qualitative effect regardless of sampling time, even if prevalence changes. Furthermore, we have also left aside the temporal density‐mediated effect of parasitism; for example, trematodes can increase unionid mussel mortality under stressful conditions (Jokela et al, 2005) and reduce population‐level reproductive capacity (Brian et al, 2021).…”

“…Incorporating such effects into models of ecosystem function requires understanding how reproductive limitation influences long‐term population dynamics. For example, does a 13% reduction in population‐level glochidial output (Brian et al, 2021) directly correspond to a 13% reduction in juvenile mussel recruitment the following year? To our knowledge, such information is not yet available for freshwater mussels.…”

“…The average length of mussels (± SE ) was 72.2 mm ± 0.97 mm. We did not explicitly consider mussel sex, given the extreme female bias in this river (>95% of mussels possessing female trait of marsupia; Brian et al, 2021).…”

“…The native digenean trematode Rhipidocotyle campanula is commonly observed inside the host unionid mussel Anodonta anatina . While the partial or complete castrating impacts of this parasite (and hence a possible density‐mediated effect) are well documented (Brian et al, 2021; Müller et al, 2015), there is indirect evidence, such as shell morphology changes in infected mussels (Zieritz & Aldridge, 2011), that trematodes may also affect the filtering phenotype of the host. R. campanula appears to only infect mussels of the genus Anodonta (Brian & Aldridge, 2019), but this is unlikely to be due to active choice by the trematode given the low selective ability of its infective stage (miracidia).…”