Friends or enemies: Multi‐species interactions among biofoulers, endoparasites and their gastropod hosts

Abstract

Parasites are a crucial factor that shapes the functioning of communities throughout the world, as are gregarious macrofoulers in aquatic ecosystems. However, little is known about the effects of three‐way interactions between macrofoulers, endoparasites and their hosts. We predict that macrofouling and parasite infection may act (i) independently of each other, (ii) synergistically, increasing their final negative impact on the host or (iii) antagonistically, the former weakening the negative impact of the latter. We investigated multiway relationships between an invasive freshwater filter‐feeding macrofouler (the zebra mussel), digenean endoparasite and their gastropod host, Viviparus viviparus. Furthermore, we checked the recruitment of mussels in living gastropods versus their empty shells. We sampled living V. viviparus and their empty shells with attached dreissenids from a Polish dam reservoir. We counted and weighed attached mussels and determined wet weight, shell height and sex of gastropods. Then we dissected the molluscs to look for digenean larvae and gastropod embryos. We use these parameters to look for reciprocal associations between mussel fouling, parasitic infection and gastropod size and fertility, as well as to infer the most likely mechanisms of the observed relationships. Dreissenid overgrowth was associated with reduced fertility and size of viviparids, but also with a lower prevalence of digenean metacercariae (Leucochloridiomorpha sp.). We did not observe a negative influence of these digeneans on their gastropod hosts. In addition, large living viviparids and their empty shells were equally used as substrates by dreissenids, but small living gastropods were more fouled than shells of the corresponding size. A trade‐off exists in the studied system: filter‐feeding macrofoulers may bring some profits for their host, reducing the pressure of waterborne parasites (which may be crucial in the case of pathogenic species/life stages), although at the cost of the reduced growth and fertility of the host. Furthermore, mussels attached to mollusc hosts can exert a cascading effect on the reduced prevalence of digeneans in their final hosts, including those of medical or veterinary importance.

New species, new story: The impact of invasive non‐host predators on host‐trematode interactions

“…Multi-species communities can amplify or dilute parasite prevalence and abundance (Stanicka, Szopieray, et al, 2023;Strasburg & Boone, 2022), and predictions of these shifts become more complex when non-native species are involved, altering existing relationships (Stanicka, Szopieray, et al, 2023). Here, we demonstrated that gammarids could cause a significant reduction in parasite-host encounters; all gammarids preyed on trematode cercariae and reduced infection levels in the target snail host, but the Ponto-Caspian invaders were more efficient than the European native species.…”

“…Therefore, investigations of multi‐way ecological interactions and community‐level changes are required to understand parasite transmission, especially given global changes in biodiversity and increases in parasite outbreaks (Shaw & Civitello, 2021; Strasburg & Boone, 2022). Multi‐species communities can amplify or dilute parasite prevalence and abundance (Stanicka, Szopieray, et al, 2023; Strasburg & Boone, 2022), and predictions of these shifts become more complex when non‐native species are involved, altering existing relationships (Stanicka, Szopieray, et al, 2023). Here, we demonstrated that gammarids could cause a significant reduction in parasite‐host encounters; all gammarids preyed on trematode cercariae and reduced infection levels in the target snail host, but the Ponto‐Caspian invaders were more efficient than the European native species.…”

Enigmatic freshwater mussel declines could be explained by the biodiversity‐disease relationship

“…If they are non-competent they could potentially contribute to dilution and provide a cryptic benefit to natives, something recently shown to benefit native snails (Stanicka et al, 2023). Invasive mussels could also potentially consume pathogen infective stages, particularly those of trematodes (Koprivnikar et al, 2023).…”

“…If they are competent hosts for native pathogens, they provide an additional viable (reservoir) host and could thus drive further pathogen amplification, even when native hosts are at very low density (Kelly et al, 2009). If they are non‐competent they could potentially contribute to dilution and provide a cryptic benefit to natives, something recently shown to benefit native snails (Stanicka et al, 2023). Invasive mussels could also potentially consume pathogen infective stages, particularly those of trematodes (Koprivnikar et al, 2023).…”