Parasites can alter communities by reducing densities of keystone hosts, but few studies have examined how trait-mediated indirect effects of parasites can alter ecological communities. We test how trematode parasites (Microphallus spp.) that affect invasive crayfish (Orconectes rusticus) behavior alter how crayfish impact lake littoral communities. O. rusticus drive community composition in north temperate lakes, and predatory fish can reduce crayfish activity and feeding. In laboratory studies, Microphallus parasites also alter O. rusticus behavior: infected O. rusticus eat fewer macroinvertebrates and are bolder near predatory fish than uninfected individuals. We used a 2 x 2 factorial experiment to test how predatory fish and parasites affect O. rusticus impacts in large mesocosms over 4 weeks. We predicted (1) that when predators were absent, infected crayfish would have lower impacts than uninfected crayfish on macrophytes and macroinvertebrates (as well as reduced growth and higher mortality). However, (2) when predators were present but unable to consume crayfish, infected crayfish would have greater impacts (as well as greater growth and lower mortality) than uninfected crayfish because of increased boldness. Because of its effect on crayfish feeding behavior, we also predicted (3) that infection would alter macrophyte and macroinvertebrate community composition. In contrast to our first hypothesis, we found that infected and uninfected crayfish had similar impacts on lower trophic levels when predators were absent. Across all treatments, infected crayfish were more likely to be outside shelters and had greater growth than uninfected crayfish, suggesting that the reduced feeding observed in short-term experiments does not occur over longer timescales. However, in support of the second hypothesis, when predatory fish were present, infected crayfish ate more macroinvertebrates than did uninfected crayfish, likely due to increased boldness. We also observed a trend for greater macrophyte consumption associated with infection and a trend indicating infection might alter macroinvertebrate community composition. Our results suggest that parasites can alter aquatic communities in mesocosms merely by modifying host behavior.
Summary
Parasites can have profound effects on host behaviour and species interactions, but the consequences of these impacts are inadequately understood. Three common crayfish in northern Wisconsin and Michigan (native Orconectes virilis, non‐native O. propinquus and non‐native and invasive O. rusticus) are intermediate hosts for trematode parasites, Microphallus spp. Some species in the genus Microphallus alter host behaviour, increasing their predation risk, but the effects of microphallids on crayfish are unknown. Orconectes propinquus replaces O. virilis in most lakes where they are introduced, and O. rusticus replaces both. These species replacements have major effects on macrophytes, macroinvertebrates and fish. Therefore, differential parasite impacts on crayfish could have community‐level effects if competitive outcomes are altered.
We examined the shelter affinity of infected and uninfected individuals of all three species in laboratory experiments in the presence and absence of a conspecific. We also observed behaviour during agonistic interactions, and measured boldness by quantifying how quickly crayfish emerged from shelter with a predatory fish present.
Infection with Microphallus substantially altered crayfish shelter affinity, shelter competition and boldness, though infection affected each species differently. Infection reduced shelter affinity in O. propinquus and the ability of O. virilis to compete for shelter against uninfected conspecifics. Infected crayfish were bolder in the presence of a predatory fish.
Our results suggest that infection with Microphallus alters crayfish behaviour so that all three species are more vulnerable to predation. Orconectes propinquus is likely to suffer the greatest increase in predation when infected, due to a reduced affinity for shelter coupled with increased boldness. In lakes where crayfish species coexist, O. rusticus will probably be less affected by the parasite than either congener. Therefore, crayfish parasites could alter crayfish abundance and species composition in north temperate lakes via behavioural modifications.
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