Parasite avoidance behaviours in aquatic environments

Abstract

Parasites, including macroparasites, protists, fungi, bacteria and viruses, can impose a heavy burden upon host animals. However, hosts are not without defences. One aspect of host defence, behavioural avoidance, has been studied in the terrestrial realm for over 50 years, but was first reported from the aquatic environment approximately 20 years ago. Evidence has mounted on the importance of parasite avoidance behaviours and it is increasingly apparent that there are core similarities in the function and benefit of this defence mechanism between terrestrial and aquatic systems. However, there are also stark differences driven by the unique biotic and abiotic characteristics of terrestrial and aquatic (marine and freshwater) environments. Here, we review avoidance behaviours in a comparative framework and highlight the characteristics of each environment that drive differences in the suite of mechanisms and cues that animals use to avoid parasites. We then explore trade-offs, potential negative effects of avoidance behaviour and the influence of human activities on avoidance behaviours. We conclude that avoidance behaviours are understudied in aquatic environments but can have significant implications for disease ecology and epidemiology, especially considering the accelerating emergence and re-emergence of parasites.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Keywords: avoidance behaviour; behavioural immunity; freshwater; infection; marine; pathogen.

Figure 1.

Life cycle of the Caribbean spiny lobster Panulirus argus and the role of chemosensory-mediated attraction and avoidance in its ecology. CL, carapace length. Juvenile P. argus are social but able to discern attractive chemical cues emanating from shelters containing healthy conspecifics and co-habiting crustaceans (spider crab Damithrax spinosissimus), from aversive chemical cues emanating from shelters containing competitors (stone crab Menippe mercenaria), predators (octopus Octopus briarius) and conspecifics infected with the lethal virus PaV1 (see box 1 for detailed case study). Spider crab (left) and octopus drawings used with permission from Helen Casey. All other drawings are public domain.

Figure 2.

Parasite avoidance by fish in the Diplostomum system. Trematodes of the genus Diplostomum are ubiquitous parasites of freshwater fishes, with species like D. pseudospathaceum infecting the eye lenses of fish. (a) An infected first intermediate snail (Lymnaea stagnalis) host of the parasite can release tens of thousands of cercaria larvae per day (dense swarm of cercariae can be observed visually in water); (b) a cercaria (photos by Anssi Karvonen and Anna Faltýnková, respectively). (c) In the eye lens, parasites develop to metacercariae, which in high numbers can cause opacity of the lens, reduction in vision and severe fitness consequences for the fish (photo by Ines Klemme). Fish can recognize the presence of cercariae in water and avoid them by swimming away. (d) The response time to cercarial presence is correlated with the number of infections in the eye lenses (reproduced from Karvonen et al. [12], © 2004 Cambridge University Press).

Figure 3.

Diagrammatic representation of sperm investment in the amphipod Gammarus duebeni. Parasitized females receive a lower sperm investment from males, relative to those females who are uninfected. Hypothetically, this will lead to an increased chance of uninfected offspring within the population via larger uninfected brood sizes and increased health status, as identified by Dunn et al. [71].