The behavioural ecology of cleaning mutualisms

Abstract

Cleaning interactions, in which a small ‘cleaner’ organism removes and often consumes material from a larger ‘client’, are some of the most enigmatic and intriguing of interspecies interactions. Early research on cleaning interactions canonized the view that they are mutualistic, with clients benefiting from parasite removal and cleaners benefiting from a meal, but subsequent decades of research have revealed that the dynamics of these interactions can be highly complex. Despite decades of research on marine cleaning interactions (the best studied cleaning systems), key questions remain, including how the outcome of an individual cleaning interaction depends on ecological, behavioural, and social context, how such interactions arise, and how they remain stable over time. Recently, studies of marine parasites, long-term data from coral reef communities with and without cleaners, increased behavioural observations recorded using remote video, and a focus on a larger numbers of cleaning species have helped bring about key conceptual advances in our understanding of cleaning interactions. In particular, evidence now suggests that the ecological, behavioural, and social contexts of a given cleaning interaction can result in the outcome ranging from mutualistic to parasitic, and that cleaning interactions are mediated by signals that can also vary with context. Signals are an important means by which animals extract information about one another, and thus represent a mechanism by which interspecific partners can determine when, how, and with whom to interact. Here, I review our understanding of the behavioural ecology of marine cleaning interactions. In particular, I argue that signals provide a useful framework for advancing our understanding of several important outstanding questions. I discuss the costs and benefits of cleaning interactions, review how cleaners and clients recognize and assess one another using signals, and discuss how signal reliability, or ‘honesty’, may be maintained in cleaning systems. Lastly, I discuss the sensory ecology of both cleaners and clients to highlight what marine cleaning systems can tell us about signalling behaviour, signal form, and signal evolution in a system where signals are aimed at multiple receiver species. Overall, I argue that future research on cleaning interactions has much to gain by continuing to shift the research focus toward examining the variable outcomes of cleaning interactions in relation to the broader behavioural, social, and ecological contexts.