New perspectives on the role of cleaning symbiosis in the possible transmission of fish diseases

For the last seven decades, cleaning symbiosis in the marine environment has been a research field of intrigue. There is substantial evidence that, by removing undesired items from their client fishes, cleaner organisms have positive ecosystem effects. These include increased fish recruitment, abundance and enhanced fish growth. However, the intimate association and high frequency of interactions between cleaners and clients potentially facilitates pathogen transmission and disease spread. In this review, we identify knowledge gaps and develop novel hypotheses on the interrelationship between parasites, hosts and the environment (disease triangle concept), with a particular emphasis on the potential role of cleaner organisms as hosts and/or transmitters of parasites. Despite evidence supporting the positive effects of cleaner organisms, we propose the cleaners as transmitters hypothesis; that some parasites may benefit from facilitated transmission to cleaners during cleaning interactions, or may use cleaner organisms as transmitters to infect a wider diversity and number of hosts. This cost of cleaning interactions has not been previously accounted for in cleaning theory. We also propose the parasite hotspot hypothesis; that parasite infection pressure may be higher around cleaning stations, thus presenting a conundrum for the infected client with respect to cleaning frequency and duration. The impact of a changing environment, particularly climate stressors on cleaners’ performance and clients’ cleaning demand are only beginning to be explored. It can be expected that cleaners, hosts/clients, and parasites will be impacted in different ways by anthropogenic changes which may disrupt the long-term stability of cleaning symbiosis.