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

This article has been updated

Abstract

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.

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Data availability

All references used to generate Fig. 2 are contained in the Online Resource 1.

Change history

  • 27 February 2021

    The original online version of this article was revised: the link to the online resource on the page of the paper was not included previously and it is now included.

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Acknowledgements

We thank Mark McCormick and Renato Morais for helpful insight, discussion, and comments on the manuscript. We thank Derek Sun for his contribution of unpublished data. The authors thank two anonymous reviewers for their suggestions, which improved the content of this article. We thank the platform IAN Image Library for providing free vectors and more specifically Christine Thurber for Naso unicornis and Epinephelus malabaricus, Tracey Saxby for Chaetodon lineolatus, Dascyllus aruanus, Plectorhinchus polytaenia and for the gorgonians and the triggerfish species, Joanna Woerner for Acanthurus nigrofuscus, and Dieter Tracey and Diana Kleine for anemones and corals. Cleaner wrasse model was purchased with all “All Extended Uses” from Turbosquid website (https://www.turbosquid.com/).

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James Cook University Postgraduate Research Scholarship (JCUPRS) to PN.

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This review was designed by PN and KSH. The literature search and data analysis were done by PN. The initial draft was written by PN. The development of the manuscript was done by PN, KSH, DBV, ASG.

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Correspondence to Pauline Narvaez.

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Narvaez, P., Vaughan, D.B., Grutter, A.S. et al. New perspectives on the role of cleaning symbiosis in the possible transmission of fish diseases. Rev Fish Biol Fisheries (2021). https://doi.org/10.1007/s11160-021-09642-2

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Keywords

  • Cleaners
  • Clients
  • Hosts
  • Parasite transmission
  • Anthropogenic changes
  • Ecosystem function