Parasite infestation increases on coral reefs without cleaner fish

Abstract

Mutualisms are pivotal in shaping ecological communities. Iconic images of cleaner fish entering the mouths of predatory fish clients to remove ectoparasites epitomize their mutual benefit. Experimental manipulations of cleaner wrasse reveal declines in fish size and growth, and population abundance and diversity of client fishes in the absence of cleaner wrasse. Fishes grow more slowly and are less abundant and diverse on reefs without cleaner wrasse, both for larger species that are regularly cleaned and have high ectoparasite loads (“attractive species”), and for those smaller species that are rarely cleaned and are rarely infested with parasites (“unattractive species”). We therefore considered whether these previously observed declines in individual and population parameters on reefs without cleaners were related to increased ectoparasite infestation using an attractive species (Hemigymnus melapterus, Labridae) and an unattractive species (Pomacentrus amboinensis, Pomacentridae). Traps with these fish as a form of bait were deployed to sample blood-sucking gnathiid ectoparasites (Gnathiidae: Isopoda) on reefs from which cleaners (Labroides dimidiatus, Labridae) have been removed for 13 yr. Cleaner fish could not enter traps to access the clients/hosts, but gnathiids could enter the traps to infest hosts; thus, this method sampled the indirect effect of cleaners on gnathiid infestation of fish. Infestation was higher on reefs without cleaners than on those with them. The effect was only detected during the daytime when cleaners are active and only on the attractive species (H. melapterus). Thus, cleaner presence indirectly reduced fish exposure to parasites in a species that is highly susceptible to parasites, but not in one that is rarely infested with parasites. This suggests that cleaner presence indirectly reduces exposure of a common fish species to harmful parasites, which may explain some observed benefits in fishes at this location.

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References

  1. Adlard RD, Lester RJG (1994) Dynamics of the interaction between the parasitic isopod, Anilocra pomacentri, and the coral reef fish, Chromis nitida. Parasitology 109:311–324

    Article  PubMed  Google Scholar 

  2. Artim JM, Sikkel PC (2013) Live coral repels a common reef fish ectoparasite. Coral Reefs 32:487–494

    Article  Google Scholar 

  3. Bronstein JL (1998) The contribution of ant–plant protection studies to our understanding of mutualism. Biotropica 30:150–161

    Article  Google Scholar 

  4. Bronstein JL (2015) Mutualism. Oxford University Press, New York

    Google Scholar 

  5. Bshary R (2003) The cleaner wrasse, Labroides dimidiatus, is a key organism for reef fish diversity at Ras Mohammed National Park, Egypt. J Anim Ecol 72:169–176

    Article  Google Scholar 

  6. Cheney KL, Bshary R, Grutter AS (2008) Cleaner fish cause predators to reduce aggression toward bystanders at cleaning stations. Behav Ecol 19:1063–1067

    Article  Google Scholar 

  7. Clague GE, Cheney KL, Goldizen AW, McCormick MI, Waldie PA, Grutter AS (2011) Long-term cleaner fish presence affects growth of a coral reef fish. Biol Lett 7:863–865

    Article  PubMed  PubMed Central  Google Scholar 

  8. Coile AM, Sikkel PC (2013) An experimental field test of susceptibility to ectoparasitic gnathiid isopods among Caribbean reef fishes. Parasitology 140:888–896

    CAS  Article  PubMed  Google Scholar 

  9. Côté IM (2000) Evolution and ecology of cleaning symbioses in the sea. Oceanogr Mar Biol Annu Rev 38:311–355

    Google Scholar 

  10. Curtis LM, Grutter AS, Smit NJ, Davies AJ (2013) Gnathia aureamaculosa, a likely definitive host of Haemogregarina balistapi and potential vector for Haemogregarina bigemina between fishes of the Great Barrier Reef, Australia. Int J Parasitol 43:361–370

    Article  PubMed  Google Scholar 

  11. Del-Claro K, Oliveira PS (2000) Conditional outcomes in a neotropical treehopper–ant association: temporal and species-specific variation in ant protection and homopteran fecundity. Oecologia 124:156–165

    CAS  Article  PubMed  Google Scholar 

  12. Ferreira ML, Smit NJ, Grutter AS, Davies AJ (2009) A new species of gnathiid (Crustacea: Isopoda) parasitizing teleosts from Lizard Island, Great Barrier Reef, Australia. J Parasitol 95:1066–1075

    Article  PubMed  Google Scholar 

  13. Finley RA, Forrester GE (2003) Impact of ectoparasites on the demography of a small reef fish. Mar Ecol Prog Ser 248:305–309

    Article  Google Scholar 

  14. Gorlick DL, Atkins PD, Losey GS (1987) Effect of cleaning by Labroides dimidiatus (Labridae) on an ectoparasite population infecting Pomacentrus vaiuli (Pomacentridae) at Enewetak Atoll. Copeia 1:41–45

    Article  Google Scholar 

  15. Grutter AS (1995) The relationship between cleaning rates and ectoparasite loads in coral reef fishes. Mar Ecol Prog Ser 118:51–58

    Article  Google Scholar 

  16. Grutter AS (1996) Parasite removal rates by the cleaner wrasse Labroides dimidiatus. Mar Ecol Prog Ser 130:61–70

    Article  Google Scholar 

  17. Grutter AS (1997) Size-selective predation by the cleaner fish Labroides dimidiatus. J Fish Biol 50:1303–1308

    Google Scholar 

  18. Grutter AS (1999) Cleaner fish really do clean. Nature 398:672–673

    CAS  Article  Google Scholar 

  19. Grutter AS (2002) Cleaning symbioses from the parasites’ perspective. Parasitology 124:S65–S81

    Article  PubMed  Google Scholar 

  20. Grutter AS (2003) Feeding ecology of the fish ectoparasite Gnathia sp (Crustacea: Isopoda) from the Great Barrier Reef, and its implications for fish cleaning behaviour. Mar Ecol Prog Ser 259:295–302

    Article  Google Scholar 

  21. Grutter AS, Poulin R (1998) Intraspecific and interspecific relationships between host size and the abundance of parasitic larval gnathiid isopods on coral reef fishes. Mar Ecol Prog Ser 164:263–271

    Article  Google Scholar 

  22. Grutter AS, Bshary R (2003) Cleaner fish prefer client mucus: support for partner control mechanisms in cleaning interactions. Proc R Soc Lond B Biol Sci 70:S242–S244

    Article  Google Scholar 

  23. Grutter AS, Murphy JM, Choat JH (2003) Cleaner fish drives local fish diversity on coral reefs. Curr Biol 13:64–67

    CAS  Article  PubMed  Google Scholar 

  24. Grutter AS, Pickering JL, McCallum H, McCormick MI (2008) Impact of micropredatory gnathiid isopods on young coral reef fishes. Coral Reefs 27:655–661

    Article  Google Scholar 

  25. Grutter AS, Crean AJ, Curtis LM, Kuris AM, Warner RR, McCormick MI (2011) Indirect effects of an ectoparasite reduce successful establishment of a damselfish at settlement. Funct Ecol 25:586–594

    Article  Google Scholar 

  26. Hayes PM, Smit NJ, Davies AJ (2007) Pathology associated with parasitic juvenile gnathiids feeding on the puffadder shyshark, Haploblepharus edwardsii (Voight). J Fish Dis 30:55–58

    CAS  Article  PubMed  Google Scholar 

  27. Hayes PM, Smit NJ, Grutter AS, Davies AJ (2011) Unexpected response of a captive blackeye thicklip, Hemigymnus melapterus (Bloch), from Lizard Island, Australia, exposed to juvenile isopods Gnathia aureamaculosa Ferreira & Smit. J Fish Dis 34:563–566

    CAS  Article  PubMed  Google Scholar 

  28. Jones CM, Grutter AS (2005) Parasitic isopods (Gnathia sp.) reduce haematocrit in captive blackeye thicklip (Labridae) on the Great Barrier Reef. J Fish Biol 66:860–864

    Article  Google Scholar 

  29. Jones CM, Grutter AS (2007) Variation in emergence of parasitic and predatory isopods among habitats at Lizard Island, Great Barrier Reef. Mar Biol 150:919–927

    Article  Google Scholar 

  30. Jones CM, Grutter AS (2008) Reef-based micropredators reduce the growth of post-settlement damselfish in captivity. Coral Reefs 27:677–684

    Article  Google Scholar 

  31. Jones CM, Nagel L, Hughes GL, Cribb TH, Grutter AS (2007) Host specificity of two species of Gnathia (Isopoda) determined by DNA sequencing blood meals. Int J Parasitol 37:927–935

    CAS  Article  PubMed  Google Scholar 

  32. Lafferty KD, Kuris AM (2002) Trophic strategies, animal diversity and body size. Trends in Ecology Evolution 17:507–513

    Article  Google Scholar 

  33. Palmer TM, Pringle EG, Stier A, Holt RD (2015) Mutualism in a community context. Oxford University Press, New York

    Google Scholar 

  34. Penfold R, Grutter AS, Kuris AM, McCormick MI, Jones CM (2008) Interactions between juvenile marine fish and gnathiid isopods: predation versus micropredation. Mar Ecol Prog Ser 357:111–119

    Article  Google Scholar 

  35. Pringle EG, Gordon DM (2013) Protection mutualisms and the community: geographic variation in an ant–plant symbiosis and the consequences for herbivores. Sociobiology 60:242–251

    Article  Google Scholar 

  36. R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  37. Randall JE (1958) A review of the labrid fish genus Labroides, with description of two new species and notes on ecology. Pac Sci 12:327–347

    Google Scholar 

  38. Rohde K (2005) Marine parasitology. CSIRO Publishing, Clayton

    Google Scholar 

  39. Sikkel PC, Ziemba RE, Sears WT, Wheeler JC (2009) Diel ontogenetic shift in parasitic activity in a gnathiid isopod on Caribbean coral reefs. Coral Reefs 28:489–495

    Article  Google Scholar 

  40. Sikkel PC, Sears WT, Weldon B, Tuttle B (2011) An experimental field test of host-finding mechanisms in a Caribbean gnathiid isopod. Mar Biol 158:1075–1083

    Article  Google Scholar 

  41. Smit NJ, Davies AJ (2004) The curious life-style of the parasitic stages of gnathiid isopods. Adv Parasitol 58:289–391

    CAS  Article  PubMed  Google Scholar 

  42. Smit NJ, Grutter AS, Adlard RD, Davies AJ (2006) Hematozoa of teleosts from Lizard Island, Australia, with some comments on their possible mode of transmission and the description of a new hemogregarine species. J Parasitol 92:778–788

    Article  PubMed  Google Scholar 

  43. Soares MC, Bshary R, Côté IM (2008) Does cleanerfish service quality depend on client value or choice options? Anim Behav 76:123–130

    Article  Google Scholar 

  44. Soares MC, Oliveira RF, Ros AFH, Grutter AS, Bshary R (2011) Tactile stimulation lowers stress in fish. Nat Commun 2:534

    Article  PubMed  Google Scholar 

  45. Sun D, Cheney KL, Werminghausen J, Meekan MG, McCormick MI, Cribb TH, Grutter AS (2015) Presence of cleaner wrasse increases the recruitment of damselfishes to coral reefs. Biol Lett 11:20150456

    Article  PubMed  PubMed Central  Google Scholar 

  46. Sun D, Cheney KL, Werminghausen J, McClure EC, Meekan MG, McCormick MI, Cribb TH, Grutter AS (2016) Cleaner wrasse influence habitat selection of young damselfish. Coral Reefs 35:427–436

    Article  Google Scholar 

  47. Vaughan DB, Grutter AS, Costello MJ, Hutson KS (2017) Cleaner fishes and shrimp diversity and a re-evaluation of cleaning symbioses. Fish Fish 18:698–716

    Article  Google Scholar 

  48. Waldie PA, Blomberg SP, Cheney KL, Goldizen AW, Grutter AS (2011) Long-term effects of the cleaner fish Labroides dimidiatus on coral reef fish communities. PLoS One 6:e21201

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. Wagner E, Roche DG, Binning SA, Wismer S, Bshary R (2015) Temporal comparison and predictors of fish species abundance and richness on undisturbed coral reef patches. Peerj 3:e1459

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank S. P. Blomberg for statistical advice, and field assistants and Lizard Island Research Station staff. This work was funded by the Australian Research Council, Sea World Research and Rescue Foundation, Australia, the US National Science Foundation (OCE-1536794, PC Sikkel, PI), and The University of Queensland.

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Correspondence to A. S. Grutter.

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Communicated by Biology Editor Dr. Andrew Hoey

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Grutter, A.S., De Brauwer, M., Bshary, R. et al. Parasite infestation increases on coral reefs without cleaner fish. Coral Reefs 37, 15–24 (2018). https://doi.org/10.1007/s00338-017-1628-z

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Keywords

  • Mutualism
  • Cleaning behavior
  • Coral-reef fish parasites
  • Gnathiidae
  • Labridae
  • Labroides dimidiatus