A dark side of cleaning symbiosis: manned submersible observations

  • Rodrigo L. Moura
  • Fernando C. Moraes
  • Gilberto M. Amado-Filho
  • Leonardo M. Neves
  • Alexandre D. Kassuga
  • Danielle D’Agostini
  • Alex C. Bastos
Short Communication

Abstract

Cleaning is a ubiquitous interspecific interaction on shallow tropical, subtropical, and temperate reefs, involving hundreds of species in all ocean basins. This remarkable mutualism encompasses fish and/or shrimp “cleaners” that remove and consume organic debris, parasites, tissue, and mucus from “client” invertebrates (e.g., anemones, crabs, octopuses) and vertebrates (e.g., sharks, bony fishes, turtles, iguanas, and cetaceans. Often regarded as a facilitative interaction, cleaning may be an important driver of reef community structure. Cleaning evolved independently in several unrelated taxa, resulting in a remarkable diversity of interaction types and behaviors. Besides the burden of epibionts, wounds, and parasites, visual and tactile signaling comprise the proximate causation of cleaning interactions. However, there are a few examples of nocturnal cleaning on marine ecosystems, which always involve shrimps acting as cleaners. Here, we report on caridean shrimps (Decapoda: Caridea) cleaning four species of carnivorous fishes in the disphotic-aphotic transition zone (280–320 m depth), based on submersible observations at the continental shelf slope off Northeastern Brazil. This is the first record of shrimp-fish cleaning interactions in deep-cold waters, and our observations support the idea that tactile signaling is of foremost importance in such interactions. We hypothesize that the complex daytime behavior and other adaptations of dedicated cleaner shrimps may have evolved from incidental cleaning by shrimps seeking food on nocturnal shelters of larger fish, or on deep water, where vision plays a minor role.

Keywords

Caridea Abrolhos Deep reefs Mutualism Diel cycles 

Notes

Acknowledgments

We thank Shirley Pomponi (Florida Atlantic University), the crew of R/V Seward Johnson, and the CEPEMAIS team for logistical support during fieldwork. The Brazilian Biodiversity Agency, ICMBio, provided research permits. The authors benefitted from CNPq, FAPERJ, and FAPES grants. This is a contribution from the Rede Abrolhos (www.abrolhos.org), sponsored by ANP/Brasoil. The authors declare no conflicts of interest. No animals were killed or harmed during this research.

Supplementary material

12526_2018_852_MOESM1_ESM.jpg (2.4 mb)
Supplementary Figure 1 The Abrolhos Bank region, Brazil with the two sampled sites highlighted in red (left), and their corresponding slope morphology (right). Submersible tracks are shown as black spots. (JPEG 2508 kb)
12526_2018_852_MOESM2_ESM.jpg (1.8 mb)
Supplementary Figure 2 Additional cleaning events recorded during the survey, involving: A) morid cod, Physiculus kaupi; B) Darwin limehead Gephyroberyx darwinii; C) deepwater squirrelfish, Sargocentron bullisi; D) glasseye, Priacanthus arenatus. (JPEG 1877 kb)
12526_2018_852_MOESM3_ESM.mp4 (67.1 mb)
Supplementary Video 1 Cleaner shrimps and several fish clients in the disphotic-aphotic transition zone in the continental slope of the Abrolhos Bank, Brazil. (MP4 68,721 kb)

References

  1. Baeza JA (2009) Molecular systematics of peppermint and cleaner shrimps: phylogeny and taxonomy of the genera Lysmata and Exhippolysmata (Crustacea:Caridea:Hippolytidae). Zool J Linnean Soc 160:254–265CrossRefGoogle Scholar
  2. Baeza JA, Schubart CD, Zillner P, Fuentes S, Bauer RT (2009) Molecular phylogeny of shrimps from the genus Lysmata (Caridea: Hippolytidae): the evolutionary origins of protandric simultaneous hermaphroditism and social monogamy. Biol J Linn Soc 96:415–424CrossRefGoogle Scholar
  3. Bauer RT (2004) Remarkable shrimps: natural history and adaptations of the carideans. University of Okalahoma Press, Norman, p 316Google Scholar
  4. Becker JH, Grutter AS (2004) Cleaner shrimp do clean. Coral Reefs 23:515–520Google Scholar
  5. Becker JH, Curtis LM, Grutter AS (2005) Cleaner shrimp use a rocking dance to advertise cleaning service to clients. Curr Biol 15:760–764CrossRefPubMedGoogle Scholar
  6. Bonaldo RM, Grutter AS, Sazima I, Krajewski JP (2006) 24/7 service: nocturnal cleaning in a tropical Indo-Pacific reef. Mar Biodivers.  https://doi.org/10.1007/s12526-014-0289-1
  7. Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends in Ecology and Evolution 18:119–125CrossRefGoogle Scholar
  8. Calado R (2008) Marine ornamental shrimp: biology, aquaculture and conservation. Wiley-Blackwell, Hoboken, p 262Google Scholar
  9. Cheney KL (2011) Cleaner wrasse mimics inflict higher costs on their models when they are more aggressive towards signal receivers. Biol Lett 8(1):10–12CrossRefPubMedPubMedCentralGoogle Scholar
  10. Côté IM (2000) Evolution and ecology of cleaning symbioses in the sea. Oceanogr Mar Biol Annu Rev 38:311–355Google Scholar
  11. Cushman JH, Beattie AJ (1991) Mutualisms: assessing the benefits to hosts and visitors. Trends in Ecology and Evolution 6:193–195CrossRefPubMedGoogle Scholar
  12. De Grave S, Li CP, Tsang LM, Chu KH, Chan T (2014) Unweaving hippolytoid systematics (Crustacea, Decapoda, Hippolytidae): resurrection of several families. Zool Scr 43:496–507CrossRefGoogle Scholar
  13. De Grave S, Fransen CHJM, Page TJ (2015) Let’s be pals again: major systematic changes in Palaemonidae (Crustacea: Decapoda). PeerJ 3:e1167CrossRefPubMedPubMedCentralGoogle Scholar
  14. Esaka Y, Yoshioka E, Takeuchi Y, Hur SP, Takemura A (2016) Effect of light intensity and wavelength on diurnal activity of the banded coral shrimp Stenopus hispidus (Decapoda, Stenopodidae): a possible adaptation for a cleaner shrimp in reef environments. Pac Sci 70(2):191–200CrossRefGoogle Scholar
  15. Floeter SR, Vázquez DP, Grutter AS (2006) The macroecology of marine cleaning mutualisms. J Anim Ecol 76:105–111CrossRefGoogle Scholar
  16. Grutter AS (1999) Cleaner fish really do clean. Nature 398:672–673CrossRefGoogle Scholar
  17. Grutter AS, Murphy J, Choat H (2003) Cleaner fish drives local fish diversity on coral reefs. Curr Biol 13:64–67CrossRefPubMedGoogle Scholar
  18. Hendler G (1984) The association of Ophiotrix lineata and Callyspongia vaginalis: a brittlestar-sponge cleaning symbiosis. Mar Ecol 5:9–27CrossRefGoogle Scholar
  19. Herring P (2002) The biology of the deep ocean. Oxford University Press, Oxford, p 315Google Scholar
  20. Horká I, De Grave S, Fransen CHJM, Petrusek A, Ďuriš Z (2016) Multiple host switching events shape the evolution of symbiotic palaemonid shrimps (Crustacea:Decapoda). Sci Rep 6:26486CrossRefPubMedPubMedCentralGoogle Scholar
  21. Kassuga AD, Diele K, Hostim-Silva M (2015) New records of the striped cleaner shrimp Lysmata grabhami (Gordon, 1935) from Brazil, southwestern Atlantic. Braz J Biol 75:936–939CrossRefPubMedGoogle Scholar
  22. Limbaugh C, Pederson H, Chace-Jr FA (1961) Shrimps that clean fishes. Bull Mar Sci 11:237–257Google Scholar
  23. Lindner A (2004) Evolution of shallow-water stylasterid corals (Cnidaria; Hydrozoa; Stylasteridae) from deep-sea ancestors. Integr Comp Biol 43(6):1074–1074Google Scholar
  24. Maul GE (1986) Trachichthyidae. In: PJP W, Bauchot M-L, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the north-eastern Atlantic and the Mediterranean, vol 2. UNESCO, Paris, pp 749–752Google Scholar
  25. Mémery L, Arhan M, Alvarez-Salgado XA, Messias MJ, Mercier H, Castro CG, Rios AF (2000) The water masses along the western boundary of the south and equatorial Atlantic. Prog Oceanogr 47:69–98CrossRefGoogle Scholar
  26. Menezes NA, Buckup PA, Figueiredo JL, Moura RL (2003) Catálogo das espécies de peixes marinhos do Brasil. Museu de Zoologia da Universidade de São Paulo, São Paulo, p 160Google Scholar
  27. Militz TA, Hutson KS (2015) Beyond symbiosis: cleaner shrimp clean up in culture. PLoS One 10(2):e0117723CrossRefPubMedPubMedCentralGoogle Scholar
  28. Moorhouse P (2015) A modern history of the manned submersible. Mar Technol Soc J 49(6):65–78CrossRefGoogle Scholar
  29. Moura RL et al (2013) Spatial patterns of benthic megahabitats and conservation planning in the Abrolhos Bank. Cont Shelf Res 70:109–117CrossRefGoogle Scholar
  30. Pyle R et al (2016) A comprehensive investigation of mesophotic coral ecosystems in the Hawaiian Archipelago. PeerJ 4:e2475CrossRefPubMedPubMedCentralGoogle Scholar
  31. Rhyne AL, Lin J (2006) A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bull Mar Sci 79:165–204Google Scholar
  32. Sazima I, Moura RL, Sazima C (1999) Cleaning activity of juvenile angelfish, Pomacanthus paru, on the reefs of the Abrolhos Archipelago, western South Atlantic. Environ Biol Fish 56:399–407CrossRefGoogle Scholar
  33. Simon T, Pinheiro HT, Moura RL, Carvalho-Filho A, Rocha LA, Martins AS, Mazzei E, Francini-Filho RB, Amado-Filho GM, Joyeux JC (2016) Mesophotic fishes of the Abrolhos Shelf, the largest reef ecosystem in the South Atlantic. J Fish Biol.  https://doi.org/10.1111/jfb.12967
  34. Soledade GO, Baeza JA, Boehs G, Simões SM, Santos PS, Costa RC, Ameida AO (2013) A precautionary tale when describing species in a world of invaders: morphology, coloration and genetics demonstrate that Lysmata rauli is not a new species endemic to Brazil but a junior synonym of the Indo-pacific L. vittata. J Crustac Biol 33(1):66–77CrossRefGoogle Scholar
  35. 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 11:20150456CrossRefPubMedPubMedCentralGoogle Scholar
  36. Vaughan DB, Grutter AS, Costello MJ, Hutson KS (2016) Cleaner fishes and shrimp diversity and a re-evaluation of cleaning symbioses. Fish Fish 00:1–19.  https://doi.org/10.1111/faf.12198 Google Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Rodrigo L. Moura
    • 1
  • Fernando C. Moraes
    • 2
  • Gilberto M. Amado-Filho
    • 2
  • Leonardo M. Neves
    • 3
  • Alexandre D. Kassuga
    • 4
  • Danielle D’Agostini
    • 5
  • Alex C. Bastos
    • 5
  1. 1.Instituto de Biologia and SAGE-COPPEUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  2. 2.Instituto de Pesquisas Jardim Botânico do Rio de JaneiroRio de JaneiroBrazil
  3. 3.Departamento de Ciências do Meio AmbienteUniversidade Federal Rural do Rio de JaneiroTrês RiosBrazil
  4. 4.Instituto de Estudos do Mar Almirante Paulo Moreira, Marinha do BrasilArraial do CaboBrazil
  5. 5.Departamento de OceanografiaUniversidade Federal do Espírito SantoVitóriaBrazil

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