Marine Biodiversity

, Volume 49, Issue 2, pp 1037–1041 | Cite as

A dark side of cleaning symbiosis: manned submersible observations

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


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.


Caridea Abrolhos Deep reefs Mutualism Diel cycles 



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 (, 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)


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Copyright information

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

Authors and Affiliations

  • Rodrigo L. Moura
    • 1
    Email author
  • 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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