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Coral Reefs

, Volume 34, Issue 3, pp 823–833 | Cite as

Fish mucus versus parasitic gnathiid isopods as sources of energy and sunscreens for a cleaner fish

  • Maxi Eckes
  • Sophie Dove
  • Ulrike E. Siebeck
  • Alexandra S. GrutterEmail author
Report

Abstract

The cleaning behaviour of the bluestreak cleaner wrasse Labroides dimidiatus is extensively used as a model system for understanding cooperation. It feeds mainly on blood-sucking gnathiid isopods and also on the epidermal mucus of client fish; the nutritional quality of these foods, however, is unknown. The epidermal mucus of reef fish contains ultraviolet (UV)-absorbing compounds (mycosporine-like amino acids, MAAs), which are only obtained via the diet; nevertheless, while La. dimidiatus has high amounts of MAAs in its mucus, their source is unknown. Therefore, the energetic value (calories and protein estimated using carbon and nitrogen) and MAA level in gnathiids and mucus from several clients [parrotfishes, wrasses (Labridae), and a snapper (Lutjanidae)] were determined. The energetic value of mucus and gnathiids varied among fishes. Overall, carbon, nitrogen, calories, and protein per dry weight were higher in the mucus of most client species compared to gnathiids. Thus, depending on the client species, mucus may be energetically more advantageous for cleaner wrasse to feed on than gnathiids. UV absorbance, a confirmed proxy for MAA levels, indicated high MAA levels in mucus, whereas gnathiids had no detectable MAAs. This suggests that La. dimidiatus obtain MAAs from mucus but not from gnathiids. Hence, in addition to energy, the mucus of some clients also provides La. dimidiatus with the added bonus of UV-absorbing compounds. This may explain why cleaner fish prefer to feed on mucus over gnathiid isopods. The likely costs and benefits to clients of the removal of UV protecting mucus and parasitic gnathiids, respectively, and the variation in benefits gained by cleaner fish from feeding on these foods may explain some variation in cooperation levels in cleaning interactions.

Keywords

Mycosporine-like amino acids (MAA) Fish mucus Cleaning behaviour Ultraviolet (UV) absorbance UV protection Calories 

Notes

Acknowledgments

Thanks to J. Fenton, L. Curtis, and T. Byrne for their field assistance. Sirada Oratanachai helped with formatting of the manuscript. Staffs of Lizard Island Research Station, a facility of the Australian Museum, are greatly appreciated for their help. This work was funded by a Seaworld Research and Rescue Foundation award (ME), the ARC Centre of Excellence for Coral Reef Studies (SD), and The University of Queensland Foundation Research Excellence Award (ASG). This study was conducted under the approval of The University of Queensland Ethics Committee.

References

  1. Adam TC (2010) High-quality habitat and facilitation ameliorate competitive effects of prior residents on new settlers. Oecologia 166:121–130PubMedCentralPubMedCrossRefGoogle Scholar
  2. Anger K, Schultze K (1995) Elemental composition (Chn), growth and exuvial loss in the larval stages of 2 semiterrestrial crabs, Sesarma-Curacaoense and Armases-Miersii (Decapoda, Grapsidae). Comp Biochem Physiol A Physiol 111:615–623CrossRefGoogle Scholar
  3. Arnal C, Morand S (2001) Importance of ectoparasites and mucus in cleaning interactions in the Mediterranean cleaner wrasse Symphodus melanocercus. Mar Biol 138:777–784CrossRefGoogle Scholar
  4. Arnal C, Cote IM, Morand S (2001) Why clean and be cleaned? The importance of client ectoparasites and mucus in a marine cleaning symbiosis. Behav Ecol Sociobiol 51:1–7CrossRefGoogle Scholar
  5. Banaszak AT, Lesser MP (2009) Effects of solar ultraviolet radiation on coral reef organisms. Photochem Photobiol Sci 8:1276–1294PubMedCrossRefGoogle Scholar
  6. Bansemer C, Grutter AS, Poulin R (2002) Geographic variation in the behaviour of the cleaner fish Labroides dimidiatus (Labridae). Ethology 108:353–366CrossRefGoogle Scholar
  7. Bentley R (1990) The Shikimate pathway—a metabolic tree with many branches. Crit Rev Biochem Mol Biol 25:307–384PubMedCrossRefGoogle Scholar
  8. Bshary R (2011) Machiavellian intelligence in fishes. In: Brown C, Laland K, Krause J (eds) Fish cognition and behavior. Wiley, Oxford, pp 277–297CrossRefGoogle Scholar
  9. Bshary R, Grutter AS (2002a) Asymmetric cheating opportunities and partner control in the cleaner fish mutualism. Anim Behav 63:547–555CrossRefGoogle Scholar
  10. Bshary R, Grutter AS (2002b) Parasite distribution on client reef fish determines cleaner fish foraging patterns. Mar Ecol Prog Ser 235:217–222CrossRefGoogle Scholar
  11. Bshary R, Schaffer D (2002) Choosy reef fish select cleaner fish that provide high-quality service. Anim Behav 63:557–564CrossRefGoogle Scholar
  12. Byrne JE (1970) Mucous envelope formation in two species of Hawaiian parrotfishes (Genus Scarus). Pac Sci 24:490–493Google Scholar
  13. Carreto JI, Carignan MO (2011) Mycosporine-like amino acids: relevant secondary metabolites. Chemical and ecological aspects. Mar Drugs 9:387–446PubMedCentralPubMedCrossRefGoogle Scholar
  14. Carreto JI, Carignan MO, Montoya NG (2001) Comparative studies on mycosporine-like amino acids, paralytic shellfish toxins and pigment profiles of the toxic dinoflagellates Alexandrium tamarense, A. catenella and A. minutum. Mar Ecol Prog Ser 223:49–60CrossRefGoogle Scholar
  15. Choat JH (1969) Studies on labroid fishes (Labridae and Scaridae) at Heron Island, Great Barrier Reef part 2. Ph.D. thesis, University of Queensland, p 294Google Scholar
  16. Choat JH (1991) The biology of herbivorous fishes on coral reefs. In: Sale PF (ed) The ecology of fishes on coral reefs. Academic Press, San Diego, pp 120–155CrossRefGoogle Scholar
  17. Coile AM, Sikkel PC (2013) An experimental field test of susceptibility to ectoparasitic gnathiid isopods among Caribbean reef fishes. Parasitology 140:888–896PubMedCrossRefGoogle Scholar
  18. Coile AM, Welicky RL, Sikkel PC (2014) Female Gnathia marleyi (Isopoda: Gnathiidae) feeding on more susceptible fish hosts produce larger but not more offspring. Parasitol Res 113:3875–3880PubMedCrossRefGoogle Scholar
  19. Coles SL, Strathmann R (1973) Observations on coral mucus flocs and their potential trophic significance. Limnol Oceanogr 18:673–678CrossRefGoogle Scholar
  20. Crossman DJ, Clements KD, Cooper GJS (2000) Determination of protein for studies of marine herbivory: a comparison of methods. J Exp Mar Bio Ecol 244:45–65CrossRefGoogle Scholar
  21. Davies AJ, Curtis L, Grutter AS, Smit NJ (2009) Suspected viral erythrocytic necrosis (VEN) in a juvenile blackbar triggerfish, Rhinecanthus aculeatus, from Lizard Island, Great Barrier Reef, Australia. Mar Biodivers Rec 2:e149CrossRefGoogle Scholar
  22. Davies AJ, Smit NJ, Hayes PM, Seddon AM, Wertheim D (2004) Haemogregarina bigemina (Protozoa: Apicomplexa: Adeleorina)—Past, present and future. Folia Parasitol (Praha) 51:99–108CrossRefGoogle Scholar
  23. Dunlap WC, Shick JM (1998) Ultraviolet radiation-absorbing mycosporine-like amino acids in coral reef organisms: a biochemical and environmental perspective. J Phycol 34:418–430CrossRefGoogle Scholar
  24. Eckes MJ, Siebeck UE, Dove S, Grutter AS (2008) Ultraviolet sunscreens in reef fish mucus. Mar Ecol Prog Ser 353:203–211CrossRefGoogle Scholar
  25. Foster SA (1985) Wound healing: a possible role of cleaning stations. Copeia 1985:875–880CrossRefGoogle Scholar
  26. Gerking SD (1994) Fish that eat other fish and some unusual sources of food. In: Gerking SD (ed) Feeding ecology of fish. Academic Press, New York, pp 265–295CrossRefGoogle Scholar
  27. Gorlick DL (1980) Ingestion of host fish surface mucus by the Hawaiian cleaning wrasse, Labroides phthirophagus (Labridae), and its effect on host species preference. Copeia 4:863–868CrossRefGoogle Scholar
  28. Gorlick D (1984) Preference for ectoparasite-infected host fishes by the Hawaiian cleaning wrasse, Labroides phthirophagus (Labridae). Copeia 1984:758–762CrossRefGoogle Scholar
  29. Grutter AS (1994) Spatial and temporal variations of the ectoparasites of 7 reef fish species from Lizard Island and Heron Island, Australia. Mar Ecol Prog Ser 115:21–30CrossRefGoogle Scholar
  30. Grutter AS (1995a) Comparison of methods for sampling ectoparasites from coral reef fishes. Mar Freshw Res 46:897–903CrossRefGoogle Scholar
  31. Grutter AS (1995b) Relationship between cleaning rates and ectoparasite loads in coral reef fishes. Mar Ecol Prog Ser 118:51–58CrossRefGoogle Scholar
  32. Grutter AS (1996) Parasite removal rates by the cleaner wrasse Labroides dimidiatus. Mar Ecol Prog Ser 130:61–70CrossRefGoogle Scholar
  33. Grutter AS (1997) Spatio-temporal variation and feeding selectivity in the diet of the cleaner fish Labroides dimidiatus. Copeia 1997:346–355CrossRefGoogle Scholar
  34. Grutter AS (2001) Parasite infection rather than tactile stimulation is the proximate cause of cleaning behaviour in reef fish. Proc R Soc Lond B Biol Sci 268:1361–1365CrossRefGoogle Scholar
  35. Grutter AS (2002) Cleaning behaviour: from the parasite’s perspective. Parasitology 124:S65–S81PubMedCrossRefGoogle Scholar
  36. 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 164:263–271CrossRefGoogle Scholar
  37. Grutter AS, Bshary R (2003) Cleaner wrasse prefer client mucus: support for partner control mechanisms in cleaning interactions. Proc R Soc Lond B Biol Sci 270:S242–S244CrossRefGoogle Scholar
  38. Grutter AS, Bshary R (2004) Cleaner fish, Labroides dimidiatus, diet preferences for different types of mucus and parasitic gnathiid isopods. Anim Behav 68:583–588CrossRefGoogle Scholar
  39. Grutter AS, Irving AD (2007) Positive interactions in marine communities. In: Connell SD, Gillanders BM (eds) Marine ecology. Oxford University Press, Melbourne, pp 110–137Google Scholar
  40. Grutter AS, Glover S, Bshary R (2005) Does client size affect cleaner fish choice of client? An empirical test using client fish models. J Fish Biol 66:1748–1752CrossRefGoogle Scholar
  41. Grutter AS, Rumney JG, Franklin CE (2011) Fish mucous cocoons: the ‘mosquito nets’ of the sea. Biol Lett 7:292–294PubMedCentralPubMedCrossRefGoogle Scholar
  42. Holland B, Welch AA, Unwin ID, Buss DH, Paul AA, Southgate AT (1991) McCance and Widdowson’s the composition of foods. Royal Society of Chemistry and Ministry of Agriculture, Fisheries and Food, CambridgeGoogle Scholar
  43. Lenke R (1991) The opercular gland of the cleaner-wrasse Labroides dimidiatus(Labridae), a light-, electron and scanning electron microscopic investigation. J Fish Biol 39:383–392CrossRefGoogle Scholar
  44. Lewis RW (1970) Fish cutaneous mucus: a new source of skin surface lipid. Lipids 5:947–949CrossRefGoogle Scholar
  45. Losey GS Jr (1972) The ecological importance of cleaning symbiosis. Copeia 4:820–833CrossRefGoogle Scholar
  46. Losey GS Jr (1974) Cleaning symbiosis in Puerto Rico with comparison to the tropical pacific. Copeia 1974:960–970CrossRefGoogle Scholar
  47. Masiri I, Nunez M, Weller E (2008) A 10-year climatology of solar radiation for the Great Barrier Reef: implications for recent mass coral bleaching events. Int J Remote Sens 29:4443–4462CrossRefGoogle Scholar
  48. Nagel L, Grutter AS (2007) Host preference and specialisation in Gnathia sp., a common parasitic isopod of coral reef fishes. J Fish Biol 70:497–508CrossRefGoogle Scholar
  49. Niimi AJ (1972) Total nitrogen, non-protein nitrogen and protein content in largemouth bass (Micropterus salmoides) with reference to quantitative protein estimates. Can J Zool 50:1607–1610CrossRefGoogle Scholar
  50. Parsons TR, Stephens K, Strickland JDH (1961) On the chemical composition of 11 species of marine phytoplankters. J Fish Board Can 18:1001–1016CrossRefGoogle Scholar
  51. Plack PA, Fraser NW, Grant PT, Middleton C, Mitchell AI, Thompsom RH (1981) Gadusol, an enolic derivative of cyclohexane-1,3-dione present in the roes of cod and other marine fish—isolation, properties and occurrence compared with ascorbic-acid. Biochem J 199:741–747PubMedCentralPubMedGoogle Scholar
  52. Platt T, Brawn VM, Irwin B (1969) Caloric and carbon equivalents of zooplankton biomass. J Fish Board Can 26:2345–2349CrossRefGoogle Scholar
  53. Potts GW (1973) The ethology of Labroides dimidiatus (Cuv. and Val.) (Labridae, Pisces) on aldabra. Anim Behav 21:250–291CrossRefGoogle Scholar
  54. Randall JE (1958) A review of the labrid fish genus Labroides, with description of two new species and notes on ecology. Pac Sci 12:327–347Google Scholar
  55. Shephard KL (1994) Functions for fish mucus. Rev Fish Biol Fish 4:401–429CrossRefGoogle Scholar
  56. Sikkel PC, Schaumburg CS, Mathenia JK (2006) Diel infestation dynamics of gnathiid isopod larvae parasitic on Caribbean reef fish. Coral Reefs 25:683–689CrossRefGoogle Scholar
  57. 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 92:778–788PubMedCrossRefGoogle Scholar
  58. Stevens CE, Hume ID (1995) Comparative physiology of the vertebrate digestive system. University Press, CambridgeGoogle Scholar
  59. Svavarsson J, Bruce NL (2012) New and little-known gnathiid isopod crustaceans (Cymothoida) from the northern Great Barrier Reef and the Coral Sea. Zootaxa 3380:1–33Google Scholar
  60. Van Oosten J (1957) Physiology of fishes. Academic Press, New YorkGoogle Scholar
  61. White TCR (1993) The inadequate environment: nitrogen and the abundance of animals. Springer, BerlinCrossRefGoogle Scholar
  62. Zamzow JP (2003) The physiological ecology of UV-absorbing compounds in the mucus of marine fishes, Ph.D. thesis, University of Hawaii, p 113Google Scholar
  63. Zamzow JP (2004) Effects of diet, ultraviolet exposure, and gender on the ultraviolet absorbance of fish mucus and ocular structures. Mar Biol 144:1057–1064CrossRefGoogle Scholar
  64. Zamzow J, Losey GS Jr (2002) Ultraviolet radiation absorbance by coral reef fish mucus: photo-protection and visual communication. Env Biol Fishes 63:41–47CrossRefGoogle Scholar
  65. Zamzow JP, Siebeck UE (2006) Ultraviolet absorbance of the mucus of a tropical damselfish: effects of ontogeny, captivity and disease. J Fish Biol 69:1583–1594CrossRefGoogle Scholar
  66. Zamzow JP, Eckes MJ, Siebeck UE, Grutter AS (2013) Ultraviolet-B wavelengths regulate changes in UV absorption of cleaner fish mucus. PLoS One 8:e78527PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Maxi Eckes
    • 1
  • Sophie Dove
    • 1
    • 2
  • Ulrike E. Siebeck
    • 3
    • 4
  • Alexandra S. Grutter
    • 1
    Email author
  1. 1.School of Biological SciencesThe University of QueenslandSt. LuciaAustralia
  2. 2.ARC Centre for Excellence in Coral Reef StudiesThe University of QueenslandSt. LuciaAustralia
  3. 3.Sensory Neurobiology Group, School of Biomedical SciencesThe University of QueenslandSt. LuciaAustralia
  4. 4.Global Change Institute and Visual Neuroethology group, SBMSThe University of QueenslandSt. LuciaAustralia

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