Abstract
Hypoxia tolerance and air-breathing occur in a range of freshwater, estuarine and intertidal fishes. Here it is shown for the first time that coral reef fishes from the genera Gobiodon, Paragobiodon and Caracanthus, which all have an obligate association with living coral, also exhibit hypoxia tolerance and a well-developed air-breathing capacity. All nine species maintained adequate respiration in water at oxygen concentrations down to 15–25% air saturation. This hypoxia tolerance is probably needed when the oxygen levels in the coral habitat drops sharply at night. Air-breathing abilities of the species correlated with habitat association, being greatest (equaling oxygen uptake in water) in species that occupy corals extending into shallow water, where they may become air exposed during extreme low tides. Air-breathing was less well-developed or absent in species inhabiting corals from deeper waters. Loss of scales and a network of subcutaneous capillaries appear to be key adaptations allowing cutaneous respiration in air. While hypoxia tolerance may be an ancestral trait in these fishes, air-breathing is likely to be a more recent adaptation exemplifying convergent evolution in the unrelated genera Gobiodon and Caracanthus in response to coral-dwelling lifestyles.
References
Graham JB (1976) Respiratory adaptations of marine air-breathing fishes. In: Hughes GM (ed) Respiration of amphibious vertebrates. Academic, New York, pp 65–187
Graham JB (1997) Air-breathing fishes: evolution, diversity, and adaptation. Academic, San Diego
Helfman GS, Collette BB, Facey DE (1997) The diversity of fishes. Blackwell, Malden
Hobbs J-P A, Munday PL (2004) Intraspecific competition controls spatial distribution and social organisation of the coral-dwelling goby, Gobiodon histrio. Mar Ecol Prog Ser 278:253–259
Lassig B (1976) Field observations on the reproductive behaviour of Paragobiodon spp. (Gobiidae) at Heron Island Great Barrier Reef. Mar Behav Physiol 3:283–293
Liem KL (1981) Larvae of air-breathing fishes as countercurrent flow devices in hypoxic environments. Science 211:1177–1179
Martin KLM (1995) Time and tide wait for no fish: intertidal fishes out of water. Environ Biol Fish 44:165–181
Martin KLM (1996) An ecological gradient in air-breathing ability among marine cottid fishes. Physiol Zool 69:1096–1113
Munday PL (2004) Competition among coral-dwelling fishes: the lottery model revisited. Ecology 85:623–628
Munday PL, Jones GP, Caley MJ (1997) Habitat specialisation and the distribution and abundance of coral-dwelling gobies. Mar Ecol Prog Ser 152:227–239
Munday PL, Harold AS, Winterbottom R (1999) Guide to coral-dwelling gobies (genus Gobiodon) of Papua New Guinea and the Great Barrier Reef. Revue francaise Aquariologie 26:49–54
Munday PL, Jones GP, Caley MJ (2001) Interspecific competition and coexistance in a guild of coral-dwelling fishes. Ecology 82:2177–2189
Munday PL, Schubert M, Baggio JA, Jones GP, Caley MJ, Grutter AS (2003) Skin toxins and external parasitism in coral-dwelling gobies. J Fish Biol 62:976–981
Munday PL, van Herwerden L, Dudgeon C (2004) Evidence for sympatric speciation by host shift in the sea. Curr Biol 14:1498–1504
Nilsson GE (1996) Brain and body oxygen requirements of Gnathonemus petersii, a fish with an exceptionally large brain. J Exp Biol 199:603–607
Nilsson GE, Östlund-Nilsson S (2004) Hypoxia in paradise: widespread hypoxia tolerance in coral reef fishes. Proc R Soc Lond B (Biol Lett Suppl) 271:S30–S33
Nilsson GE, Hobbs JP, Munday PL, Östlund-Nilsson S (2004) Coward or braveheart: extreme habitat fidelity through hypoxia tolerance in a coral-dwelling goby. J Exp Biol 207:33–39
Nilsson GE, Renshaw GMC (2004) Hypoxic survival strategies in two fishes: extreme anoxia tolerance in the North European crucian carp and natural hypoxic preconditioning in a coral-reef shark. J Exp Biol 207:3131–3139
Nilsson GE, Östlund-Nilsson S (2006) Hypoxia tolerance in coral reef fishes. In: Val AL, Val VM, Randall DJ (eds) Fish physiology: the physiology of tropical fishes, vol 21. Academic/Elsevier, Amsterdam, pp 583–596
Piiper J (1982) Respiratory gas exchange at lungs, gills and tissues: mechanisms and adjustments. J Exp Biol 100:5–22
Prosser CL, Brown FA (1961) Comparative animal physiology. WB Saunders Co, Philadelphia
Randall JE, Allen RG, Steene RC (1997) Fishes of the Great Barrier Reef and Coral Sea. Crawford House Publishing, Bathurst
Schubert M, Munday PL, Caley MJ, Jones GP, Llewellyn LE (2003) The toxicity of skin secretions from coral-dwelling gobies and their potential role as a predator deterrent. Environ Biol Fish 67:359–367
Shinohara G, Imamura H (2005). Anatomical description and phylogenetic classification of the orbicular velvetfishes (Scorpaenoidea: Caracanthus). Ichthyol Res 52:64–76
Thompson GG, Withers PC (2002) Aerial and aquatic respiration of the Australian desert goby, Chlamydogobius eremius. Comp Biochem Physiol A 131:871–879
Val AL, Silva MNP, Almeida-Val VMF (1998) Hypoxia adaptation in fish of the Amazon: a never-ending task. S Afr J Zool 33:107–114
Wong M, Munday PL, Jones GP (2005) Habitat patch size, facultative monogamy and sex change in a coral-dwelling reef fish. Environ Biol Fishes 74:141–150
Acknowledgments
We thank the personnel of Lizard Island Research Station for assistance. The study was financed by the Research Council of Norway and the Australian Research Council.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Biology Editor M.I. McCormick.
Rights and permissions
About this article
Cite this article
Nilsson, G.E., Hobbs, JP.A., Östlund-Nilsson, S. et al. Hypoxia tolerance and air-breathing ability correlate with habitat preference in coral-dwelling fishes. Coral Reefs 26, 241–248 (2007). https://doi.org/10.1007/s00338-006-0167-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-006-0167-9