Abstract
Many estuarine habitats are characterized by episodes of hypoxia, the frequency and severity of which may vary seasonally. Accordingly, resident fish species may show seasonal differences in their capacity to tolerate hypoxia. We have tested this hypothesis in the gulf killifish, Fundulus grandis, sampled from the Lake Pontchartrain estuary (Louisiana) at different times of the year. We measured 2 indicators of hypoxia tolerance, the frequency of aquatic surface respiration (ASR) during gradual reduction in dissolved oxygen (D.O.) and survival time during severe hypoxic stress, and found both to be significantly affected by season. Fish collected during the summer did not engage in ASR until the D.O. concentration dropped to values lower than that required to elicit ASR by fish collected during other seasons. Laboratory acclimation of fish to low oxygen did not change the relationship between ASR behavior and D.O., suggesting that the observed seasonal effect on ASR was not simply due to previous exposure of summer fish to environmental hypoxia. Furthermore, fish collected during the summer and winter had significantly longer survival times during exposure to severe hypoxia than fish collected during the fall. Survival analysis indicated that the condition of fish was positively associated with survival time, and seasonal variation in condition accounted for about half of the observed difference between survival times of fish collected during the summer and fall. Seasonal variation in ASR and survival, when taken together, demonstrate that hypoxia tolerance in F. grandis may be subject to acclimatization. An increase in hypoxia tolerance during the summer could increase survivorship of fish when exposed to elevated temperatures and low oxygen concentrations which prevail during the summer months.
Similar content being viewed by others
References cited
Atkinson, A.C. 1980. A note on the generalized information criterion for choice of a model. Biometrika 67: 413–418.
Breitburg, D.L. 1990. Near-shore hypoxia in the Chesapeake Bay: patterns and relationships among physical factors. Estuarine, Coastal and Shelf Science 30: 593–609.
Cali, F.J. 1972. Ecology of a brackish pond system in southeastern Louisiana. M.S. Thesis, University of New Orleans, New Orleans. 87 pp.
Chapman, L.J. & C.A. Chapman. 1998. Hypoxia tolerance of the mormyrid Petrocephalus catostoma: implications for persistence in swamp refugia. Copeia 1998: 762–768.
Chapman, L.J., C.A. Chapman, D.A. Brazeau, B. McLaughlin & M. Jordan. 1999. Papyrus swamps, hypoxia, and faunal diversification: variation among populations of Barbus neumayeri. J. Fish Biol. 54: 310–327.
Chapman, L.J., L.S. Kaufman, C.A. Chapman & F.E. McKenzie. 1995. Hypoxia tolerance in twelve species of East African cichlids: potential for lowoxygen refugia in LakeVictoria. Conserv. Biol. 9: 1274–1288.
Diaz, R.J. & R. Rosenberg. 1995. Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanography and Marine Biology: an Annual Review 33: 245–303.
Dixon, P.M. & M.C. Newman. 1991. Analyzing toxicity data using statistical models for time-to-death: an introduction. pp. 207–241. In: M.C. Newman & A.W. McIntosh (ed.) Metal Ecotoxicology, Concepts and Applications, Lewis Publishers, Inc., Chelsea.
Dyer, C.L. 1983. Hypoxia tolerance and habitat partitioning in two estuarine cyprinodonts, Fundulus similis and Fundulus grandis. M.S. Thesis, University of Alabama, Tuscaloosa. 51 pp.
Gee, J.H. & P.A. Gee. 1991. Reaction of gobioid fishes to hypoxia: buoyancy control and aquatic surface respiration. Copeia 1991: 17–28.
Gee, J.H., R.F. Tallman & H.J. Smart. 1978. Reactions of some great plains fishes to progressive hypoxia. Can. J. Zool. 56: 1962–1966.
Godinho, A.L. 1997. Weight-length relationship and condition of the characiform Triportheus guentheri. Env. Biol. Fish. 50: 319–330.
Greaney, G.S., A.R. Place, R.E. Cashon, G. Smith & D.A. Powers. 1980. Time course of changes in enzyme activities and blood respiratory properties of killifish during long-term acclimation to hypoxia. Physiol. Zool. 53: 136–144.
Greeley, M.S. & R. MacGregor III. 1983. Annual and semilunar reproductive cycles of the gulf killifish, Fundulus grandis, on the Alabama gulf coast. Copeia 1983: 711–718.
Hochachka, P.W. 1980. Living without oxygen: closed and open systems in hypoxia tolerance. Harvard University Press, Cambridge. 181 pp.
Hoese, H.D. & R.M. Moore. 1998. Fishes of the Gulf of Mexico, Texas, Louisiana, and adjacent waters. Texas A & M University Press, College Station. 422 pp.
Jensen, F.B., M. Nikinmaa & R.E. Weber. 1993. Environmental perturbations of oxygen transport in teleost fishes: causes, consequences and compensations. pp. 161–179. In: J.C. Rankin & F.B. Jensen (ed.) Fish Ecophysiology, Chapman & Hall, London.
Jobling, M. 1993. Bioenergetics: feed intake and energy partitioning. pp. 1-44. In: J.C. Rankin & F.B. Jensen (ed.) Fish Ecophysiology, Chapman & Hall, London.
Kramer, D.L. 1983a. Aquatic surface respiration in the fishes of Panama: distribution in relation to risk of hypoxia. Env. Biol. Fish. 8: 49–54.
Kramer, D.L. 1983b. The evolutionary ecology of respiratory mode in fishes: an analysis based on the costs of breathing. Env. Biol. Fish. 9: 145–158.
Kramer, D.L. 1987. Dissolved oxygen and fish behavior. Env. Biol. Fish. 18: 81–92.
Kramer, D.L. & M. McClure. 1982. Aquatic surface respiration, a widespread adaptation to hypoxia in tropical freshwater fishes. Env. Biol. Fish. 7: 47–55.
Kramer, D.L. & J.P. Mehegan. 1981. Aquatic surface respiration, an adaptive response to hypoxia in the guppy, Poecilia reticulata (Pisces, Poeciliidae). Env. Biol. Fish. 6: 299–313.
Lewis, M.W. 1970. Morphological adaptations of cyprinodontoids for inhabiting oxygen deficient waters. Copeia 1970: 319–326.
Malone, T.C. 1991. River flow, phytoplankton production and oxygen depletion in Chesapeake Bay. pp. 83–93. In: R.V. Tyson & T.H. Pearson (ed.) Modern and Ancient Continental Shelf Anoxia, Geological Society Special Publication No. 58, the Geological Society, London.
Malone, T.C., W.M. Kemp, H.W. Ducklow, W.R. Boynton, J.H. Tuttle & R.B. Jonas. 1986. Lateral variation in the production and fate of phytoplankton in a partially stratified estuary. Mar. Ecol. Prog. Ser. 32: 149–160.
Moss, D.D. & D.C. Scott. 1961. Dissolved-oxygen requirements of three species of fish. Trans. Amer. Fish. Soc. 90: 377–393.
Olowo, J.P. & L.J. Chapman. 1996. Papyrus swamps and variation in the respiratory behaviour of the African fish Barbus neumayeri. African J. Ecol. 34: 211–222.
Pedalino, F.M. 1999. Macrobenthic invertebrate community structure in Lake Pontchartrain' ‘dead zone’ following a summer algal bloom. M.S. Thesis, University of New Orleans, New Orleans. 131 pp.
Rees, B.B., F.A. Sudradjat & J.W. Love. 2001. Acclimation to hypoxia increases survival time of zebrafish, Danio rerio, during lethal hypoxia. J. Exp. Zool. 289: 266–272.
Seliger, H.H., J.A. Boggs & J.A. Biggley. 1985. Catastrophic anoxia in the Chesapeake Bay in 1984. Science 228: 70–73.
Shepard, M.P. 1955. Resistance and tolerance of young speckled trout (Salvelinus fontinalis) to oxygen lack, with special reference to low oxygen acclimation. J. Fish. Res. Board Can. 12: 387–446.
Sokal, R.R. & F.J. Rohlf. 1981. Biometry, 2nd ed. W.H. Freeman and Company, New York. 859 pp.
Targett, T.E. 1978. Respiratory metabolism of temperature acclimated Fundulus heteroclitus (L.): zones of compensation and dependence. J. Exp. Marine Biol. Ecol. 32: 197–206.
Turner, R.E. & N.N Rabalais. 1994. Coastal eutrophication near the Mississippi River delta. Nature 368: 619-621.
Turner, R.E., W.W. Schroeder & W.J. Wiseman, Jr. 1987. The role of stratification in the deoxygenation of Mobile Bay and adjacent shelf bottom waters. Estuaries 10: 13–19.
Tyson, R.V. & T.H. Pearson. 1991. Modern and ancient continental shelf anoxia: an overview. pp. 1–24. In: R.V. Tyson & T.H. Pearson (ed.) Modern and Ancient Continental Shelf Anoxia, Geological Society Special Publication No. 58, the Geological Society, London.
U.S. EPA. 1995. Short-term methods for estimating the chronic toxicity of effluents and receiving waters to west coast marine and estuarine organisms. United States Environmental Protection Agency, Washington, DC 436 pp.
Verheyen, E., R. Blust & W. Decleir. 1994. Metabolic rate, hypoxia tolerance and aquatic surface respiration of some lacustrine and riverine African cichlid fishes (Pisces: Cichlidae). Comp. Biochem. Physiol. A 107: 403–411.
Walsh, S.J., D.C. Haney, C.M. Timmerman & R.M. Dorazio. 1998. Physiological tolerances of juvenile robust redhorse, Moxostoma robustum: conservation implications for an imperiled species. Env. Biol. Fish. 52: 429–444.
Wells, N.A. 1935. Variations in the respiratory metabolism of the Pacific killifish Fundulus parvipinnis due to size, season, and continued constant temperature. Physiol. Zool. 8: 318–336.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Love, J.W., Rees, B.B. Seasonal Differences in Hypoxia Tolerance in Gulf Killifish, Fundulus Grandis (Fundulidae). Environmental Biology of Fishes 63, 103–115 (2002). https://doi.org/10.1023/A:1013834803665
Issue Date:
DOI: https://doi.org/10.1023/A:1013834803665