Abstract
Many small, isolated north temperate waterbodies experience hypoxic conditions and winterkill events. Although such waterbodies are found in the natural ranges of two congeneric sunfishes (pumpkinseed, Lepomis gibbosus and bluegill, L. macrochirus), many contain pumpkinseed but no bluegill; a biogeographic pattern that has remained unexplained. To test whether a greater hypoxia tolerance in pumpkinseeds could explain these differences in distribution, we conducted hypoxia tolerance trials by subjecting each species to declining oxygen concentrations over ca. 16 h in aquaria. We also measured the activities of key metabolic enzymes in the muscle of wild individuals. Pumpkinseeds showed significantly higher tolerance to hypoxic stress than bluegills, as indicated by dissolved oxygen concentration at the time of equilibrium loss. Consistent with this result, white muscle from pumpkinseed had higher levels of lactate dehydrogenase, a marker enzyme for anaerobic capacity. There was no difference between species in the activity level of pyruvate kinase, suggesting that pumpkinseed do not display a general upregulation of glycolysis, but rather an upregulation of anaerobic capacity. Our results support the hypothesis that evolved differences in winter hypoxia tolerance can act as a macrohabitat partitioning mechanism in North American sunfishes.
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Almeida-Val VMF, Val AL, Duncan WP, Souza FCA, Paula-Silva MN, Land S (2000) Scaling effects on hypoxia tolerance in the Amazon fish Astronotus ocellatus (Perciformes: Cichlidae): contribution of tissue enzyme levels. Comp Biochem Physiol B 125:219–126
Arendt JD, Wilson DS (1999) Countergradient selection for rapid growth in pumpkinseed sunfish: disentangling ecological and evolutionary effects. Ecology 80:2793–2798
Booth RK (1991) A comparison of the respiratory physiology and behavior of two populations of pumkinseeds (Lepomis gibbosus) exposed to simulated winter hypoxia. BSc Thesis, Trent University, pp 7
Burleson ML, Wilhelm DR, Smatresk NJ (2001) The influence of fish size on the avoidance of hypoxia and oxygen selection by large mouth bass. J Fish Biol 59:1336–1349
Chapman LJ, Chapman CA, Ogutu-Ohwayo R, Chandler M, Kaufman S, Keiter AE (1996) Refugia for endangered fishes from an introduced predator in Lake Nabugabo, Uganda. Conserv Biol 10:554–561
Chapman LJ, Galis F, Shinn J (2000) Phenotypic plasticity and the possible role of genetic assimilation: hypoxia-induced trade-offs in morphological traits of an African cichlid. Ecol Lett 3:388–393
Coutant CC (1985) Striped bass, temperature, and dissolved oxygen: a speculative hypothesis for environmental risk. Trans Am Fish Soc 114:31–61
Dauer DM (1993) Biological criteria, environmental health and estuarine macrobenthic community structure. Mar Poll Bull 26:249–257
Davis JC (1975) Minimal dissolved oxygen requirements of aquatic life with emphasis on Canadian species: a review. J Fish Res Board Can 32:2295–2332
Fox MG, Keast A (1990) Effects of winterkill on population structure, body size and prey consumption patterns of pumpkinseed in isolated beaver ponds. Can J Zool 68:2487–2498
Hall DJ, Ehlinger TJ (1989) Perturbation, planktivory, and pelagic community structure: the consequence of winterkill in a small lake. Can J Fish Aquat Sci 46:2203–2209
Harris PM, Roe KJ, Hayden RL (2005) A mitochondrial DNA perspective on the molecular systematics of the sunfish genus Lepomis (Actinopterygii: Centrarchidae). Copeia 2005: 340–346
Hochachka PW, Stanley C, Merkt J, Sumar-Kalinowski J (1982) Metabolic meaning of elevated levels of oxidative enzymes in high altitude adapted animals: an interpretive hypothesis. Resp Physiol 52:303–313
Hochachka PW, Stanley C, McKensie DC, Villena A, Monge C (1992) Enzyme mechanisms for pyruvate-to-lactate flux attenuation: a study of Sherpas, Quechuas, and hummingbirds. Int J Sports Med 13:S119–S122
Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, Oxford, pp 466
Holopainen IJ, Pitkänen AK (1985) Population size and structure of crucian carp (Carassius Carassius (L.)) in two small, natural ponds in Eastern Finland. Ann Zool Fennici 22:397–406
Keast A (1978a) Feeding interrelations between age-groups of pumpkinseed (Lepomis gibbosus) and comparisons with bluegill (L. macrochirus). J Fish Res Board Can 35:12–27
Keast A (1978b) Trophic and spatial interrelationships in the fish species of an Ontario temperate lake. Environ Biol Fish 3:7–31
Keast A, Harker J, Turnbull D (1978) Nearshore fish habitat utilization and species associations in Lake Opinicon (Ontario, Canada). Environ Biol Fish 3:173–184
Keast A, Welsh L (1968) Daily feeding periodicities, food uptake rates, and dietary changes with hour of day in some lake fishes. J Fish Res Board Can 25:1133–1144
Keast A, Fox MG (1990) Fish community structure, spatial distribution and feeding ecology in a beaver pond. Environ Biol Fish 27:210–214
Klinger SA, Magnuson JJ, Gallepp GW (1982) Survival mechanisms of the central mudminnow (Umbra limi), fathead minnow (Pimephales promelas) and brook stickleback (Culaea inconstans) for low oxygen in winter. Environ Biol Fish 7:113–120
Magnuson JJ, Karlen DJ (1970) Visual observation of fish beneath the ice in a winterkill lake. J Fish Res Board Can 27:1059–1068
Magnuson JJ, Beckel AL, Mills K, Brandt SB (1985) Surviving winter hypoxia: behavioural adaptations of fishes in a northern Wisconsin winterkill lake. Environ Biol Fish 14: 241–250
Melnychuk MC, Chapman LJ (2002) Hypoxia tolerance of two haplochromine cichlids: Swamp leakage and potential for interlacustrine dispersal. Environ Biol Fish 65:99–110
Mittelbach GG, Osenberg CW, Wainwright PC (1999) Variation in feeding morphology between pumpkinseed populations: phenotypic plasticity or evolution? Evol Ecol Res 1:111–128
Moore WG (1942) Field studies on the oxygen requirements of certain fresh-water fishes. Ecology 23:319–329
Near TJ, Bolnick DI, Wainwright PC (2004) Investigating phylogenetic relationships of sunfishes and black basses (Actinopterygii: Centrarchidae) using DNA sequences from mitochondrial and nuclear genes. Mol Phylogenet Evol 32:344–357
Osenberg CW, Werner EE, Mittelbach GG, Hall DJ (1988) Growth patterns in bluegill (Lepomis macrochirus) and pumpkinseed (Lepomis gibbosus) sunfish: environmental variation and the importance of ontogenetic niche shifts. Can J Fish Aquat Sci 45:17–26
Petrosky BR, Magnuson JJ (1973) Behavioural responses of northern pike, yellow perch and bluegill to oxygen concentrations under simulated winterkill conditions. Copeia 1973:124–133
Peterson MS (1990) Hypoxia-induced physiological changes in two mangrove swamp fishes: Sheepshead minnow, Cyprinodon variegatus Lacepede and sailfin molly, Poecilia latipinna (Lesueur). Comp Biochem Physiol A 97:17–21
Rahel FJ (1984) Factors structuring fish assemblages along a bog lake successional gradient. Ecology 65:1276–1289
Rahel FJ, Nutzman JW (1994) Foraging in a lethal environment: fish predation in hypoxic waters of a stratified lake. Ecology 75:1246–1253
Scott WB, Crossman EJ (1973) Freshwater fishes of Canada. Bulletin 184. Fisheries Research Board of Canada, Ottawa, pp 966
Sneddon LU, Yerbury J (2004) Differences in response to hypoxia in the three-spined stickleback from lotic and lentic localities: dominance and an anaerobic metabolite. J Fish Biol 64:799–804
Somero GN, Childress JJ (1980) A violation of the metabolism size scaling paradigm: activities of glycolytic enzymes in muscle increase in larger-size fish. Physiol Zool 53:322–337
Suarez RK (1996) Upper limits to mass-specific metabolic rates. Annu Rev Physiol 58:583–605
Tonn WM, Magnuson JJ (1982) Patterns in the species composition and richness of fish assemblages in northern Wisconsin lakes. Ecology 63:1149–1166
Tonn WM, Magnuson JJ (1983) Community analysis in fishery management: an application with northern Wisconsin lakes. Trans Am Fish Soc 112:368–377
Tonn WM, Paszkowski CA (1986) Size-limited predation, winterkill, and the organization of Umbra—Perca fish assemblages. Can J Fish Aquat Sci 43:194–202
Werner EE, Hall DJ, Laughlin DR, Wagner DJ, Wilsmann LA, Funk FC (1977) Habitat partitioning in a freshwater fish community. J Fish Res Board Can 34:360–370
West JL, Bailey JR, Almeida-Val VMF, Val AL, Sidell BD, Driedzic WR (1999) Activity levels of enzymes of energy metabolism in heart and red muscle are higher in north-temperate-zone than in Amazonian teleosts. Can J Zool 77:690–696
Wu RSS (2002) Hypoxia: from molecular responses to ecosystem responses. Mar Poll Bull 45:35–45
Acknowledgements
Financial support for this research was provided by a National Science and Engineering Research Council (Canada) Discovery Grant to MGF, CDM and GB. M. Bérubé, J. MacLeod and B. Tufts provided assistance in the field. Two anonymous reviewers provided helpful comments on an earlier draft of this manuscript.
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Farwell, M., Fox, M.G., Moyes, C.D. et al. Can Hypoxia Tolerance Explain Differences in Distribution of Two Co-Occurring North Temperate Sunfishes?. Environ Biol Fish 78, 83–90 (2007). https://doi.org/10.1007/s10641-006-9079-3
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DOI: https://doi.org/10.1007/s10641-006-9079-3