Ectothermic animals are especially susceptible to temperature change, considering that their metabolism and core temperature are linked to the environmental temperature. As global water temperatures continue to increase, so does the need to understand the capacity of organisms to tolerate change. Sheepshead minnows (Cyprinodon variegatus) are the most eurythermic fish species known to date and can tolerate a wide range of environmental temperatures from − 1.9 to 43.0 °C. But little is known about the physiological adjustments that occur when these fish are subjected to acute thermal challenges and long-term thermal acclimation. Minnows were acclimated to 10, 21, or 32 °C for 4 weeks or acutely exposed to 10 and 32 °C and then assessed for swimming performance [maximum sustained swimming velocity (Ucrit), optimum swimming velocity (Uopt)] and metabolic endpoints (extrapolated standard and maximum metabolic rate [SMR, MMR), absolute aerobic scope (AS), and cost of transport (COT)]. Our findings show that the duration of thermal exposure (acute vs. acclimation) did not influence swimming performance. Rather, swimming performance was influenced by the exposure temperature. Swimming performance was statistically similar in fish exposed to 21 or 32 °C (approximately 7.0 BL s−1), but was drastically reduced in fish exposed to 10 °C (approximately 2.0 BL s−1), resulting in a left-skewed performance curve. There was no difference in metabolic end points between fish acutely exposed or acclimated to 10 °C. However, a different pattern was observed in fish exposed to 32 °C. MMR was similar between acutely exposed or acclimated fish, but acclimated fish had a 50% reduction in extrapolated SMR, which increased AS by 25%. However, this enhanced AS was not associated with changes in swimming performance, which opposes the oxygen-capacity limited thermal tolerance concept. Our findings suggest that sheepshead minnows may utilize two distinct acclimation strategies, resulting in different swimming performance and metabolic patterns observed between 10 and 32 °C exposures.
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Bennett WA, Beitinger TL (1997) Temperature tolerance of the sheepshead minnow, Cyprinodon variegatus. Copeia 1997:77–87. https://doi.org/10.2307/1447842
Billett HH (1990) Hemoglobin and hematocrit. In: Walker HK, Hall WD, Hurst JW (eds) Clinical methods: the history, physical, and laboratory examinations. Butterworth Publishers, a division of Reed Publishing, Boston
Birchard GF (1997) Optimal hematocrit: theory, regulation and implications. Am Zool 37:65–72
Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789. https://doi.org/10.1890/03-9000
Chitty JD, Able KW (2004) Habitat use, movements and growth of the sheepshead minnow, Cyprinodon variegatus, in a restored salt marsh in Delaware Bay. Bull N J Acad Sci 49:1–9
Claireaux G, Couturier C, Groison A-L (2006) Effect of temperature on maximum swimming speed and cost of transport in juvenile European sea bass (Dicentrarchus labrax). J Exp Biol 209:3420–3428
Clark TD, Sandblom E, Jutfelt F (2013) Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. J Exp Biol 216:2771–2782
Crowell JW, Ford RG, Lewis VM (1959) Oxygen transport in hemorrhagic shock as a function of the hematocrit ratio. Am J Physiol-Leg Content 196:1033–1038
Dickson KA, Donley JM, Sepulveda C, Bhoopat L (2002) Effects of temperature on sustained swimming performance and swimming kinematics of the chub mackerel Scomber japonicus. J Exp Biol 205:969–980
Duarte CM (2007) Marine ecology warms up to theory. Trends Ecol Evol 22:331–333
Ern R, Phuong NT, Wang T, Bayley M (2014) Oxygen delivery does not limit thermal tolerance in a tropical eurythermal crustacean. J Exp Biol 217:809–814
Fangue NA, Hofmeister M, Schulte PM (2006) Intraspecific variation in thermal tolerance and heat shock protein gene expression in common killifish, Fundulus heteroclitus. J Exp Biol 209:2859–2872
Fangue NA, Mandic M, Richards JG, Schulte PM (2008) Swimming performance and energetics as a function of temperature in killifish Fundulus heteroclitus. Physiol Biochem Zool 81:389–401
Fangue NA, Wunderly MA, Dabruzzi TF, Bennett WA (2014) Asymmetric thermal acclimation responses allow sheepshead minnow Cyprinodon variegatus to cope with rapidly changing temperatures. Physiol Biochem Zool 87:805–816
Farrell A (2009) Environment, antecedents and climate change: lessons from the study of temperature physiology and river migration of salmonids. J Exp Biol 212:3771–3780
Franklin CE, Davison W, Seebacher F (2007) Antarctic fish can compensate for rising temperatures: thermal acclimation of cardiac performance in Pagothenia borchgrevinki. J Exp Biol 210:3068–3074
Gräns A et al (2014) Aerobic scope fails to explain the detrimental effects on growth resulting from warming and elevated CO2 in Atlantic halibut. J Exp Biol 217:711–717
Harrington R, Harrington E (1982) Effects on fishes and their forage organisms of impounding a Florida salt marsh to prevent breeding by salt marsh mosquitoes. Bull Mar Sci 32:523–531
Healy TM, Schulte PM (2012) Thermal acclimation is not necessary to maintain a wide thermal breadth of aerobic scope in the common killifish (Fundulus heteroclitus). Physiol Biochem Zool 85:107–119. https://doi.org/10.1086/664584
Healy TM, Chung DJ, Crowther KG, Schulte PM (2017) Metabolic and regulatory responses involved in cold acclimation in Atlantic killifish, Fundulus heteroclitus. J Comp Physiol B 187:463–475. https://doi.org/10.1007/s00360-016-1042-9
Heuton M et al (2018) Oxygen consumption of desert pupfish at ecologically relevant temperatures suggests a significant role for anaerobic metabolism. J Comp Physiol B 188:821–830. https://doi.org/10.1007/s00360-018-1174-1
Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Biochemistry and Molecular Biology Education. Oxford University Press, New York
Johnson WE (1974) Morphological variation and local distribution of Cyprinodon variegatus in Florida. Retrospective theses and dissertations, 109. https://stars.library.ucf.edu/rtd/109
Johnson T, Bennett A (1995) The thermal acclimation of burst escape performance in fish: an integrated study of molecular and cellular physiology and organismal performance. J Exp Biol 198:2165–2175
Johnston IA, Temple GK (2002) Thermal plasticity of skeletal muscle phenotype in ectothermic vertebrates and its significance for locomotory behaviour. J Exp Biol 205:2305–2322
Lee C, Farrell A, Lotto A, MacNutt M, Hinch S, Healey M (2003) The effect of temperature on swimming performance and oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks. J Exp Biol 206:3239–3251
Mager EM et al (2014) Acute embryonic or juvenile exposure to Deepwater Horizon crude oil impairs the swimming performance of mahi-mahi (Coryphaena hippurus). Environ Sci Technol 48:7053–7061. https://doi.org/10.1021/es501628k
McDonnell LH, Chapman LJ (2016) Effects of thermal increase on aerobic capacity and swim performance in a tropical inland fish. Comp Biochem Physiol Part A Mol Integr Physiol 199:62–70. https://doi.org/10.1016/j.cbpa.2016.05.018
Moore RH (1976) Observations on fishes killed by cold at Port Aransas, Texas, 11–12 January 1973. Southwestern Nat 20:461–466. https://doi.org/10.2307/3669862
Nguyen KDT, Morley SA, Lai C-H, Clark MS, Tan KS, Bates AE, Peck LS (2011) Upper temperature limits of tropical marine ectotherms: global warming implications. PloS One 6:e29340–e29340. https://doi.org/10.1371/journal.pone.0029340
Norin T, Malte H, Clark TD (2014) Aerobic scope does not predict the performance of a tropical eurythermal fish at elevated temperatures. J Exp Biol 217:244–251. https://doi.org/10.1242/jeb.089755
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 Physiol 97:17–21. https://doi.org/10.1016/0300-9629(90)90715-5
Pilakouta N, Killen SS, Kristjánsson BK, Skúlason S, Lindström J, Metcalfe NB, Parsons KJ (2020) Multigenerational exposure to elevated temperatures leads to a reduction in standard metabolic rate in the wild. Funct Ecol 34:1205–1214. https://doi.org/10.1111/1365-2435.13538
Pörtner H (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146
Raimondo S, Rutter H, Hemmer B, Jackson C, Cripe G (2013) The influence of density on adults and juveniles of the estuarine fish, the sheepshead minnow (Cyprinodon variegatus). J Exp Mar Biol Ecol 439:69–75
Rummer JL, Couturier CS, Stecyk JAW, Gardiner NM, Kinch JP, Nilsson GE, Munday PL (2014) Life on the edge: thermal optima for aerobic scope of equatorial reef fishes are close to current day temperatures. Glob Change Biol 20:1055–1066. https://doi.org/10.1111/gcb.12455
Sandblom E, Gräns A, Axelsson M, Seth H (2014) Temperature acclimation rate of aerobic scope and feeding metabolism in fishes: implications in a thermally extreme future. Proc R Soc Lond B Biol Sci 281:20141490
Schnell A, Seebacher F (2008) Can phenotypic plasticity facilitate the geographic expansion of the tilapia Oreochromis mossambicus? Physiol Biochem Zool 81:733–742
Sidell BD, O’Brien KM (2006) When bad things happen to good fish: the loss of hemoglobin and myoglobin expression in Antarctic icefishes. J Exp Biol 209:1791–1802
Somero G (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. J Exp Biol 213:912–920
Stieglitz JD, Mager EM, Hoenig RH, Benetti DD, Grosell M (2016) Impacts of deepwater horizon crude oil exposure on adult mahi-mahi (Coryphaena hippurus) swim performance. Environ Toxicol Chem 35:2613–2622
Wilhelm Filho D, Eble GJ, Kassner G, Caprario FX, Dafré AL, Ohira M (1992) Comparative hematology in marine fish. Comp Biochem Physiol A Physiol 102:311–321
The authors would like to thank Dr. Aaron Roberts at the University of North Texas for supplying bench space and aquarium equipment at the UNT Environmental Science Aquatics Facility for the duration of these exposures. We would also like to thank Dr. Kurt Gamperl at Memorial University of Newfoundland for his valuable insight and recommendations during the data analysis and writing process. Lastly, we would like to thank the anonymous reviewers whose constructive feedback helped elevate this paper. This project was made possible through the University of North Texas start-up funds awarded to Dane A. Crossley and Edward M. Mager.
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Kirby, A.R., Crossley, D.A. & Mager, E.M. The metabolism and swimming performance of sheepshead minnows (Cyprinodon variegatus) following thermal acclimation or acute thermal exposure. J Comp Physiol B 190, 557–568 (2020). https://doi.org/10.1007/s00360-020-01293-2