Abstract
For effective conservation and management of marine systems, it is essential that we understand the biological impacts of and capacity for acclimation to increased ocean temperatures. This study investigated for the first time the effects of developing in projected warmer ocean conditions in the tropical wrasse species: Halichoeres melanurus, Halichoeres miniatus and Thalassoma amblycephalum. New recruits were reared for 11 weeks in control (29 °C) and +2 °C (31 °C) temperature treatments, consistent with predicted increases in sea surface temperature by 2100. A broad range of key attributes and performance parameters was tested, including aerobic metabolism, swimming ability, burst escape performance and physical condition. Response latency of burst performance was the only performance parameter in which evidence of beneficial thermal developmental acclimation was found, observed only in H. melanurus. Generally, development in the +2 °C treatment came at a significant cost to all species, resulting in reduced growth and physical condition, as well as metabolic and swimming performance relative to controls. Development in +2 °C conditions exacerbated the effects of warming on aerobic metabolism and swimming ability, compared to short-term warming effects. Burst escape performance parameters were only mildly affected by development at +2 °C, with non-locomotor performance (response latency) showing greater thermal sensitivity than locomotor performance parameters. These results indicate that the effects of future climate change on tropical wrasses would be underestimated with short-term testing. This study highlights the importance of holistic, longer-term developmental experimental approaches, with warming found to yield significant, species-specific responses in all parameters tested.
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References
Allan BJ, Domenici P, Munday PL, McCormick MI (2015) Feeling the heat: the effect of acute temperature changes on predator–prey interactions in coral reef fish. Conserv Physiol 3:cov011
Allan BJ, Miller GM, McCormick MI, Domenici P, Munday PL (2014) Parental effects improve escape performance of juvenile reef fish in a high-CO2 world. Proc R Soc Lond B Biol Sci 281:20132179
Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, Oxford
Angilletta MJ, Wilson RS, Navas CA, James RS (2003) Tradeoffs and the evolution of thermal reaction norms. Trends Ecol Evol 18:234–240
Beddow TA, Johnston I (1995) Plasticity of muscle contractile properties following temperature acclimation in the marine fish Myoxocephalus scorpius. J Exp Biol 198:193–201
Berkström C, Jones GP, McCormick MI, Srinivasan M (2012) Ecological versatility and its importance for the distribution and abundance of coral reef wrasses. Mar Ecol Prog Ser 461:151–163
Blaxter J, Fuiman L (1990) The role of the sensory systems of herring larvae in evading predatory fishes. J Mar Biol Assoc UK 70:413–427
Brett JR (1964) The respiratory metabolism and swimming performance of young sockeye salmon. Can J Fish Aquat Sci 21:1183–1226
Cheung WW, Sarmiento JL, Dunne J, Frölicher TL, Lam VW, Palomares MD, Watson R, Pauly D (2013) Shrinking of fishes exacerbates impacts of global ocean changes on marine ecosystems. Nat Clim Chang 3:254–258
Clark TD, Sandblom E, Jutfelt F (2013) Aerobic scope measurements of fishes in an era of climatic change: respirometry, relevance and recommendations. J Exp Biol 216:2771–2782
Daufresne M, Lengfellner K, Sommer U (2009) Global warming benefits the small in aquatic ecosystems. Proc Natl Acad Sci U S A 106:12788–12793
Domenici P (2010) Context-dependent variability in the components of fish escape response: integrating locomotor performance and behavior. J Exp Zool A Ecol Genet Physiol 313:59–79
Domenici P, Blake R (1997) The kinematics and performance of fish fast-start swimming. J Exp Biol 200:1165–1178
Domenici P, Lefrancois C, Shingles A (2007) Hypoxia and the antipredator behaviours of fishes. Philos Trans R Soc Lond B Biol Sci 362:2105–2121
Donelson JM (2015) Development in a warm future ocean may enhance performance in some species. J Exp Mar Bio Ecol 472:119–125
Donelson JM, Munday PL (2012) Thermal sensitivity does not determine acclimation capacity for a tropical reef fish. J Anim Ecol 81:1126–1131
Donelson JM, Munday PL (2015) Transgenerational plasticity mitigates the impact of global warming to offspring sex ratios. Glob Chang Biol 21:2954–2962
Donelson JM, Munday PL, McCormick MI, Pitcher CR (2012) Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat Clim Chang 2:30–32
Donelson JM, Munday PL, McCormick MI, Nilsson GE (2011) Acclimation to predicted ocean warming through developmental plasticity in a tropical reef fish. Glob Chang Biol 17:1712–1719
Donelson JM, Munday PL, McCormick MI, Pankhurst NW, Pankhurst PM (2010) Effects of elevated water temperature and food availability on the reproductive performance of a coral reef fish. Mar Ecol Prog Ser 401:233–243
Drucker EG (1996) The use of gait transition speed in comparative studies of fish locomotion. Am Zool 36:555–566
Fuiman LA, Meekan MG, McCormick MI (2010) Maladaptive behavior reinforces a recruitment bottleneck in newly settled fishes. Oecologia 164:99–108
Fulton CJ, Bellwood DR (2002) Patterns of foraging in labrid fishes. Mar Ecol Prog Ser 226:135–142
Gardiner NM, Munday PL, Nilsson GE (2010) Counter-gradient variation in respiratory performance of coral reef fishes at elevated temperatures. PLoS One 5:e13299
Gräns A, Jutfelt F, Sandblom E, Jönsson E, Wiklander K, Seth H, Olsson C, Dupont S, Ortega-Martinez O, Einarsdottir I (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
Grenchik MK, Donelson JM, Munday PL (2013) Evidence for developmental thermal acclimation in the damselfish, Pomacentrus moluccensis. Coral Reefs 32:85–90
Hanel R, Wieser W (1996) Growth of swimming muscles and its metabolic cost in larvae of whitefish at different temperatures. J Fish Biol 48:937–951
Hoey AS, McCormick MI (2004) Selective predation for low body condition at the larval–juvenile transition of a coral reef fish. Oecologia 139:23–29
Hubble M (2003) The ecological significance of body size in tropical wrasses (Pisces: Labridae). Ph.D. thesis, James Cook University, Townsville
Huey RB, Kingsolver JG (1989) Evolution of thermal sensitivity of ectotherm performance. Trends Ecol Evol 4:131–135
IPCC (2014) Climate change 2014: synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Pachauri RK, Allen MR, Barros VR, Broome J, Cramer W, Christ R, Church JA, Clarke L, Dahe Q, Dasgupta P, Dubash NK (eds). IPCC, Geneva, Switzerland
Jackson JBC (2008) Ecological extinction and evolution in the brave new ocean. Proc Natl Acad Sci U S A 105:11458–11465
Janzen DH (1967) Why mountain passes are higher in the tropics. Am Nat 101:233–249
Johansen JL, Jones GP (2011) Increasing ocean temperature reduces the metabolic performance and swimming ability of coral reef damselfishes. Glob Chang Biol 17:2971–2979
Johansen JL, Steffensen JF, Jones GP (2015) Winter temperatures decrease swimming performance and limit distributions of tropical damselfishes. Conserv Physiol 3:cov039
Johansen JL, Messmer V, Coker DJ, Hoey AS, Pratchett MS (2013) Increasing ocean temperatures reduce activity patterns of a large commercially important coral reef fish. Glob Chang Biol 20:1067–1074
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
Karino K, Kuwamura T, Nakashima Y, Sakai Y (2000) Predation risk and the opportunity for female mate choice in a coral reef fish. J Ethol 18:109–114
McCormick MI, Ryen CA, Munday PL, Walker SPW (2010) Differing mechanisms underlie sexual size-dimorphism in two populations of a sex-changing fish. PLoS One 5:e10616
Moyes C, Schulte P, West T (1993) Burst exercise recovery metabolism in fish white muscle. In: Hochachka P, Lutz P, Sick T, Rosenthal M, van den Thillart G (eds) Surviving hypoxia: mechanisms of control and adaptation. CRC Press, Florida, pp 527–539
Munday PL, Kingsford MJ, O’Callaghan M, Donelson JM (2008a) Elevated temperature restricts growth potential of the coral reef fish Acanthochromis polyacanthus. Coral Reefs 27:927–931
Munday PL, Jones GP, Pratchett MS, Williams AJ (2008b) Climate change and the future for coral reef fishes. Fish Fish 9:261–285
Munday P, Ryen C, McCormick M, Walker S (2009) Growth acceleration, behaviour and otolith check marks associated with sex change in the wrasse Halichoeres miniatus. Coral Reefs 28:623–634
Nilsson GE, Östlund-Nilsson S (2004) Hypoxia in paradise: widespread hypoxia tolerance in coral reef fishes. Proc R Soc Lond B Biol Sci 271:S30–S33
Nilsson GE, Östlund-Nilsson S, Munday PL (2010) Effects of elevated temperature on coral reef fishes: loss of hypoxia tolerance and inability to acclimate. Comp Biochem Physiol A Mol Integr Physiol 156:389–393
Nilsson GE, Östlund-Nilsson S, Penfold R, Grutter AS (2007) From record performance to hypoxia tolerance: respiratory transition in damselfish larvae settling on a coral reef. Proc R Soc Lond B Biol Sci 274:79–85
Paaijmans KP, Heinig RL, Seliga RA, Blanford JI, Blanford S, Murdock CC, Thomas MB (2013) Temperature variation makes ectotherms more sensitive to climate change. Glob Chang Biol 19:2373–2380
Poloczanska ES, Brown CJ, Sydeman WJ, Kiessling W, Schoeman DS, Moore PJ, Brander K, Bruno JF, Buckley LB, Burrows MT, Duarte CM, Halpern BS, Holding J, Kappel CV, O’Connor MI, Pandolfi JM, Parmesan C, Schwing F, Thompson SA, Richardson AJ (2013) Global imprint of climate change on marine life. Nat Clim Chang 3:919–925
Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97
Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322:690–692
Pörtner HO, Bennett AF, Bozinovic F, Clarke A, Lardies MA, Lucassen M, Pelster B, Schiemer F, Stillman JH (2006) Trade-offs in thermal adaptation: the need for a molecular to ecological integration. Physiol Biochem Zool 79:295–313
Randall JE, Allen GR, Steene RC (1997) Fishes of the Great Barrier Reef and Coral Sea. University of Hawaii Press, Honolulu
Rodgers G, Tenzing P, Clark T (2016) Experimental methods in aquatic respirometry: the importance of mixing devices and accounting for background respiration. J Fish Biol 88:65–80
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 Chang Biol 20:1055–1066
Schaefer J, Ryan A (2006) Developmental plasticity in the thermal tolerance of zebrafish Danio rerio. J Fish Biol 69:722–734
Scott GR, Johnston IA (2012) Temperature during embryonic development has persistent effects on thermal acclimation capacity in zebrafish. Proc Natl Acad Sci USA 109:14247–14252
Seebacher F, Ward A, Wilson R (2013) Increased aggression during pregnancy comes at a higher metabolic cost. J Exp Biol 216:771–776
Seebacher F, Holmes S, Roosen NJ, Nouvian M, Wilson RS, Ward AJ (2012) Capacity for thermal acclimation differs between populations and phylogenetic lineages within a species. Funct Ecol 26:1418–1428
Sheridan JA, Bickford D (2011) Shrinking body size as an ecological response to climate change. Nat Clim Chang 1:401–406
Steffensen JF (1989) Some errors in respirometry of aquatic breathers: how to avoid and correct for them. Fish Physiol Biochem 6:49–59
Stillman JH, Somero GN (2000) A comparative analysis of the upper thermal tolerance limits of eastern Pacific porcelain crabs, Genus Petrolisthes: influences of latitude, vertical zonation, acclimation, and phylogeny. Physiol Biochem Zool 73:200–208
Stobutzki IC, Bellwood DR (1994) An analysis of the sustained swimming abilities of pre-and post-settlement coral reef fishes. J Exp Mar Bio Ecol 175:275–286
Sunday JM, Bates AE, Dulvy NK (2011) Global analysis of thermal tolerance and latitude in ectotherms. Proc R Soc Lond B Biol Sci 278:1823–1830
Svendsen M, Bushnell P, Steffensen J (2015) Design and setup of intermittent-flow respirometry system for aquatic organisms. J Fish Biol 88:26–50
Szabo TM, Brookings T, Preuss T, Faber DS (2008) Effects of temperature acclimation on a central neural circuit and its behavioral output. J Neurophysiol 100:2997–3008
Temple GK, Johnston I (1998) Testing hypotheses concerning the phenotypic plasticity of escape performance in fish of the family Cottidae. J Exp Biol 201:317–331
Tewksbury JJ, Huey RB, Deutsch CA (2008) Putting the heat on tropical animals. Science 320:1296–1297
Vigliola L, Meekan MG (2002) Size at hatching and planktonic growth determine post-settlement survivorship of a coral reef fish. Oecologia 131:89–93
Vilchis LI, Tegner MJ, Moore JD, Friedman CS, Riser KL, Robbins TT, Dayton PK (2005) Ocean warming effects on growth, reproduction, and survivorship of southern California abalone. Ecol Appl 15:469–480
Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin J-M, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395
Westneat M (2001) Labridae. Wrasses, hogfishes, razorfishes, corises, tuskfishes. In: Carpenter KE, Niem V (eds) FAO species identification guide for fishery purposes. The living marine resources of the Western Central Pacific. FAO, Rome, pp 3381–3467
Acknowledgements
We thank staff at the JCU aquarium facility for technical assistance, and volunteers D. Rowen, R. Streit and D. Warren for their help during the project. Thanks to P.L. Munday for guidance and feedback throughout, and to the two reviewers, whose insightful and thorough comments helped to improve the manuscript. Funding was provided by the Ian Potter Foundation (JMD) and University of Technology Sydney (JMD). This research was conducted under JCU ethics approval A1990.
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An erratum to this article is available at http://dx.doi.org/10.1007/s00338-017-1580-y.
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Motson, K., Donelson, J.M. Limited capacity for developmental thermal acclimation in three tropical wrasses. Coral Reefs 36, 609–621 (2017). https://doi.org/10.1007/s00338-017-1546-0
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DOI: https://doi.org/10.1007/s00338-017-1546-0