Advertisement

Coral Reefs

, Volume 36, Issue 2, pp 609–621 | Cite as

Limited capacity for developmental thermal acclimation in three tropical wrasses

  • K. Motson
  • J. M. Donelson
Report

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.

Keywords

Climate change Thermal sensitivity Plasticity Swimming Burst escape performance Metabolism 

Notes

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.

Supplementary material

338_2017_1546_MOESM1_ESM.docx (72 kb)
Supplementary material 1 (DOCX 71 kb)

References

  1. 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:cov011CrossRefPubMedPubMedCentralGoogle Scholar
  2. 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 281:20132179CrossRefGoogle Scholar
  3. Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, OxfordCrossRefGoogle Scholar
  4. Angilletta MJ, Wilson RS, Navas CA, James RS (2003) Tradeoffs and the evolution of thermal reaction norms. Trends Ecol Evol 18:234–240CrossRefGoogle Scholar
  5. Beddow TA, Johnston I (1995) Plasticity of muscle contractile properties following temperature acclimation in the marine fish Myoxocephalus scorpius. J Exp Biol 198:193–201PubMedGoogle Scholar
  6. 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 461:151–163CrossRefGoogle Scholar
  7. Blaxter J, Fuiman L (1990) The role of the sensory systems of herring larvae in evading predatory fishes. J Mar Biol Assoc UK 70:413–427CrossRefGoogle Scholar
  8. Brett JR (1964) The respiratory metabolism and swimming performance of young sockeye salmon. Can J Fish Aquat Sci 21:1183–1226Google Scholar
  9. 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 3:254–258CrossRefGoogle Scholar
  10. 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 216:2771–2782CrossRefPubMedGoogle Scholar
  11. Daufresne M, Lengfellner K, Sommer U (2009) Global warming benefits the small in aquatic ecosystems. Proc Natl Acad Sci U S A 106:12788–12793CrossRefPubMedPubMedCentralGoogle Scholar
  12. 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 313:59–79CrossRefPubMedGoogle Scholar
  13. Domenici P, Blake R (1997) The kinematics and performance of fish fast-start swimming. J Exp Biol 200:1165–1178PubMedGoogle Scholar
  14. Domenici P, Lefrancois C, Shingles A (2007) Hypoxia and the antipredator behaviours of fishes. Philos Trans R Soc Lond B Biol Sci 362:2105–2121CrossRefPubMedPubMedCentralGoogle Scholar
  15. Donelson JM (2015) Development in a warm future ocean may enhance performance in some species. J Exp Mar Bio Ecol 472:119–125CrossRefGoogle Scholar
  16. Donelson JM, Munday PL (2012) Thermal sensitivity does not determine acclimation capacity for a tropical reef fish. J Anim Ecol 81:1126–1131CrossRefPubMedGoogle Scholar
  17. Donelson JM, Munday PL (2015) Transgenerational plasticity mitigates the impact of global warming to offspring sex ratios. Glob Chang Biol 21:2954–2962CrossRefPubMedGoogle Scholar
  18. Donelson JM, Munday PL, McCormick MI, Pitcher CR (2012) Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat Clim Chang 2:30–32CrossRefGoogle Scholar
  19. 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 17:1712–1719CrossRefGoogle Scholar
  20. 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 401:233–243CrossRefGoogle Scholar
  21. Drucker EG (1996) The use of gait transition speed in comparative studies of fish locomotion. Am Zool 36:555–566CrossRefGoogle Scholar
  22. Fuiman LA, Meekan MG, McCormick MI (2010) Maladaptive behavior reinforces a recruitment bottleneck in newly settled fishes. Oecologia 164:99–108CrossRefPubMedGoogle Scholar
  23. Fulton CJ, Bellwood DR (2002) Patterns of foraging in labrid fishes. Mar Ecol Prog Ser 226:135–142CrossRefGoogle Scholar
  24. Gardiner NM, Munday PL, Nilsson GE (2010) Counter-gradient variation in respiratory performance of coral reef fishes at elevated temperatures. PLoS One 5:e13299CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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 217:711–717CrossRefPubMedGoogle Scholar
  26. Grenchik MK, Donelson JM, Munday PL (2013) Evidence for developmental thermal acclimation in the damselfish, Pomacentrus moluccensis. Coral Reefs 32:85–90CrossRefGoogle Scholar
  27. Hanel R, Wieser W (1996) Growth of swimming muscles and its metabolic cost in larvae of whitefish at different temperatures. J Fish Biol 48:937–951CrossRefGoogle Scholar
  28. Hoey AS, McCormick MI (2004) Selective predation for low body condition at the larval–juvenile transition of a coral reef fish. Oecologia 139:23–29CrossRefPubMedGoogle Scholar
  29. Hubble M (2003) The ecological significance of body size in tropical wrasses (Pisces: Labridae). Ph.D. thesis, James Cook University, TownsvilleGoogle Scholar
  30. Huey RB, Kingsolver JG (1989) Evolution of thermal sensitivity of ectotherm performance. Trends Ecol Evol 4:131–135CrossRefPubMedGoogle Scholar
  31. 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, SwitzerlandGoogle Scholar
  32. Jackson JBC (2008) Ecological extinction and evolution in the brave new ocean. Proc Natl Acad Sci U S A 105:11458–11465CrossRefPubMedPubMedCentralGoogle Scholar
  33. Janzen DH (1967) Why mountain passes are higher in the tropics. Am Nat 101:233–249CrossRefGoogle Scholar
  34. Johansen JL, Jones GP (2011) Increasing ocean temperature reduces the metabolic performance and swimming ability of coral reef damselfishes. Glob Chang Biol 17:2971–2979CrossRefGoogle Scholar
  35. Johansen JL, Steffensen JF, Jones GP (2015) Winter temperatures decrease swimming performance and limit distributions of tropical damselfishes. Conserv Physiol 3:cov039CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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 20:1067–1074CrossRefPubMedGoogle Scholar
  37. 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 198:2165–2175PubMedGoogle Scholar
  38. 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 18:109–114CrossRefGoogle Scholar
  39. 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:e10616CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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 527–539Google Scholar
  41. Munday PL, Kingsford MJ, O’Callaghan M, Donelson JM (2008a) Elevated temperature restricts growth potential of the coral reef fish Acanthochromis polyacanthus. Coral Reefs 27:927–931CrossRefGoogle Scholar
  42. Munday PL, Jones GP, Pratchett MS, Williams AJ (2008b) Climate change and the future for coral reef fishes. Fish Fish 9:261–285CrossRefGoogle Scholar
  43. 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 28:623–634CrossRefGoogle Scholar
  44. 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–S33CrossRefGoogle Scholar
  45. 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 156:389–393CrossRefPubMedGoogle Scholar
  46. 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 274:79–85CrossRefGoogle Scholar
  47. 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 19:2373–2380CrossRefPubMedPubMedCentralGoogle Scholar
  48. 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 3:919–925CrossRefGoogle Scholar
  49. Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97CrossRefPubMedGoogle Scholar
  50. Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322:690–692CrossRefPubMedGoogle Scholar
  51. 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 79:295–313CrossRefPubMedGoogle Scholar
  52. Randall JE, Allen GR, Steene RC (1997) Fishes of the Great Barrier Reef and Coral Sea. University of Hawaii Press, HonoluluGoogle Scholar
  53. 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 88:65–80CrossRefPubMedGoogle Scholar
  54. 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 20:1055–1066CrossRefPubMedGoogle Scholar
  55. Schaefer J, Ryan A (2006) Developmental plasticity in the thermal tolerance of zebrafish Danio rerio. J Fish Biol 69:722–734CrossRefGoogle Scholar
  56. Scott GR, Johnston IA (2012) Temperature during embryonic development has persistent effects on thermal acclimation capacity in zebrafish. Proc Natl Acad Sci USA 109:14247–14252CrossRefPubMedPubMedCentralGoogle Scholar
  57. Seebacher F, Ward A, Wilson R (2013) Increased aggression during pregnancy comes at a higher metabolic cost. J Exp Biol 216:771–776CrossRefPubMedGoogle Scholar
  58. 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 26:1418–1428CrossRefGoogle Scholar
  59. Sheridan JA, Bickford D (2011) Shrinking body size as an ecological response to climate change. Nat Clim Chang 1:401–406CrossRefGoogle Scholar
  60. Steffensen JF (1989) Some errors in respirometry of aquatic breathers: how to avoid and correct for them. Fish Physiol Biochem 6:49–59CrossRefPubMedGoogle Scholar
  61. 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 73:200–208CrossRefPubMedGoogle Scholar
  62. 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 175:275–286CrossRefGoogle Scholar
  63. Sunday JM, Bates AE, Dulvy NK (2011) Global analysis of thermal tolerance and latitude in ectotherms. Proc R Soc Lond B Biol Sci 278:1823–1830CrossRefGoogle Scholar
  64. Svendsen M, Bushnell P, Steffensen J (2015) Design and setup of intermittent-flow respirometry system for aquatic organisms. J Fish Biol 88:26–50CrossRefPubMedGoogle Scholar
  65. Szabo TM, Brookings T, Preuss T, Faber DS (2008) Effects of temperature acclimation on a central neural circuit and its behavioral output. J Neurophysiol 100:2997–3008CrossRefPubMedPubMedCentralGoogle Scholar
  66. Temple GK, Johnston I (1998) Testing hypotheses concerning the phenotypic plasticity of escape performance in fish of the family Cottidae. J Exp Biol 201:317–331PubMedGoogle Scholar
  67. Tewksbury JJ, Huey RB, Deutsch CA (2008) Putting the heat on tropical animals. Science 320:1296–1297CrossRefPubMedGoogle Scholar
  68. Vigliola L, Meekan MG (2002) Size at hatching and planktonic growth determine post-settlement survivorship of a coral reef fish. Oecologia 131:89–93CrossRefGoogle Scholar
  69. 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 15:469–480CrossRefGoogle Scholar
  70. 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 416:389–395CrossRefPubMedGoogle Scholar
  71. 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 3381–3467Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.College of Marine and Environmental ScienceJames Cook UniversityTownsvilleAustralia
  2. 2.ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  3. 3.School of Life SciencesUniversity of Technology SydneySydneyAustralia

Personalised recommendations