Advertisement

Marine Biology

, Volume 162, Issue 12, pp 2379–2389 | Cite as

Interannual variation in the larval development of a coral reef fish in response to temperature and associated environmental factors

  • Ian M. McLeod
  • Rhondda E. Jones
  • Geoffrey P. Jones
  • Miwa Takahashi
  • Mark I. McCormick
Original Paper

Abstract

Climate change is predicted to increase ocean temperatures and influence weather patterns. Here, we examine the influence of temperature and other environmental variables on key early life traits of the coral reef damselfish, Pomacentrus moluccensis, based on ten cohorts of newly settled fish collected over 13 years from around Lizard Island (Great Barrier Reef, Australia). Pelagic larval duration (PLD), larval growth and size at settlement were estimated through otolith microstructure analysis. Multiple regression techniques were used to measure the strength of the associations between these traits and developmental temperature, rain, wind speed and solar radiation. Temperature accounted for 18.4, 26.7 and 25.0 % of the variability in PLD, growth rates and settlement size, respectively. PLDs generally declined and growth rates generally increased with increasing temperatures to ~28 °C, above which PLDs tended to increase and growth rates tended to decrease. Size at settlement did not differ between ~25 and ~28 °C, but tended to decrease with increasing temperature above ~28 °C. Together rain, wind speed and solar radiation explained 6.3, 26.3 and 33.7 % of the remaining variability in PLD, growth rates and size at settlement, respectively. Higher wind speeds were generally associated with longer PLDs. Increasing wind, high rainfall and increasing solar radiation were associated with slower growth rates and smaller sizes at settlement. Overall, results suggest that ~28 °C is likely to be a thermal optimum for larval development for this species and other environmental factors associated with climate change including rainfall, wind speed and solar radiation should be considered in predictions of effects on larval fish.

Keywords

Wind Speed Solar Radiation Larval Development Great Barrier Reef Larval Fish 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Oona Lönnstedt, Shaun Smith and Tom Jones for collecting fish, Timothy Clark, Philip Munday, Agnès Le Port and Jodie Rummer for helpful discussions that contributed to this manuscript and Maya Srinivasan for providing the Pomacentrus moluccensis image used in Fig. 1. We also thank Lyle Vail and Anne Hogget from Lizard Island Research Station for providing logistical support and information about historical environmental conditions and the editor and two anonymous reviews who improved the manuscript. The Australian Research Council, AIMS@JCU and James Cook University supplied funding for this research.

References

  1. Anderson JT (1988) A review of size dependent survival during pre-recruit stages of fishes in relation to recruitment. J Northwest Atl Fish Sci 8:55–66CrossRefGoogle Scholar
  2. Bergenius MAJ, McCormick MI, Meekan MG, Robertson DR (2005) Environmental influences on larval duration, growth and magnitude of settlement of a coral reef fish. Mar Biol 147:291–300CrossRefGoogle Scholar
  3. Bindoff NL (2007) Observations: Oceanic climate change and sea level. In: Climate change 2007: the physical science basis, pp 385–432Google Scholar
  4. Booth DJ, Kingsford MJ, Doherty PJ, Beretta GA (2000) Recruitment of damselfishes in one tree island lagoon: persistent interannual spatial patterns. Mar Ecol Prog Ser 202:219–230CrossRefGoogle Scholar
  5. Brunton BJ, Booth DJ (2003) Density- and size-dependent mortality of a settling coral-reef damselfish (Pomacentrus moluccensis, Bleeker). Oecologia 137:377–384CrossRefGoogle Scholar
  6. Cheal AJ, Wilson SK, Emslie MJ, Dolman AM, Sweatman H (2008) Responses of reef fish communities to coral declines on the Great Barrier Reef. Mar Ecol Prog Ser 372:211–223CrossRefGoogle Scholar
  7. Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Ann Rev Mar Sci 1:443–466CrossRefGoogle Scholar
  8. Cushing D (1995) Population production and regulation in the sea: a fisheries perspective. Cambridge University Press, CambridgeGoogle Scholar
  9. D’Alessandro EK, Sponaugle S, Cowen RK (2013) Selective mortality during the larval and juvenile stages of snappers (Lutjanidae) and great barracuda Sphyraena barracuda. Mar Ecol Prog Ser 474:227–242CrossRefGoogle Scholar
  10. D’Croz L, Robertson DR, Martínez JA (1999) Cross-shelf distribution of nutrients, plankton, and fish larvae in the San Blas Archipelago, Caribbean Panamá. Rev Biol Trop 47:203–215Google Scholar
  11. De’ath G, Fabricius KE, Sweatman H, Puotinen M (2012) The 27-year decline of coral cover on the Great Barrier Reef and its causes. Proc Natl Acad Sci USA 109:17995–17999CrossRefGoogle Scholar
  12. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Ann Rev Mar Sci 1:169–192CrossRefGoogle Scholar
  13. Dower JF, Miller TJ, Leggett WC (1997) The role of microscale turbulence in the feeding ecology of larval fish. Adv Mar Biol 31:211–220Google Scholar
  14. Fisher R (2005) Swimming speeds of larval coral reef fishes: impacts on self-recruitment and dispersal. Mar Ecol Prog Ser 285:223–232CrossRefGoogle Scholar
  15. Fortier L, Harris RP (1989) Optimal foraging and density-dependent competition in marine fish larvae. Mar Ecol Prog Ser 51:19–33CrossRefGoogle Scholar
  16. Fowler AJ (1990) Validation of annual growth increments in the otoliths of a small, tropical coral reef fish. Mar Ecol Prog Ser 64:25–38CrossRefGoogle Scholar
  17. Fraser MR, McCormick MI (2014) Gender-specific benefits of eating eggs at resident reef fish spawning aggregation sites. Mar Ecol Prog Ser 517:209–216CrossRefGoogle Scholar
  18. Gagliano M, McCormick MI (2009) Hormonally mediated maternal effects shape offspring survival potential in stressful environments. Oecologia 160:657–665CrossRefGoogle Scholar
  19. Gagliano M, McCormick MI, Meekan MG (2007a) Survival against the odds: ontogenetic changes in selective pressure mediate growth-mortality tradeoffs. Proc R Soc Lond B 274:1575–1582CrossRefGoogle Scholar
  20. Gagliano M, McCormick MI, Meekan MG (2007b) Temperature-induced shifts in selective pressure at a critical developmental transition. Oecologia 152:219–225CrossRefGoogle Scholar
  21. Gallego A, Heath MR, McKenzie E, Cargill LH (1996) Environmentally induced short-term variability in the growth rates of larval herring. Mar Ecol Prog Ser 137:11–23CrossRefGoogle Scholar
  22. Green BS, Fisher R (2004) Temperature influences swimming speed, growth and larval duration in coral reef fish larvae. J Exp Mar Biol Ecol 299:115–132CrossRefGoogle Scholar
  23. Green BS, McCormick MI (2005) Maternal and paternal influences determine size, growth and performance in a tropical reef fish larvae. Mar Ecol Prog Ser 289:263–272CrossRefGoogle Scholar
  24. Häder DP, Helbling EW, Williamson CE, Worrest RC (2011) Effects of UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol Sci 10:242–260CrossRefGoogle Scholar
  25. Heath MR (1992) Field investigations of the early life stages of marine fish. Adv Mar Biol 28:1–174CrossRefGoogle Scholar
  26. Houde ED (1989) Comparative growth, mortality, and energetics of marine fish larvae: temperature and implied latitudinal effects. Fish Bull 87:471–495Google Scholar
  27. IPCC (2013) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. In: Stocker TF, Qin D, K. PG, Tingor M, Allan SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) The physical science basis contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change, Cainbridge University Press, Cambridge, UKGoogle Scholar
  28. Kendall MS, Poti M, Wynne TT, Kinlan BP, Bauer LB (2013) Consequences of the life history traits of pelagic larvae on interisland connectivity during a changing climate. Mar Ecol Prog Ser 489:43–59CrossRefGoogle Scholar
  29. Kouwenberg JHM, Browman HI, St-Pierre JF, Runge JA, Cullen JJ, Davis RF (1999) Biological weighting of ultraviolet (280–400 nm) induced mortality in marine zooplankton and fish. I. Atlantic cod (Gadus morhua) eggs. Mar Biol 134:269–284CrossRefGoogle Scholar
  30. Laurel BJ, Bradbury IR (2006) “Big” concerns with high latitude marine protected areas (MPAs): trends in connectivity and MPA size. Can J Fish Aquat Sci 63:2603–2607CrossRefGoogle Scholar
  31. Leis JM (1991) The pelagic stage of reef fishes: the larval biology of coral reef fishes. In: Sale PF (ed) The ecology of fishes on coral reefs. Academic Press, San Deigo, pp 183–230CrossRefGoogle Scholar
  32. Lemberget T, McCormick MI (2009) Replenishment success linked to fluctuating asymmetry in larval fish. Oecologia 159:83–93CrossRefGoogle Scholar
  33. Lemberget T, McCormick MI, Wilson DT (2009) Environmental influences on the replenishment of lizardfish (family Synodontidae) in Caribbean Panama. Coral Reefs 28:737–750CrossRefGoogle Scholar
  34. Lough JM, Hobday AJ (2011) Observed climate change in Australian marine and freshwater environments. Mar Freshw Res 62:984–999CrossRefGoogle Scholar
  35. MacKenzie BR, Kiorboe T (1995) Encounter rates and swimming behavior of pause-travel and cruise larval fish predators in calm and turbulent laboratory environments. Limnol Oceanogr 40:1278–1289CrossRefGoogle Scholar
  36. Maddams JC, McCormick MI (2012) Not all offspring are created equal: variation in larval characteristics in a serially spawning damselfish. PLoS One. doi: 10.1371/journal.pone.0048525 CrossRefGoogle Scholar
  37. McCormick MI (1998) Behaviorally induced maternal stress in a fish influences progeny quality by a hormonal mechanism. Ecology 79:1873–1883CrossRefGoogle Scholar
  38. McCormick MI (2003) Consumption of coral propagules after mass spawning enhances larval quality of damselfish through maternal effects. Oecologia 136:37–45CrossRefGoogle Scholar
  39. McCormick MI (2006) Mothers matter: crowded reefs lead to stressed mothers and smaller offspring in marine fish. Ecology 87:1104–1109CrossRefGoogle Scholar
  40. McCormick MI, Hoey AS (2004) Larval growth history determines juvenile growth and survival in a tropical marine fish. Oikos 106:225–242CrossRefGoogle Scholar
  41. McCormick MI, Molony BW (1995) Influence of water temperature during the larval stage on size, age and body condition of a tropical reef fish at settlement. Mar Ecol Prog Ser 118:59–68CrossRefGoogle Scholar
  42. McCormick MI, Nechaev IV (2002) Influence of cortisol on developmental rhythms during embryogenesis in a tropical damselfish. J Exp Zool 293:456–466CrossRefGoogle Scholar
  43. McCormick MI, Makey L, Dufour V (2002) Comparative study of metamorphosis in tropical reef fishes. Mar Biol 141:841–853CrossRefGoogle Scholar
  44. McLeod IM, Rummer JL, Clark TD, Jones GP, McCormick MI, Wenger AS, Munday PL (2013) Climate change and the performance of larval coral reef fishes: the inter- action between temperature and food availability. Conserv Physiol 1:cot024CrossRefGoogle Scholar
  45. McLeod IM, McCormick MI, Munday PL, Clark TD, Wenger AS, Brooker RM, Takahashi M, Jones GP (2015) Latitudinal variation in larval development of coral reef fishes: implications of a warming ocean. Mar Ecol Prog Ser 521:129–141CrossRefGoogle Scholar
  46. Meehl GA (2007) Global climate projections. In: Climate change 2007: the physical science basis, pp 747–845Google Scholar
  47. Meekan MG, Wilson SG, Halford A, Retzel A (2001) A comparison of catches of fishes and invertebrates by two light trap designs, in tropical NW Australia. Mar Biol 139:373–381CrossRefGoogle Scholar
  48. Meekan MG, Carleton JH, McKinnon AD, Flynn K, Furnas M (2003) What determines the growth of tropical reef fish larvae in the plankton: food or temperature? Mar Ecol Prog Ser 256:193–204CrossRefGoogle Scholar
  49. Milicich MJ, Meekan MG, Doherty PJ (1992) Larval supply: a good predictor of recruitment of three species of reef fish (Pomacentridae). Mar Ecol Prog Ser 86:153–166CrossRefGoogle Scholar
  50. Munday PL (2014) Transgenerational acclimation of fishes to climate change and acid acidification. F1000 Prime Rep 6:99CrossRefGoogle Scholar
  51. Munday PL, Jones GP, Pratchett MS, Williams AJ (2008) Climate change and the future for coral reef fishes. Fish Fish 9:261–285CrossRefGoogle Scholar
  52. Munday PL, Leis JM, Lough JM, Paris CB, Kingsford M, Berumen ML, Lambrechts J (2009) Climate change and coral reef connectivity. Coral Reefs 28:379–393CrossRefGoogle Scholar
  53. Munday PL, Warner RR, Monro K, Pandolfi JM, Marshall DJ (2013) Predicting evolutionary responses to climate change in the sea. Ecol Lett 16:1488–1500CrossRefGoogle Scholar
  54. O’Connor MI, Bruno JF, Gaines SD, Halpern BS, Lester SE, Kinlan BP, Weiss JM (2007) Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation. Proc Natl Acad Sci USA 104:1266–1271CrossRefGoogle Scholar
  55. Pankhurst NW, Munday PL (2011) Effects of climate change on fish reproduction and early life history stages. Mar Freshw Res 62:1015–1026CrossRefGoogle Scholar
  56. Peck MA, Huebert KB, Llopiz JK (2012) Intrinsic and extrinsic factors driving match-mismatch dynamics during the early life history of marine fishes advances in ecological research. Elsvier, San Diego, pp 177–302Google Scholar
  57. Politis SN, Dahlke FT, Butts IAE, Peck M, Trippel EA (2014) Temperature, paternity and asynchronous hatching influence early developmental characteristics of larval Atlantic cod, Gadus morhua. J Exp Mar Biol Ecol 459:70–79CrossRefGoogle Scholar
  58. Poloczanska ES, Babcock RC, Butler A, Hobday AJ, Hoegh-Guldberg O, Kunz TJ, Matear R, Milton DA, Okey TA, Richardson AJ (2007) Climate change and Australian marine life. Oceanogr Mar Biol 45:407–478Google Scholar
  59. Pörtner HO, Peck MA (2011) Effects of climate change. In: Farrell AP (ed) Encyclopedia of fish physiology. Academic Press, San Diego, pp 1738–1745CrossRefGoogle Scholar
  60. Pratchett MS, Munday PL, Wilson SK, Graham NAJ, Cinner JE, Bellwood DR, Jones GP, Polunin NVC, McClanahan TR (2008) Effects of climate-induced coral bleaching on coral-reef fishes-ecological and economic consequences. Oceanogr Mar Biol 46:251–296Google Scholar
  61. R Development Core Team (2013) R: a language and environment for statistical computing. Foundation for Statistical Computing, ViennaGoogle Scholar
  62. Radtke RL, Kinzie Iii RA, Shafer DJ (2001) Temporal and spatial variation in length of larval life and size at settlement of the Hawaiian amphidromous goby Lentipes concolor. J Fish Biol 59:928–938Google Scholar
  63. Randall JE, Allen GR, Steene RC (1990) fishes of the great barrier reef and coral sea. University of Hawaii Press, HonoluluGoogle Scholar
  64. Sogard SM (1997) Size-selective mortality in the juvenile stage of teleost fishes: a review. Bull Mar Sci 60:1129–1157Google Scholar
  65. Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (2007) Summary for policymakers. In: Climate change 2007: the physical science basis contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change, pp 1–18Google Scholar
  66. Sponaugle S, Cowen RK (1996) Larval supply and patterns of recruitment for two caribbean reef fishes, Stegastes partitus and Acanthurus bahianus. Mar Freshw Res 47:433–447CrossRefGoogle Scholar
  67. Sponaugle S, Grorud-Colvert K (2006) Environmental variability, early life-history traits, and survival of new coral reef fish recruits. Integr Comp Biol 46:623–633CrossRefGoogle Scholar
  68. Takahashi M, McCormick MI, Munday PL, Jones GP (2012) Influence of seasonal and latitudinal temperature variation on early life-history traits of a coral reef fish. Mar Freshw Res 63:856–864. doi: 10.1071/MF11278 CrossRefGoogle Scholar
  69. Thorrold SR, Hare JA (2002) Otolith applications in reef fish ecology. In: Sale PF (ed) Advances in the ecology of fishes on coral reefs. Academic Press, San DeigoGoogle Scholar
  70. Utne-Palm AC (2004) Effects of larvae ontogeny, turbidity, and turbulence on prey attack rate and swimming activity of Atlantic herring larvae. J Exp Mar Biol Ecol 310:147–161CrossRefGoogle Scholar
  71. Wilson DT, McCormick MI (1997) Spatial and temporal validation of settlement-marks in the otoliths of tropical reef fishes. Mar Ecol Prog Ser 153:259–271CrossRefGoogle Scholar
  72. Wilson DT, McCormick MI (1999) Microstructure of settlement-marks in the otoliths of tropical reef fishes. Mar Biol 134:29–41CrossRefGoogle Scholar
  73. Wilson DT, Meekan MG (2002) Growth-related advantages for survival to the point of replenishment in the coral reef fish Stegastes partitus (Pomacentridae). Mar Ecol Prog Ser 231:247–260CrossRefGoogle Scholar
  74. Zagarese HE, Williamson CE (2001) The implications of solar UV radiation exposure for fish and fisheries. Fish Fish 2:250–260CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Ian M. McLeod
    • 1
    • 2
    • 3
    • 4
  • Rhondda E. Jones
    • 1
  • Geoffrey P. Jones
    • 1
    • 2
  • Miwa Takahashi
    • 1
    • 5
  • Mark I. McCormick
    • 1
    • 2
  1. 1.College of Marine and Environmental SciencesJames Cook UniversityTownsvilleAustralia
  2. 2.ARC Centre for Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  3. 3.AIMS@JCU, Australian Institute of Marine ScienceTownsvilleAustralia
  4. 4.Centre for Tropical Water and Aquatic Ecosystem Research (TropWATER)James Cook UniversityTownsvilleAustralia
  5. 5.Australian Institute of Marine ScienceTownsvilleAustralia

Personalised recommendations