Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE (Open Access)

Effects of climate change on fish reproduction and early life history stages

Ned W. Pankhurst A C and Philip L. Munday B
+ Author Affiliations
- Author Affiliations

A Australian Rivers Institute, Griffith University, Gold Coast, Qld 4222, Australia.

B ARC Centre of Excellence for Coral Reef Studies, and School of Marine and Tropical Biology, James Cook University, Townsville, Qld 4811, Australia.

C Corresponding author. Email: n.pankhurst@griffith.edu.au

Marine and Freshwater Research 62(9) 1015-1026 https://doi.org/10.1071/MF10269
Submitted: 29 October 2010  Accepted: 1 March 2011   Published: 21 September 2011

Abstract

Seasonal change in temperature has a profound effect on reproduction in fish. Increasing temperatures cue reproductive development in spring-spawning species, and falling temperatures stimulate reproduction in autumn-spawners. Elevated temperatures truncate spring spawning, and delay autumn spawning. Temperature increases will affect reproduction, but the nature of these effects will depend on the period and amplitude of the increase and range from phase-shifting of spawning to complete inhibition of reproduction. This latter effect will be most marked in species that are constrained in their capacity to shift geographic range. Studies from a range of taxa, habitats and temperature ranges all show inhibitory effects of elevated temperature albeit about different environmental set points. The effects are generated through the endocrine system, particularly through the inhibition of ovarian oestrogen production. Larval fishes are usually more sensitive than adults to environmental fluctuations, and might be especially vulnerable to climate change. In addition to direct effects on embryonic duration and egg survival, temperature also influences size at hatching, developmental rate, pelagic larval duration and survival. A companion effect of marine climate change is ocean acidification, which may pose a significant threat through its capacity to alter larval behaviour and impair sensory capabilities. This in turn impacts on population replenishment and connectivity patterns of marine fishes.

Additional keywords: acidification, estrogens, larval behaviour, spawning, temperature.


References

Akazome, Y., Kanda, S., Okubo, K., and Oka, Y. (2010). Functional and evolutionary insights into vertebrate kisspeptin systems from studies of fish brain. Journal of Fish Biology 76, 161–182.
Functional and evolutionary insights into vertebrate kisspeptin systems from studies of fish brain.CrossRef | 1:CAS:528:DC%2BC3cXkt1agsb8%3D&md5=ef98653f76647550df958a4f0993a2b7CAS |

Angilletta, M. J. (2009). ‘Thermal Adaptation: A Theoretical and Empirical Synthesis.’ (Oxford University Press: New York.)

Babin, P. J., Carnevali, O., Lubzens, E., and Schneider, W. J. (2007). Molecular aspects of oocyte vitellogenesis in fish. In ‘The Fish Oocyte: From Basic Studies to Biotechnical Applications.’ (Eds P. J. Babin, J. Cerdá and E. Lubzens.) pp. 39–76. (Springer: Dordrecht.)

Barton, B. A. (1996). General biology of salmonids. In ‘Principles of Salmonid Aquaculture.’ (Eds W. Pennell and B. A. Barton.) pp. 29–95. (Elsevier: Amsterdam.)

Benoît, H. P., Pepin, P., and Brown, J. A. (2000). Patterns of metamorphic age and length in marine fishes, from individuals to taxa. Canadian Journal of Fisheries and Aquatic Sciences 57, 856–869.
Patterns of metamorphic age and length in marine fishes, from individuals to taxa.CrossRef |

Bergenius, M. A. J., Meekan, M. G., Robertson, D. R., and McCormick, M. I. (2002). Larval growth predicts the recruitment success of a coral reef fish. Oecologia 131, 521–525.
Larval growth predicts the recruitment success of a coral reef fish.CrossRef |

Blaxter, J. H. S. (1991). The effects of temperature on larval fishes. Netherlands Journal of Zoology 42, 336–357.
The effects of temperature on larval fishes.CrossRef |

Brauner, C. J. (2009). Acid–base balance. In ‘Fish Larval Physiology’. (Eds R. N. Finn and B. G. Kapoor.) pp. 185–198. (Science Publishers: Enfield.)

Cheal, A. J., Delean, S., Sweatman, H., and Thompson, A. A. (2007). Spatial synchrony in coral reef fish populations and the influence of climate. Ecology 88, 158–169.
Spatial synchrony in coral reef fish populations and the influence of climate.CrossRef | 1:STN:280:DC%2BD2s3ot1Khug%3D%3D&md5=40a3de0c2cf25573c55ad52f8e779decCAS |

Claiborne, J. B., Edwards, S. L., and Morrison-Shetlar, A. I. (2002). Acid–base regulation in fishes: cellular and molecular mechanisms. The Journal of Experimental Zoology 293, 302–319.
Acid–base regulation in fishes: cellular and molecular mechanisms.CrossRef | 1:CAS:528:DC%2BD38XlvVKktr0%3D&md5=ad26d46df5d54a0862d7bdc3e5e341d7CAS |

Crawshaw, L. I., and O’Connor, C. S. (1997). Behavioural compensation for long-term thermal change. In ‘Global Warming: Implications for Freshwater and Marine Fish’. (Eds C. M. Wood and D. G. McDonald.) pp. 351–376. (Cambridge University Press: Cambridge.)

Devlin, R. H., and Nagahama, Y. (2002). Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208, 191–364.
Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences.CrossRef | 1:CAS:528:DC%2BD38XktFKjsbY%3D&md5=01b7fecd33f7675f212072da2280172cCAS |

Dixson, D. L., Munday, P. L., and Jones, G. P. (2010). Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecology Letters 13, 68–75.
Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues.CrossRef |

Donelson, J. M., Munday, P. L., McCormick, M. I., Pankhurst, N. W., and Pankhurst, P. M. (2010). Effects of elevated water temperature and food availability on the reproductive performance of a coral reef fish. Marine Ecology Progress Series 401, 233–243.
Effects of elevated water temperature and food availability on the reproductive performance of a coral reef fish.CrossRef |

Donelson, J. M., Munday, P. L., McCormick, M. I., and Nilsson, G. E. (2011). Acclimation to predicted ocean warming through developmental plasticity in a tropical reef fish. Global Change Biology 17, 1712–1719.
Acclimation to predicted ocean warming through developmental plasticity in a tropical reef fish.CrossRef |

Dufour, S., Sebert, M.-E., Weltzein, F.-A., Rousseau, K., and Pasqualini, C. (2010). Neuroendocrine control by dopamine of teleost reproduction. Journal of Fish Biology 76, 129–160.
Neuroendocrine control by dopamine of teleost reproduction.CrossRef | 1:CAS:528:DC%2BC3cXkt1agsb4%3D&md5=bea3c1be994c2a5e255e623e5bf98b7fCAS |

Fabry, V. J., Seibel, B. A., Feely, R. A., and Orr, J. C. (2008). Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Science 65, 414–432.
Impacts of ocean acidification on marine fauna and ecosystem processes.CrossRef | 1:CAS:528:DC%2BD1cXntFegtL4%3D&md5=25f0681d20c358a38b757d741fc1cf94CAS |

Farrell, A. P., Hinch, S. G., Cooke, S. J., Patterson, D. A., Crossin, G. T., et al. (2008). Pacific salmon in hot water: applying aerobic scope models and biotelemetry to predict the success of spawning migrations. Physiological and Biochemical Zoology 81, 697–709.
Pacific salmon in hot water: applying aerobic scope models and biotelemetry to predict the success of spawning migrations.CrossRef | 1:STN:280:DC%2BD1cjhtlWitQ%3D%3D&md5=4997e7a8bf95e78c6c51729853573e09CAS |

Frisch, A. (2004). Sex-change and gonadal steroids in sequentially-hermaphroditic teleost fish. Reviews in Fish Biology and Fisheries 14, 481–499.
Sex-change and gonadal steroids in sequentially-hermaphroditic teleost fish.CrossRef |

Frommel, A. Y., Stiebens, V., Clemmesen, C., and Havenhand, J. (2010). Effect of ocean acidification on marine fish sperm (Baltic cod: Gadus morhua). Biogeosciences Discussion 7, 5859–5872.
Effect of ocean acidification on marine fish sperm (Baltic cod: Gadus morhua).CrossRef |

Fu, C., Wilson, J. M., Rombough, P. J., and Brauner, C. J. (2010). Ions first: Na+ uptake shifts from the skin to the gills before O2 uptake in developing rainbow trout, Oncorhynchus mykiss. Proceedings of the Royal Society Series B, Biological Sciences 277, 1553–1560.
Ions first: Na+ uptake shifts from the skin to the gills before O2 uptake in developing rainbow trout, Oncorhynchus mykiss.CrossRef | 1:CAS:528:DC%2BC3cXhtVehtbnK&md5=8d822fb4930205d8ace322639fab9e8aCAS |

Fuiman, L. A., Poling, K. R., and Higgs, D. M. (1998). Quantifying developmental progress from comparative studies of larval fishes. Copeia 1998, 602–611.
Quantifying developmental progress from comparative studies of larval fishes.CrossRef |

Gagliano, M., McCormick, M. I., and Meekan, M. G. (2007). Temperature-induced shifts in selective pressure at a critical developmental transition. Oecologia 152, 219–225.
Temperature-induced shifts in selective pressure at a critical developmental transition.CrossRef |

Gardiner, N. M., Munday, P. L., and Nilsson, G. E. (2010). Counter-gradient variation in respiratory performance of coral reef fishes at elevated temperatures. PLoS ONE 5, e13299.
Counter-gradient variation in respiratory performance of coral reef fishes at elevated temperatures.CrossRef |

Gillet, C. (1991). Egg production in an Arctic charr (Salvelinus alpinus L.) brood stock: effects of temperature on the timing of spawning and the quality of eggs. Aquatic Living Resources 4, 109–116.
Egg production in an Arctic charr (Salvelinus alpinus L.) brood stock: effects of temperature on the timing of spawning and the quality of eggs.CrossRef |

Gillet, C., and Breton, B. (2009). LH secretion and ovulation following exposure of Arctic charr to different temperature and photoperiod regimes: Responsiveness of females to a gonadotropin-releasing hormone analogue and a dopamine antagonist. General and Comparative Endocrinology 162, 210–218.
LH secretion and ovulation following exposure of Arctic charr to different temperature and photoperiod regimes: Responsiveness of females to a gonadotropin-releasing hormone analogue and a dopamine antagonist.CrossRef | 1:CAS:528:DC%2BD1MXlslWhu7w%3D&md5=759da0068c7233ef4855bdd99b99f542CAS |

Gillet, C., Breton, B., and Mikolajczyk, T. (1996). Effects of GnRHa and pimozide treatments on the timing of ovulation and egg quality in Arctic charr (Salvelinus alpinus) at 5 and 10°C. Aquatic Living Resources 9, 257–263.
Effects of GnRHa and pimozide treatments on the timing of ovulation and egg quality in Arctic charr (Salvelinus alpinus) at 5 and 10°C.CrossRef |

Graham, C. T., and Harrod, C. (2009). Implications of climate change for the fishes of the British Isles. Journal of Fish Biology 74, 1143–1205.
Implications of climate change for the fishes of the British Isles.CrossRef | 1:STN:280:DC%2BC3cjnt1ygug%3D%3D&md5=c45aed507470998e7e370afdb13d5565CAS |

Green, B. S., and Fisher, R. (2004). Temperature influences swimming speed, growth and larval duration in coral reef fish larvae. Journal of Experimental Marine Biology and Ecology 299, 115–132.
Temperature influences swimming speed, growth and larval duration in coral reef fish larvae.CrossRef |

Guiguen, Y., Fostier, A., Piferrer, F., and Chang, C.-F. (2010). Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. General and Comparative Endocrinology 165, 352–366.
Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish.CrossRef | 1:CAS:528:DC%2BC3cXktVegtQ%3D%3D&md5=f0e2a5989788b735776ba61c3c6dffafCAS |

Haddy, J. A., and Pankhurst, N. W. (1999). Stress-induced changes in concentrations of plasma sex steroids in black bream. Journal of Fish Biology 55, 1304–1316.
Stress-induced changes in concentrations of plasma sex steroids in black bream.CrossRef | 1:CAS:528:DC%2BD3cXht1CmsQ%3D%3D&md5=22424bb4c4bc6952e920d9e571f30832CAS |

Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S., Greenfield, P., et al. (2007). Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742.
Coral reefs under rapid climate change and ocean acidification.CrossRef | 1:CAS:528:DC%2BD2sXhsVWhu7fN&md5=b074c829a513c1a5f7a4dd1596f39ea3CAS |

Houde, E. D. (1989). Comparative growth, mortality, and energetics of marine fish larvae – temperature and implied latitudinal effects. Fishery Bulletin 87, 471–495.

Howell, B. R., Day, O. J., Ellis, T., and Baynes, S. M. (1998). Early life stages of farmed fish. In ‘Biology of Farmed Fish’. (Eds K. D. Black and A. D. Pickering.) pp. 27–66. (Sheffield Academic Press: Sheffield.)

Inaba, K., Dreanno, C., and Cosson, J. (2003). Control of flatfish sperm motility by CO2 and carbonic anhydrase. Cell Motility and the Cytoskeleton 55, 174–187.
Control of flatfish sperm motility by CO2 and carbonic anhydrase.CrossRef | 1:CAS:528:DC%2BD3sXmtFWjtLg%3D&md5=9ce0cce0d6c1f64065abfe2dea09560dCAS |

Ishimatsu, A., Hayashi, M., and Kikkawa, T. (2008). Fishes in high-CO2, acidified oceans. Marine Ecology Progress Series 373, 295–302.
Fishes in high-CO2, acidified oceans.CrossRef | 1:CAS:528:DC%2BD1MXisVCrsLo%3D&md5=4929319c5a0d6651489b1368b768a496CAS |

Janhunen, M., Piironen, J., and Peuhkuri, N. (2010). Parental effects on embryonic viability and growth in Arctic charr Salvelinus alpinus at two incubation temperatures. Journal of Fish Biology 76, 2558–2570.
Parental effects on embryonic viability and growth in Arctic charr Salvelinus alpinus at two incubation temperatures.CrossRef | 1:STN:280:DC%2BC3crhtlaqsw%3D%3D&md5=6c61de340b635518e42fb6f6bc4bce52CAS |

Jobling, M. (1997). Temperature and growth: modulation of growth rate via temperature change. In ‘Global Warming: Implications for Freshwater and Marine Fish’. (Eds C. M. Wood and D. G. McDonald.) pp. 225–253. (Cambridge University Press: Cambridge.)

Jobling, M., Johnsen, H. K., Pettersen, G. W., and Henderson, R. J. (1995). Effect of temperature on reproductive development in Arctic charr, Salvelinus alpinus (L.). Journal of Thermal Biology 20, 157–165.
Effect of temperature on reproductive development in Arctic charr, Salvelinus alpinus (L.).CrossRef |

Jonsson, B., and Jonsson, N. (2009). A review of the likely effects of climate change on anadromous Atlantic salmon Salmo salar and brown trout Salmo trutta with particular reference to water temperature and flow. Journal of Fish Biology 75, 2381–2447.
A review of the likely effects of climate change on anadromous Atlantic salmon Salmo salar and brown trout Salmo trutta with particular reference to water temperature and flow.CrossRef | 1:STN:280:DC%2BC3cjnsVOqug%3D%3D&md5=eb886b896e7dc76914ee588406a3fdf9CAS |

Kikkawa, T., Ishimatsu, A., and Kita, J. (2003). Acute CO2 tolerance during the early developmental stages of four marine teleosts. Environmental Toxicology 18, 375–382.
Acute CO2 tolerance during the early developmental stages of four marine teleosts.CrossRef | 1:CAS:528:DC%2BD3sXpsVCmtrk%3D&md5=30e23985093239d95b1814d2fb5170faCAS |

Kikkawa, T., Kita, J., and Ishimatsu, A. (2004). Comparison of the lethal effect of CO2 and acidification on red sea bream (Pagrus major) during the early developmental stages. Marine Pollution Bulletin 48, 108–110.
Comparison of the lethal effect of CO2 and acidification on red sea bream (Pagrus major) during the early developmental stages.CrossRef | 1:CAS:528:DC%2BD2cXisFKhtQ%3D%3D&md5=6a6fb26dd672421bdf430907ce030cdcCAS |

King, H. R., Pankhurst, N. W., and Watts, M. (2007). Reproductive sensitivity to elevated water temperatures in female Atlantic salmon is heightened at certain stages of vitellogenesis. Journal of Fish Biology 70, 190–205.
Reproductive sensitivity to elevated water temperatures in female Atlantic salmon is heightened at certain stages of vitellogenesis.CrossRef | 1:CAS:528:DC%2BD2sXis1Sjsr8%3D&md5=0d8ebdc8f30c79e1c8e493f6fb3a9ac9CAS |

Lambert, Y., Dutil, J.-D., and Ouellet, P. (2000). Nutritional condition and reproductive success in wild fish populations. In ‘Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish’. (Eds B. Norberg, O. S. Kjesbu, G-L. Taranger, E. Andersson and S. O. Stefansson.) pp. 77–84. (John Grieg A/S: Bergen.)

Leatherland, J. F., Li, M., and Barkataki, S. (2010). Stressors, glucocorticoids and ovarian function in teleosts. Journal of Fish Biology 76, 86–111.
Stressors, glucocorticoids and ovarian function in teleosts.CrossRef | 1:CAS:528:DC%2BC3cXkt1agsLY%3D&md5=31b1499b5214c412597eef87d4ed6f49CAS |

Levavi-Sivan, B., Bogerd, J., Mañanós, E. L., Gómez, A., and Lareyre, J. J. (2010). Perspectives on fish gonadotropins and their receptors. General and Comparative Endocrinology 165, 412–437.
Perspectives on fish gonadotropins and their receptors.CrossRef | 1:CAS:528:DC%2BC3cXktVensg%3D%3D&md5=9099d6245c87141d4429d17b917d1ed2CAS |

Lim, B.-S., Kagawa, H., Gen, K., and Okuzawa, K. (2003). Effects of water temperature on the gonadal development and expression of steroidogenic enzymes in the gonad of juvenile red seabream, Pagrus major. Fish Physiology and Biochemistry 28, 161–162.
Effects of water temperature on the gonadal development and expression of steroidogenic enzymes in the gonad of juvenile red seabream, Pagrus major.CrossRef | 1:CAS:528:DC%2BD2cXks1Wqtro%3D&md5=b04a01b9b85ff4ced5ef6f9d368fa5adCAS |

Lo-Yat, A., Meekan, M. G., Lecchini, D., Martinez, E., Galzin, R., et al. (2011). Extreme climatic events reduce ocean productivity and larval supply in a tropical reef ecosystem. Global Change Biology 17, 1695–1702.
Extreme climatic events reduce ocean productivity and larval supply in a tropical reef ecosystem.CrossRef |

Lough, J. M., and Hobday, A. J. (2011). Observed climate change in Australian marine and freshwater environments. Marine and Freshwater Research 62, 984–999.
Observed climate change in Australian marine and freshwater environments.CrossRef |

McCormick, M. I., and Molony, B. W. (1995). Influence of water temperature during the larval stage on size, age and body condition of a tropical reef fish at settlement. Marine Ecology Progress Series 118, 59–68.
Influence of water temperature during the larval stage on size, age and body condition of a tropical reef fish at settlement.CrossRef |

Meekan, M. G., Ackerman, J. L., and Wellington, G. M. (2001). Demography and age structures of coral reef damselfishes in the tropical eastern Pacific Ocean. Marine Ecology Progress Series 212, 223–232.
Demography and age structures of coral reef damselfishes in the tropical eastern Pacific Ocean.CrossRef |

Meekan, M. G., Carleton, J. H., McKinnon, A. D., Flynn, K., and Furnas, M. (2003). What determines the growth of tropical reef fish larvae in the plankton: food or temperature? Marine Ecology Progress Series 256, 193–204.
What determines the growth of tropical reef fish larvae in the plankton: food or temperature?CrossRef |

Melzner, F., Gutowska, M. A., Langenbuch, M., Dupont, S., Lucassen, M., et al. (2009). Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeosciences 6, 2313–2331.
Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny?CrossRef | 1:CAS:528:DC%2BC3cXltVCqsA%3D%3D&md5=6caa9b72c3c5ff2219c0190e3914df39CAS |

Michael, S. W. (2008). ‘Damselfishes and Anemonefishes: the Complete Illustrated Guide to Their Identification, Behaviours, and Captive Care.’ (TFH: New York.)

Migaud, H., Davie, A., and Taylor, J. F. (2010). Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species. Journal of Fish Biology 76, 27–68.
Current knowledge on the photoneuroendocrine regulation of reproduction in temperate fish species.CrossRef | 1:CAS:528:DC%2BC3cXkt1agsLs%3D&md5=5e46db9c129c7d4d0c712cde225f0de1CAS |

Modig, C., Westerlund, L., and Olsson, P.-E. (2007). Oocyte zona pellucida proteins. In ‘The Fish Oocyte; From Basic Studies to Biotechnical Applications’. (Eds P. J. Babin, J. Cerdá and E. Lubzens.) pp. 113–139. (Springer: Dordrecht.)

Morrongiello, J. R., Beatty, S. J., Bennett, J. C., Crook, D. A., Ikedife, D. N. E. N., Kennard, M. J., Kerezsy, A., Lintermans, M., McNeil, D. G., Pusey, B. J., and Rayner, T. (2011). Climate change and its implications for Australia's freshwater fish. Marine and Freshwater Research 62, 1082–1098.
Climate change and its implications for Australia's freshwater fish.CrossRef |

Munday, P. L., White, J. W., and Warner, R. R. (2006). A social basis for the development of primary males in a sex-changing fish. Proceedings of the Royal Society Series B, Biological Sciences 273, 2845–2851.
A social basis for the development of primary males in a sex-changing fish.CrossRef |

Munday, P. L., Jones, G. P., Pratchett, M. S., and Williams, A. J. (2008a). Climate change and the future for coral reef fishes. Fish and Fisheries 9, 261–285.
Climate change and the future for coral reef fishes.CrossRef |

Munday, P. L., Kingsford, M. J., O’Callaghan, M., and Donelson, J. M. (2008b). Elevated temperature restricts growth potential of the coral reef fish Acanthochromis polyacanthus. Coral Reefs 27, 927–931.
Elevated temperature restricts growth potential of the coral reef fish Acanthochromis polyacanthus.CrossRef |

Munday, P. L., Donelson, J. M., Dixson, D. L., and Endo, G. G. K. (2009a). Effects of ocean acidification on the early life history of a tropical marine fish. Proceedings of the Royal Society Series B, Biological Sciences 276, 3275–3283.
Effects of ocean acidification on the early life history of a tropical marine fish.CrossRef | 1:CAS:528:DC%2BD1MXhtFCgsLrJ&md5=39f3ac5437e108caa78e0f735a3df105CAS |

Munday, P. L., Crawley, N. E., and Nilsson, G. E. (2009b). Interacting effects of elevated temperature and ocean acidification on the aerobic performance of coral reef fishes. Marine Ecology Progress Series 388, 235–242.
Interacting effects of elevated temperature and ocean acidification on the aerobic performance of coral reef fishes.CrossRef | 1:CAS:528:DC%2BD1MXht1SrtrnM&md5=d4ff6d30a9d56ac2d9fc60193d0456efCAS |

Munday, P. L., Leis, J. M., Lough, J. M., Paris, C. B., Kingsford, M. J., et al. (2009c). Climate change and coral reef connectivity. Coral Reefs 28, 379–395.
Climate change and coral reef connectivity.CrossRef |

Munday, P. L., Dixson, D. L., Donelson, J. M., Jones, G. P., Pratchett, M. S., et al. (2009d). Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proceedings of the National Academy of Sciences of the United States of America 106, 1848–1852.
Ocean acidification impairs olfactory discrimination and homing ability of a marine fish.CrossRef | 1:CAS:528:DC%2BD1MXitV2isrg%3D&md5=b393a4ea34b06c3afc4a75c959e7efeeCAS |

Munday, P. L., Dixson, D. L., McCormick, M. I., Meekan, M., Ferrari, M. C. O., et al. (2010). Replenishment of fish populations is threatened by ocean acidification. Proceedings of the National Academy of Sciences of the United States of America 107, 12930–12934.
Replenishment of fish populations is threatened by ocean acidification.CrossRef | 1:CAS:528:DC%2BC3cXpsVagur4%3D&md5=29915a1998e7190bf98e919f51aaec55CAS |

Munday, P. L., Gagliano, M., Donelson, J. M., Dixson, D. L., and Thorrold, S. R. (2011). Ocean acidification does not affect the early life history development of a tropical marine fish. Marine Ecology Progress Series 423, 211–221.
Ocean acidification does not affect the early life history development of a tropical marine fish.CrossRef |

Nilsson, G. E., Crawley, N., Lunde, I. G., and Munday, P. L. (2009). Elevated temperature reduces the respiratory scope of coral reef fishes. Global Change Biology 15, 1405–1412.
Elevated temperature reduces the respiratory scope of coral reef fishes.CrossRef |

O’Connor, M. I., Bruno, J. F., Gaines, S. D., Halpern, B. S., Lester, S. E., et al. (2007). Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation. Proceedings of the National Academy of Sciences of the United States of America 104, 1266–1271.
Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation.CrossRef | 1:CAS:528:DC%2BD2sXht12jtL4%3D&md5=6c1c390793bbdd6527a6927e7658fc2eCAS |

Okuzawa, K., Kumakura, N., Gen, K., Yamaguchi, S., Lim, B.-S., et al. (2003). Effect of high water temperature on brain–pituitary–gonad axis of the red seabream during its spawning season. Fish Physiology and Biochemistry 28, 439–440.
Effect of high water temperature on brain–pituitary–gonad axis of the red seabream during its spawning season.CrossRef | 1:CAS:528:DC%2BD2cXks1ajtrc%3D&md5=3872b6e95f409a7d497e07f406ba82b5CAS |

Pankhurst, N. W. (1998). Reproduction. In ‘Biology of Farmed Fish’. (Eds K. D. Black and A. D. Pickering.) pp. 1–26. (Sheffield Academic Press: Sheffield.)

Pankhurst, N. W. (2008). Gonadal steroids: Functions and patterns of change. In ‘Fish Reproduction’. (Eds M. J. Rocha, A. Arukwe and B. G. Kapoor.) pp. 67–111. (Science Publishers: Enfield, NH, USA.)

Pankhurst, N. W. (2011). The endocrinology of stress in fish: an environmental perspective. General and Comparative Endocrinology 170, 265–275.
The endocrinology of stress in fish: an environmental perspective.CrossRef | 1:CAS:528:DC%2BC3MXht1Kntw%3D%3D&md5=1ca92080125b5483a9399c419ac10d27CAS |

Pankhurst, N. W., and King, H. R. (2010). Temperature and salmonid reproduction: implications for aquaculture. Journal of Fish Biology 76, 69–85.
Temperature and salmonid reproduction: implications for aquaculture.CrossRef | 1:STN:280:DC%2BC3cjnsV2qtQ%3D%3D&md5=d0d625b57b8a103bea2b8bc79dc91636CAS |

Pankhurst, N. W., and Porter, M. J. R. (2003). Cold and dark or warm and light: variations on the theme of environmental control of reproduction. Fish Physiology and Biochemistry 28, 385–389.
Cold and dark or warm and light: variations on the theme of environmental control of reproduction.CrossRef | 1:CAS:528:DC%2BD2cXks1ajsb4%3D&md5=66f0f55fda1023fd073162ad0fc9b422CAS |

Pankhurst, N. W., and Thomas, P. M. (1998). Maintenance at elevated temperature delays the steroidogenic and ovulatory responsiveness of rainbow trout Oncorhynchus mykiss to luteinizing hormone releasing hormone analogue. Aquaculture 166, 163–177.
Maintenance at elevated temperature delays the steroidogenic and ovulatory responsiveness of rainbow trout Oncorhynchus mykiss to luteinizing hormone releasing hormone analogue.CrossRef | 1:CAS:528:DyaK1cXkslyksLc%3D&md5=ee436eeeda946f3ba1847a7928fa3b7eCAS |

Pankhurst, N. W., and Van Der Kraak, G. (1997). Effects of stress on growth and reproduction. In ‘Fish Stress and Health in Aquaculture’. (Eds G. K. Iwama, A. D. Pickering, J. P. Sumpter and C. B. Schreck.) pp. 73–93. (Cambridge University Press: Cambridge.)

Pankhurst, N. W., Van Der Kraak, G., and Peter, R. E. (1995). Evidence that the inhibitory effects of stress on reproduction in teleost fish are not mediated by the action of cortisol on ovarian steroidogenesis. General and Comparative Endocrinology 99, 249–257.
Evidence that the inhibitory effects of stress on reproduction in teleost fish are not mediated by the action of cortisol on ovarian steroidogenesis.CrossRef | 1:CAS:528:DyaK2MXnvVeks7w%3D&md5=c4a43608087ce79066348e4b1e961479CAS |

Pankhurst, N. W., Purser, G. J., Van Der Kraak, G., Thomas, P. M., and Forteath, G. N. R. (1996). Effect of holding temperature on ovulation, egg fertility, plasma levels of reproductive hormones and in vitro ovarian steroidogenesis in the rainbow trout Oncorhynchus mykiss. Aquaculture. 146, 277–290.
Effect of holding temperature on ovulation, egg fertility, plasma levels of reproductive hormones and in vitro ovarian steroidogenesis in the rainbow trout Oncorhynchus mykiss.CrossRef | 1:CAS:528:DyaK2sXktlKrtw%3D%3D&md5=cedebe59a024370d4cf58f1f552634a1CAS |

Pankhurst, N. W., Fitzgibbon, Q. P., Pankhurst, P. M., and King, H. R. (2008). Habitat-related variation in reproductive endocrine condition in the coral reef damselfish Acanthochromis polyacanthus. General and Comparative Endocrinology 155, 386–397.
Habitat-related variation in reproductive endocrine condition in the coral reef damselfish Acanthochromis polyacanthus.CrossRef | 1:CAS:528:DC%2BD1cXislCktw%3D%3D&md5=715e0493f7cf08014b13360aaba84e53CAS |

Pankhurst, N. W., King, H. R., Anderson, K., Elizur, A., Pankhurst, P. M., et al. (2011). Thermal impairment of reproduction is differentially expressed in maiden and repeat spawning Atlantic salmon. Aquaculture 316, 77–87.
Thermal impairment of reproduction is differentially expressed in maiden and repeat spawning Atlantic salmon.CrossRef | 1:CAS:528:DC%2BC3MXlsFGlt7g%3D&md5=8c8980c3ee9729dc43eb8157d323970dCAS |

Pauly, D., and Pullin, R. S. V. (1988). Hatching time in spherical pelagic marine eggs in response to temperature and egg size. Environmental Biology of Fishes 22, 261–271.
Hatching time in spherical pelagic marine eggs in response to temperature and egg size.CrossRef |

Planas, J. V., and Swanson, P. (2008). Physiological function of gonadotropins in fish. In ‘Fish Reproduction’. (Eds M. J. Rocha, A. Arukwe and B. G. Kapoor.) pp. 37–66. (Science Publishers: Enfield, NH, USA.)

Pörtner, H. O., and Farrell, A. P. (2008). Physiology and climate change. Science 322, 690–692.
Physiology and climate change.CrossRef |

Pörtner, H. O., Langenbuch, M., and Reipschlager, A. (2004). Biological impact of elevated ocean CO2 concentrations: lessons from animal physiology and earth history. Journal of Oceanography 60, 705–718.
Biological impact of elevated ocean CO2 concentrations: lessons from animal physiology and earth history.CrossRef |

Reddin, D. G., Helbig, J., Thomas, A., Whitehouse, B. G., and Friedland, K. D. (2000). Survival of Atlantic salmon (Salmo salar L.) related to marine climate. In ‘The Ocean Life of Atlantic Salmon’. (Ed. D. Mills.) pp. 88–91. (Blackwell Science: Oxford.)

Reyjol, Y., Léna, J.-P., Hervant, F., and Pont, D. (2009). Effects of temperature on biological and biochemical indicators of the life-history strategy of bullhead Cottus gobio. Journal of Fish Biology 75, 1427–1445.
Effects of temperature on biological and biochemical indicators of the life-history strategy of bullhead Cottus gobio.CrossRef | 1:CAS:528:DC%2BD1MXhs1Slur7M&md5=1c7f6d6959886e8a4a7ac101a88abce8CAS |

Robertson, D. R. (1991). The role of adult biology in the timing of spawning of tropical reef fishes. In ‘The Ecology of Fishes on Coral Reefs’. (Ed. P. F. Sale.) pp. 357–386. (Academic Press: San Diego.)

Rombough, P. J. (1997). The effects of temperature on embryonic and larval development. In ‘Global Warming: Implications for Freshwater and Marine Fish’. (Eds C. M. Wood and D. G. McDonald.) pp. 177–223. (Cambridge University Press: Cambridge.)

Schreck, C. B. (2010). Stress and fish reproduction: the roles of allostasis and hormesis. General and Comparative Endocrinology 165, 549–556.
Stress and fish reproduction: the roles of allostasis and hormesis.CrossRef | 1:CAS:528:DC%2BC3cXktVentQ%3D%3D&md5=026f2f41d60ecb00cb956263e9cec28cCAS |

Scott, S. G., and Pankhurst, N. W. (1992). Interannual variation in the reproductive cycle of the New Zealand snapper Pagrus auratus (Bloch & Schneider) (Sparidae). Journal of Fish Biology 41, 685–696.
Interannual variation in the reproductive cycle of the New Zealand snapper Pagrus auratus (Bloch & Schneider) (Sparidae).CrossRef |

Shimizu, A. (2003). Effect of photoperiod and temperature on gonadal activity and plasma steroid levels in a reared strain of the mummichog (Fundulus heteroclitus) during different phases of its annual reproductive cycle. General and Comparative Endocrinology 131, 310–324.
Effect of photoperiod and temperature on gonadal activity and plasma steroid levels in a reared strain of the mummichog (Fundulus heteroclitus) during different phases of its annual reproductive cycle.CrossRef | 1:CAS:528:DC%2BD3sXjtFWmtLs%3D&md5=65d8a1703e4b97a574552ece56328be2CAS |

Skelly, D. K., Joseph, L. N., Possingham, H. P., Freidenburg, L. K., Farrugia, T. J., et al. (2007). Evolutionary responses to climate change. Conservation Biology 21, 1353–1355.
Evolutionary responses to climate change.CrossRef |

Smith, A. M. (2009). Bryozoans as southern sentinels of ocean acidification: a major role for a minor phylum. Marine and Freshwater Research 60, 475–482.
Bryozoans as southern sentinels of ocean acidification: a major role for a minor phylum.CrossRef | 1:CAS:528:DC%2BD1MXmtlOms70%3D&md5=3a4d5f476c9a2aa59bf018271f974778CAS |

Sogard, S. M. (1997). Size-selective mortality in the juvenile stage of teleost fishes: a review. Bulletin of Marine Science 60, 1129–1157.

Soria, F. N., Strüssman, C. A., and Miranda, L. A. (2008). High water temperatures impair the reproductive ability of the pejerrey fish Odontesthes bonariensis: effects on the hypophyseal–gonadal axis. Physiological and Biochemical Zoology 81, 898–905.
High water temperatures impair the reproductive ability of the pejerrey fish Odontesthes bonariensis: effects on the hypophyseal–gonadal axis.CrossRef | 1:CAS:528:DC%2BD1cXhsFansbzF&md5=323e292c47a097e96b1ec577a68a516fCAS |

Sponaugle, S., and Cowen, R. K. (1996). Larval supply and patterns of recruitment for two Caribbean reef fishes, Stegastes partitus and Acanthurus bahianus. Marine and Freshwater Research 47, 433–447.
Larval supply and patterns of recruitment for two Caribbean reef fishes, Stegastes partitus and Acanthurus bahianus.CrossRef |

Stacey, N. E. (1984). Control of the timing of ovulation by exogenous and endogenous factors. In ‘Fish Reproduction: Strategies and Tactics’. (Eds G. W. Potts and R. J. Wootton.) pp. 207–222. (Academic Press: London.)

Tveiten, H., and Johnsen, H. K. (2001). Thermal influences on temporal changes in plasma testosterone and oestradiol-17β concentrations during gonadal recrudescence in female common wolffish. Journal of Fish Biology 59, 175–178.
| 1:CAS:528:DC%2BD3MXksF2mtLk%3D&md5=95b8301bc218710a1c6d1c2103b88da2CAS |

Tveiten, H., Solevåg, S. E., and Johnsen, H. K. (2001). Holding temperature during the breeding season influences final maturation and egg quality in common wolffish. Journal of Fish Biology 58, 374–385.
Holding temperature during the breeding season influences final maturation and egg quality in common wolffish.CrossRef |

Tyler, C. R., Santos, E. M., and Prat, F. (2000). Unscrambling the egg – cellular, biochemical, molecular and endocrine advances in oogenesis. In ‘Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish’. (Eds B. Norberg, O. S. Kjesbu, G-L. Taranger, E. Andersson and S. O. Stefansson.) pp. 273–280. (John Grieg A/S: Bergen.)

Van Der Kraak, G., and Pankhurst, N. W. (1997). Temperature effects on the reproductive performance of fish. In ‘Global Warming: Implications for Freshwater and Marine Fish’. (Eds C. M. Wood and D. G. McDonald.) pp. 159–176. (Cambridge University Press: Cambridge.)

Wahl, B., and Löffler, H. (2009). Influences on the natural reproduction of whitefish (Coregonus lavaretus) in Lake Constance. Canadian Journal of Fisheries and Aquatic Sciences 66, 547–556.
Influences on the natural reproduction of whitefish (Coregonus lavaretus) in Lake Constance.CrossRef |

Widdicombe, S., and Spicer, J. I. (2008). Predicting the impact of ocean acidification on benthic biodiversity: what can animal physiology tell us? Journal of Experimental Marine Biology and Ecology 366, 187–197.
Predicting the impact of ocean acidification on benthic biodiversity: what can animal physiology tell us?CrossRef |

Wilson, D. T., and Meekan, M. G. (2002). Growth-related advantages for survival to the point of replenishment in the coral reef fish Stegastes partitus (Pomacentridae). Marine Ecology Progress Series 231, 247–260.
Growth-related advantages for survival to the point of replenishment in the coral reef fish Stegastes partitus (Pomacentridae).CrossRef |

Zohar, Y., Muñoz-Cueto, J. A., Elizur, A., and Kah, O. (2010). Neuroendocrinology of reproduction in teleost fish. General and Comparative Endocrinology 165, 438–455.
Neuroendocrinology of reproduction in teleost fish.CrossRef | 1:CAS:528:DC%2BC3cXktVensw%3D%3D&md5=7946053c849bf4e3daaba0bd213dfcf2CAS |


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