When cooling is worse than warming: investigations into the thermal tolerance of an endemic reef fish, Boopsoidea inornata

References

• Angiulli E, Pagliara V, Cioni C, Frabetti F, Pizzetti F, Alleva E, Toni M. 2020. Increase in environmental temperature affects exploratory behaviour, anxiety and social preference in Danio rerio. Scientific Reports 10: article 5385.
   PubMed Web of Science ®Google Scholar
• Aravena G, Broitman B, Stenseth NC. 2014. Twelve years of change in coastal upwelling along the central-northern coast of Chile: spatially heterogeneous responses to climatic variability. PLoS ONE 9: e90276.
   PubMed Web of Science ®Google Scholar
• Attwood CG, Ensair HAM. 2020. Life-history trade-offs among four sympatric seabreams. Potts WM, Attwood CG, Cowley PD (eds), Linefish resilience in the Anthropocene. African Journal of Marine Science 43: 323–337.
   Google Scholar
• Bakun A. 1990. Global climate change and intensification of coastal ocean upwelling. Science 247: 198–201.
   PubMed Web of Science ®Google Scholar
• Bakun A, Field DB, Rodriquez AR, Weeks SJ. 2010. Greenhouse gas, upwelling-favourable winds, and the future of coastal ocean upwelling ecosystems. Global Change Biology 16: 1213–1228.
   Web of Science ®Google Scholar
• Bard B, Kieffer JD. 2019. The effects of repeat acute thermal stress on the critical thermal maximum (CTmax) and physiology of juvenile shortnose sturgeon (Acipenser brevirostrum). Canadian Journal of Zoology 97: 567–572.
   Google Scholar
• Barton BA. 2002. Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integrative and Comparative Biology 42: 517–525.
   PubMed Web of Science ®Google Scholar
• Barton BA, Peter RE, Paulencu CR. 1980. Plasma cortisol levels of fingerling rainbow trout (Salmo gairdneri) at rest, and subjected to handling, confinement, transport, and stocking. Canadian Journal of Fisheries and Aquatic Sciences 37: 805–811.
   Web of Science ®Google Scholar
• Bates AE, Helmuth B, Burrows MT, Duncan MI, Garrabou J, Guy-Haim T et al. 2018. Biologists ignore ocean weather at their peril. Nature 560: 299–301.
   PubMed Web of Science ®Google Scholar
• Bates AE, Cooke RS, Duncan MI, Edgar GJ, Bruno JF, Benedetti- Cecchi L et al. 2019. Climate resilience in marine protected areas and the ‘Protection Paradox’. Biological Conservation 236: 305–314.
   Web of Science ®Google Scholar
• Biro PA, Beckmann C, Stamps JA. 2010. Small within-day increases in temperature affects boldness and alters personality in coral reef fish. Proceedings of the Royal Society B: Biological Sciences 277: 71–77.
   PubMed Web of Science ®Google Scholar
• Bozinovic F, Pörtner HO. 2015. Physiological ecology meets climate change. Ecology and Evolution 5: 1025–1030.
   PubMed Web of Science ®Google Scholar
• Brandão ML, Colognesi G, Costa-Ferreira RSC, Carvalho TB, Gonçalves-de-Freitas E. 2018. Water temperature affects aggressive interactions in a Neotropical cichlid fish. Neotropical Ichthyology 16: e170081.
   Web of Science ®Google Scholar
• Brownscombe JW, Gutowsky FG, Danylchuk AJ, Cooke SJ. 2014. Foraging behaviour and activity of a marine benthivorous fish estimated using tri-axial accelerometer biologgers. Marine Ecology Progress Series 505: 241–251.
   Web of Science ®Google Scholar
• Buxton CD, Smale MJ. 1984. A preliminary investigation of the ichthyofauna of the Tsitsikamma Coastal National Park. Koedoe 27: 13–24.
   Google Scholar
• Chen IC, Hill JK, Ohlemuller R, Roy DB, Thomas CD. 2011. Rapid range shifts of species associated with high levels of climate warming. Science 333: 1024–1026.
   PubMed Web of Science ®Google Scholar
• Clark TD, Sandblom E, Jutfelt F. 2013. Response to Farrell and to Pörtner and Giomi. Journal of Experimental Biology 216: 4495–4497.
   PubMedGoogle Scholar
• Collins M, Knutti R, Arblaster J, Dufresne JL, Fichefet T, Friedlingstein P et al. 2013. Long-term climate change: projections, commitments and irreversibility. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J et al. (eds), Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK and New York: Cambridge University Press. pp 1029–1136.
   Google Scholar
• Datta T, Acharya S, Das MK. 2002. Physiological effect of cold shock in juvenile Labeo rohita (Hamilton-Buchanan). Indian Journal of Fisheries 49: 223–227.
   Google Scholar
• Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR. 2008. Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences of the United States of America 105: 6668–6672.
   PubMed Web of Science ®Google Scholar
• Donaldson MR, Cooke SJ, Patterson DA, MacDonald JS. 2008. Cold shock and fish. Journal of Fish Biology 73: 1491–1530.
   Web of Science ®Google Scholar
• Dowd WW, King FA, Denny MW. 2015. Thermal variation, thermal extremes and the physiological performance of individuals. Journal of Experimental Biology 218: 1956–1967.
   PubMed Web of Science ®Google Scholar
• Dülger N, Kumlu M, Türkmen S, Ölçülü A, Eroldoğan OT, Yılmaz HA, Öçal N. 2012. Thermal tolerance of European Sea Bass (Dicentrarchus labrax) juveniles acclimated to three temperature levels. Journal of Thermal Biology 307: 79–82.
   Google Scholar
• Duncan MI, James N, Bates A, Goschen W, Potts W. 2019a. Localised intermittent upwelling intensity has increased along South Africa’s south coast due to El Niño–Southern Oscillation phase state. African Journal of Marine Science 41: 325–330.
   Web of Science ®Google Scholar
• Duncan MI, Bates AE, James NC, Potts WM. 2019b. Exploitation may influence the climate resilience of fish populations through removing high performance metabolic phenotypes. Scientific Reports 9: 1–10.
   PubMed Web of Science ®Google Scholar
• Eme J, Bennett WA. 2009. Critical thermal tolerance polygons of tropical marine fishes from Sulawesi, Indonesia. Journal of Thermal Biology 34: 220–225.
   Web of Science ®Google Scholar
• Engelsma MY, Hougee S, Nap D, Hofenk M, Rombout JHWM, van Muiswinkel WB, Lidy Verburg-van Kemenade BM. 2003. Multiple acute temperature stress affects leucocyte populations and antibody responses in common carp, Cyprinus carpio L. Fish and Shellfish Immunology 15: 397–410.
   PubMed Web of Science ®Google Scholar
• Fangue NA, Hofmeister M, Schulte PM. 2006. Intraspecific variation in thermal tolerance and heat shock protein gene expression in common killifish, Fundulus heteroclitus. The Journal of Experimental Biology 209: 2859–2872.
   PubMed Web of Science ®Google Scholar
• García-Reyes M, Sydeman WJ, Schoeman DS, Rykaczewski RR, Black BA, Smit AJ, Bograd SJ. 2015. Under pressure: climate change, upwelling, and eastern boundary upwelling ecosystems. Frontiers in Marine Science 2: article 109.
   Web of Science ®Google Scholar
• Gonzalez RJ, McDonald DG. 2000. Ionoregulatory responses to temperature change in two species of freshwater fish. Fish Physiology and Biochemistry 33: 311–317.
   Google Scholar
• Goschen WS, Schumann EH. 1995. Upwelling and the occurrence of cold water around Cape Recife, Algoa Bay, South Africa. South African Journal of Marine Science 16: 57–67.
   Web of Science ®Google Scholar
• Goschen S, Bornman TG, Deyzel SHP, Schumann EH. 2015. Coastal upwelling on the far eastern Agulhas Bank associated with large meanders in the Agulhas Current. Continental Shelf Research 101: 34–46.
   Web of Science ®Google Scholar
• Gutiérrez D, Bouloubassi I, Sifeddine A, Purca S, Goubanova K, Graco M et al. 2011. Coastal cooling and increased productivity in the main upwelling zone off Peru since the mid-twentieth century. Geophysical Research Letters 38: L07603.
   Web of Science ®Google Scholar
• Heath AG. 1973. Ventilatory responses of teleost fish to exercise and thermal stress. American Zoology 13: 491–503.
   Google Scholar
• Hanekom N, Hutchings L, Joubert PA, van der Byl PCN. 1989. Sea temperature variations in the Tsitsikamma Coastal National Park, South Africa, with notes on the effect of cold conditions on some fish populations. South African Journal of Marine Science 8: 145–153.
   Web of Science ®Google Scholar
• Holt RE, Jørgensen C. 2015. Climate change in fish: effects of respiratory constraints on optimal life history and behaviour. Biology Letters 11: 20141032.
   PubMed Web of Science ®Google Scholar
• Hoegh-Guldberg O, Cai R, Poloczanska ES, Brewer PG, Sundby S, Hilmi K et al. 2014. The ocean. In: Barros VR, Field CB, Dokken DJ et al. (eds), Climate change 2014: impacts, adaptation, and vulnerability. Part B: regional aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press. pp 1655–1731.
   Google Scholar
• James NV, van Niekerk L, Whitfield AK, Potts WM, Götz A, Paterson AW. 2013. Effects of climate change on South African estuaries and associated fish species. Climate Research 57: 233–248.
   Web of Science ®Google Scholar
• Jayiya TP, Mann BQ, Wilke C. 2000. Boopsoidea inornata. In: Mann BQ (ed.), Southern African marine linefish status reports. Special Publication No. 7. Durban, South Africa: Oceanographic Research Institute. pp 210–211.
   Google Scholar
• Johansen JL, Messmer V, Coker DJ, Hoey AS, Pratchett MS. 2014. Increasing ocean temperatures reduce activity patterns of a large commercially important coral reef fish. Global Change Biology 20: 1067–1074.
   PubMed Web of Science ®Google Scholar
• Jutfelt F, Norin T, Ern R, Overgaard J, Wang T, McKenzie DJ et al. 2018. Oxygen- and capacity-limited thermal tolerance: blurring ecology and physiology. Journal of Experimental Biology 221: jeb169615.
   PubMed Web of Science ®Google Scholar
• Koštál V, Vambera J, Bastl J. 2004. On the nature of pre-freeze mortality in insects: water balance, ion homeostasis and energy charge in the adults of Pyrrhocoris apterus. Journal of Experimental Biology 207: 1509–1521.
   PubMed Web of Science ®Google Scholar
• Lutterschmidt W, Hutchison VH. 1997. The critical thermal maximum: data to support the onset of spasms as the definitive end point. Canadian Journal of Zoology 75: 1553–1560.
   Web of Science ®Google Scholar
• Mackie P, Wright PA, Glebe BD, Ballantyne JS. 2005. Osmoregulation and gene expression of Naþ/Kþ ATPase in families of Atlantic salmon (Salmo salar) smolts. Canadian Journal of Fisheries and Aquatic Sciences 62: 2661–2672.
   Web of Science ®Google Scholar
• MacMillan HA. 2019. Dissecting cause from consequence: a systematic approach to thermal limits. Journal of Experimental Biology 222: jeb191593.
   Web of Science ®Google Scholar
• Madeira D, Narciso L, Cabral HN, Vinagre C, Diniz MS. 2013 Influence of temperature in thermal and oxidative stress responses in estuarine fish. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology 166: 237–243.
   PubMed Web of Science ®Google Scholar
• Martínez JD, Cadena CD, Torres M. 2016. Critical thermal limits of Poecilia caucana (Steindachner, 1880) (Cyprinodontiformes: Poeciliidae). Neotropical Ichthyology 14: e150171.
   Web of Science ®Google Scholar
• Mazeaud MM, Mazeaud F, Donaldson EM. 1977. Primary and secondary effects of stress in fish: some new data with a general review. Transactions of the American Fisheries Society 106: 201–212.
   Web of Science ®Google Scholar
• McGregor HV, Dima M, Fischer HW, Mulitza S. 2007. Rapid 20th-century increase in coastal upwelling off northwest Africa. Science 315: 637–639.
   PubMed Web of Science ®Google Scholar
• Morgan R, Finnøen MH, Jutfelt F. 2018. CTmax is repeatable and doesn’t reduce growth in zebrafish. Scientific Reports 8: article 7099.
   Web of Science ®Google Scholar
• Motani R, Wainwright P. 2015. How warm is too warm for the life cycle of actinopterygian fishes? Scientific Reports 5: 11597.
   PubMed Web of Science ®Google Scholar
• Muggeo V. 2008. Segmented: an R package to fit regression models with broken-line relationships. R News 8: 20–25.
   Google Scholar
• O’Sullivan JDB, MacMillan HA, Overgaard J. 2017. Heat stress is associated with disruption of ion balance in the migratory locust, Locusta migratoria. Journal of Thermal Biology 68: 177–185.
   PubMed Web of Science ®Google Scholar
• Perry AL, Low PJ, Ellis JR, Reynolds JD. 2005. Climate change and distribution shifts in marine fishes. Science 308: 1912–1915.
   PubMed Web of Science ®Google Scholar
• Pörtner HO. 2008. Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Marine Ecology Progress Series 373: 203–217.
   Web of Science ®Google Scholar
• Pörtner HO. 2010. Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. Journal of Experimental Biology 213: 881–893.
   PubMed Web of Science ®Google Scholar
• Pörtner HO, Knust R. 2007. Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315: 95–97.
   PubMed Web of Science ®Google Scholar
• Pörtner HO, Mark FC, Bock C. 2004. Oxygen limited thermal tolerance in fish: answers obtained by nuclear magnetic resonance techniques. Respiratory Physiology and Neurobiology 141: 243–260.
   PubMed Web of Science ®Google Scholar
• Potts WM, Booth AJ, Richardson TJ, Sauer WHH. 2014. Ocean warming affects the distribution and abundance of resident fishes by changing their reproductive scope. Reviews in Fish Biology and Fisheries 24: 493–504.
   Web of Science ®Google Scholar
• Potts WM, Götz A, James N. 2015. Review of the projected impacts of climate change on coastal fishes in southern Africa. Reviews in Fish Biology and Fisheries 25: 603–630.
   Web of Science ®Google Scholar
• R Core Team. 2017. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
   Google Scholar
• Rajaguru S. 2002. Critical thermal maximum of seven estuarine fishes. Journal of Thermal Biology 27: 125–128.
   Web of Science ®Google Scholar
• Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ. 2007. Integrating animal temperament within ecology and evolution. Biological Reviews 82: 291–318.
   PubMed Web of Science ®Google Scholar
• Rezende EL, Tejedo M, Santos M. 2010. Estimating the adaptive potential of critical thermal limits: methodological problems and evolutionary implications. Functional Ecology 25: 111–121.
   Web of Science ®Google Scholar
• Rhein M, Rintoul SR, Aoki S, Campos E, Chambers D, Feely RA et al. 2013. Observations: ocean. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J et al. (eds), Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK and New York: Cambridge University Press. pp 255–316.
   Google Scholar
• Rijnsdorp AD, Peck MA, Engelhard GH, Möllmann C, Pinnegar JK. 2009. Resolving the effect of climate change on fish populations. Journal of Marine Science 66: 1570–1583.
   Web of Science ®Google Scholar
• Rouault M, Penven P, Pohl B. 2009. Warming in the Agulhas Current system since the 1980s. Geophysical Research Letters 36: L12602.
   Web of Science ®Google Scholar
• Rouault M, Pohl B, Penven P. 2010. Coastal oceanic climate change and variability from 1982 to 2009 around South Africa. African Journal of Marine Science 32: 237–246.
   Web of Science ®Google Scholar
• Schumann EH, Ross GJB, Goschen WS. 1988. Cold-water events in Algoa Bay and along the Cape South Coast, South Africa, in March/April 1987. South African Journal of Science 84: 579–584.
   Web of Science ®Google Scholar
• Schumann EH, Cohen AL, Jury MR. 1995. Coastal sea surface temperature variability along the south coast of South Africa and the relationship to regional and global climate. Journal of Marine Research 53: 231–248.
   Web of Science ®Google Scholar
• Schwing FB, Mendelssohn R. 1997. Increased coastal upwelling in the California Current System. Journal of Geophysical Research 102: 3421–3438.
   Web of Science ®Google Scholar
• Sih A, Bell AM, Johnson JC, Ziemba RE. 2004. Behavioral syndromes: an integrative overview. Quarterly Review of Biology 79: 241–277.
   PubMed Web of Science ®Google Scholar
• Smith MM, Heemstra PC (eds). 1991. Smith’s sea fishes. Johannesburg, South Africa: Southern Book Publishers.
   Google Scholar
• Somero GN, Hofmann GE. 1996. Temperature thresholds for protein adaptation: when does temperature start to ‘hurt’? ln: Wood CM, McDonald DG (eds), Global warming: implications for freshwater and marine fish. Cambridge, UK: Cambridge University Press: pp 1–24.
   Google Scholar
• Sydeman WJ, García-Reyes M, Schoeman DS, Rykaczewski RR, Thompson SA, Black BA, Bograd SJ. 2014. Climate change and wind intensification in coastal upwelling ecosystems. Science 345: 77–80.
   PubMed Web of Science ®Google Scholar
• Szekeres P, Brownscombe JW, Cull F, Danylchuk AJ, Shultz AD, Suski CD et al. 2014. Physiological and behavioural consequences of cold shock on bonefish (Albula vulpes) in The Bahamas. Journal of Experimental Marine Biology and Ecology 459: 1–7.
   Web of Science ®Google Scholar
• Tanck MWT, Vermeulen KJ, Bovenhuis H, Komen H. 2001. Heredity of stress-related cortisol response in androgenetic common carp (Cyprinus carpio L). Aquaculture 199: 283–294.
   Web of Science ®Google Scholar
• Terblanche JS, Deere JA, Clusella-Trullas S, Janion C, Chown SL. 2007. Critical thermal limits depend on methodological context. Proceedings of the Royal Society B: Biological Sciences 274: 2935–2943.
   PubMed Web of Science ®Google Scholar
• van der Elst R. 1993. The common sea fishes of southern Africa. Cape Town, South Africa: Struik Publishers.
   Google Scholar
• Van Der Kraak G, Pankhurst NW. 1997. Temperature effects on the reproductive performance of fish. In: Wood CM, McDonald DG (eds), Global warming: implications for freshwater and marine fish. Cambridge, UK: University Press. pp 159–176.
   Google Scholar
• Ward TD, Algera DA, Gallagher AJ, Hawkins E, Horodysky A, Jørgensen C et al. 2016. Understanding the individual to implement the ecosystem approach to fisheries management. Conservation Physiology 4: cow005.
   Web of Science ®Google Scholar
• Wong B, Candolin U. 2015. Behavioral responses to changing environments. Behavioral Ecology 26: 665–673.
   Web of Science ®Google Scholar
• Wood AD. 1998. A contribution towards the taxonomy of the ichthyoplankton species community and an understanding of its dynamics along the south-east coast of South Africa. PhD thesis, Rhodes University, South Africa.
   Google Scholar
• Wood AD, Brouwer SL, Cowley PD, Harrison TD. 2000. An updated checklist of the ichthyofaunal species assemblage of the Tsitsikamma National Park, South Africa. Koedoe 43: 83–95.
   Google Scholar
• Zarate J, Bradley TM. 2003. Heat shock proteins are not sensitive indicators of hatchery stress in salmon. Aquaculture 223: 175–187.
   Web of Science ®Google Scholar