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Hot or not? Comparative behavioral thermoregulation, critical temperature regimes, and thermal tolerances of the invasive lionfish Pterois sp. versus native western North Atlantic reef fishes

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Abstract

Temperature influences the geographic range, physiology, and behavior of many ectothermic species, including the invasive lionfish Pterois sp. Thermal parameters were experimentally determined for wild-caught lionfish at different acclimation temperatures (13, 20, 25 and 32 °C). Preferences and avoidance were evaluated using a videographic shuttlebox system, while critical thermal methodology evaluated tolerance. The lionfish thermal niche was compared experimentally to two co-occurring reef fishes (graysby Cephalopholis cruentata and schoolmaster Lutjanus apodus) also acclimated to 25 °C. The physiologically optimal temperature for lionfish is likely 28.7 ± 1 °C. Lionfish behavioral thermoregulation was generally linked to acclimation history; tolerance and avoidance increased significantly at higher acclimation temperatures, but final preference did not. The tolerance polygon of lionfish shows a strong correlation between thermal limits and acclimation temperature, with the highest CTmax at 39.5 °C and the lowest CTmin at 9.5 °C. The tolerance range of invasive lionfish (24.61 °C) is narrower than those of native graysby (25.25 °C) and schoolmaster (26.87 °C), mostly because of lower thermal maxima in the former. Results show that lionfish display “acquired” thermal tolerance at higher and lower acclimation temperatures, but are no more eurythermal than other tropical fishes. Collectively, these results suggest that while lionfish range expansion in the western Atlantic is likely over the next century from rising winter sea temperatures due to climate change, the magnitude of poleward radiation of this invasive species is limited and will likely be equivalent to native tropical and subtropical fishes with similar thermal minima.

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References

  • Able KW, Fahay MP (1998) The first year in the life of estuarine fishes in the middle Atlantic Bight. Rutgers University Press, New Brunswick

    Google Scholar 

  • Albins MA, Lyons PJ (2012) Invasive red lionfish Pterois volitans blow directed jets of water at prey fish. Mar Ecol Prog Ser 448:1–5

    Google Scholar 

  • Arendt MD, Lucy JA, Munroe TA (2001) Seasonal occurrence and site-utilization patterns of adult tautog, Tautoga onitis (Labridae), at manmade and natural structures in lower Chesapeake Bay. Fish Bull 99(4):519–528

    Google Scholar 

  • Barbour AB, Montgomery ML, Adamson AA, Diaz-Ferguson E, Silliman BR (2010) Mangrove use by the invasive lionfish Pterois volitans. Mar Ecol Prog Ser 401:291–294

    Google Scholar 

  • Beck MW, Heck KL Jr, Able KW, Childers DL, Eggleston DB, Gillanders BM, Halpern B, Hays CG, Hoshino K, Minello TJ, Orth RJ (2001) The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates: a better understanding of the habitats that serve as nurseries for marine species and the factors that create site-specific variability in nursery quality will improve conservation and management of these areas. Bioscience 51(8):633–641

    Google Scholar 

  • Becker CD, Genoway RG (1979) Evaluation of the critical thermal maximum for determining thermal tolerance of freshwater fish. Environ Biol Fishes 4:245–256

    Google Scholar 

  • Beitinger TL, Bennett WA, McCauley RW (2000) Temperature tolerances of North American freshwater fishes exposed to dynamic changes in temperature. Environ Biol Fishes 58:237–275

    Google Scholar 

  • Boesch DF, Turner RE (1984) Dependence of fishery species on salt marshes: the role of food and refuge. Estuaries 7:460–468

    Google Scholar 

  • Bogert CM (1949) Thermoregulation in reptiles, a factor in evolution. Evolution 3:195–211

    PubMed  CAS  Google Scholar 

  • Booth DJ, Bond N, Macreadie P (2011) Detecting range shifts among Australian fishes in response to climate change. Mar Freshw Res 62:1027–1042

    Google Scholar 

  • Brett JR (1956) Some principles in the thermal requirements of fishes. Quart Rev Biol 31(2):75–87

    Google Scholar 

  • Brett JR (1971) Energetic responses of salmon to temperature. A study of some thermal relations in the physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerka). Am Zool 11:99–113

    Google Scholar 

  • Buckley LB, Ehrenberger JC, Angilletta MJ (2015) Thermoregulatory behaviour limits local adaptation of thermal niches and confers sensitivity to climate change. Funct Ecol 29:1038–1047

    Google Scholar 

  • Cerino D, Overton AS, Rice JA, Morris JA (2013) Bioenergetics and trophic impacts of the invasive Indo-Pacific lionfish. Trans Am Fish Soc 142:1522–1534

    Google Scholar 

  • Chung KS (1995) Thermal acclimation rate of the tropical long-whiskered catfish Pimelodella chagresi to high temperature. Caribb J Sci 31:154–156

    Google Scholar 

  • Cincotta DA, Stauffer JR (1984) Temperature preference and avoidance studies of six North American freshwater fish species. Hydrobiologia 109:173–177

    Google Scholar 

  • Clark TD, Sandblom E, Jutfelt F (2013) Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. J Exp Biol 216:2771–2782

    PubMed  Google Scholar 

  • Côté IM, Green SJ (2012) Potential effects of climate change on a marine invasion: the importance of current context. Curr Zool 58:1–8

    Google Scholar 

  • Cox DK (1974) Effects of three heating rates on the critical thermal maximum of bluegill. In: Thermal ecology: proceedings of a symposium held at Augusta, Georgia, 3–5 May 1973. pp 158–163

  • Eme J, Bennett WA (2009) Critical thermal tolerance polygons of tropical marine fishes from Sulawesi, Indonesia. J Therm Biol 34:220–225

    Google Scholar 

  • Ferreira CEL, Luiz OJ, Floeter SR, Lucena MB, Barbosa MC, Rocha CR, Rocha LA (2015) First record of invasive lionfish (Pterois volitans) for the Brazilian coast. PLoS ONE 10:e0123002

    PubMed  PubMed Central  Google Scholar 

  • Figueira WF, Booth DJ (2010) Increasing ocean temperatures allow tropical fishes to survive overwinter in temperate waters. Glob Change Biol 16:506–516

    Google Scholar 

  • Freshwater DW, Hines A, Parham S, Wilbur A, Sabaoun M, Woodhead J, Akins L, Purdy B, Whitfield PE, Paris CB (2009) Mitochondrial control region sequence analyses indicate dispersal from the US East Coast as the source of the invasive Indo-Pacific lionfish Pterois volitans in the Bahamas. Mar Biol 156:1213–1221

    Google Scholar 

  • Fry FEJ (1947) Effect of environment on animal activity. Univ Toronto Stud Biol Ser 55:1–62

    Google Scholar 

  • Fry FEJ, Brett JR, Clawson GH (1942) Lethal limits of temperature for young goldfish. Revue Canadienne de Biologie 1:50–56

    Google Scholar 

  • González J, Grijalba-Bendeck M, Acero A, Betancur-R R (2009) The invasive red lionfish, Pterois volitans (Linnaeus 1758), in the southwestern Caribbean Sea. Aquat Invasions 4:507–510

    Google Scholar 

  • Habary A, Johansen JL, Nay TJ, Steffensen JF, Rummer JL (2016) Adapt, move, or die—how will tropical coral reef fishes cope with ocean warming? Glob Change Biol 23:566–577

    Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Preito R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    PubMed  CAS  Google Scholar 

  • Horodysky AZ, Cooke SJ, Brill RW (2015) Physiology in the service of fisheries science: why thinking mechanistically matters. Rev Fish Biol Fish 25:425–447

    Google Scholar 

  • Huey RB, Stevenson RD (1979) Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. Am Zool 19:357–366

    Google Scholar 

  • Hutchison VH (1961) Critical thermal maxima in salamanders. Physiol Zool 34:92–125

    Google Scholar 

  • Jobling M (1981) Temperature tolerance and the final preferendum—rapid methods for the assessment of optimum growth temperatures. J Fish Biol 19:439–455

    Google Scholar 

  • Jud ZR, Layman CA, Lee JA, Arrington DA (2011) Recent invasion of a Florida (USA) estuarine system by lionfish Pterois volitans/P. miles. Aquat Biol 13:21–26

    Google Scholar 

  • Kearney M, Shine R, Porter WP (2009) The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming. Proc Natl Acad Sci 106:3835–3840

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kelsch SW, Neill WH (1990) Temperature preference versus acclimation in fishes: selection for changing metabolic optima. Trans Am Fish Soc 119:601–610

    Google Scholar 

  • Killen SS (2014) Growth trajectory influences temperature preference in fish through an effect on metabolic rate. J Anim Ecol 83:1513–1522

    PubMed  PubMed Central  Google Scholar 

  • Kimball ME, Miller JM, Whitfield PE, Hare JA (2004) Thermal tolerance and potential distribution of invasive lionfish (Pterois volitans/miles complex) on the east coast of the United States. Mar Ecol Prog Ser 283:269–278

    Google Scholar 

  • Luiz OJ, Floeter SR, Rocha LA, Ferreira CEL (2013) Perspectives for the lionfish invasion in the South Atlantic: are Brazilian reefs protected by the currents. Mar Ecol Prog Ser 485:1–7

    Google Scholar 

  • Marais E, Chown SL (2008) Beneficial acclimation and the Bogert effect. Ecol Lett 11:1027–1036

    PubMed  Google Scholar 

  • Medvick PA, Miller JM (1979) Behavioral thermoregulation in three Hawaiian reef fishes. Environ Biol Fishes 4:23–28

    Google Scholar 

  • Miloslavich P, Klein E, Díaz JM, Hernandez CE, Bigatti G, Campos L, Artigas F, Castillo J, Penchaszadeh PE, Neill PE, Carranza A, Retana MV, Diaz de Astarloa JM, Lewis M, Yorio M, Piriz ML, Rodriguez D, Yoneshigue-Valentin Y, Gamboa L, Martin A (2011) Marine biodiversity in the Atlantic and Pacific Coasts of South America: knowledge and gaps. PLoS ONE 6:e14631

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mora C, Ospina A (2001) Tolerance to high temperatures and potential impact of sea warming on reef fishes of Gorgona Island (tropical eastern Pacific). Mar Biol 139:765–769

    Google Scholar 

  • Morris JA, Whitfield PE (2009) Biology, ecology, control and management of the invasive Indo-Pacific lionfish: an updated integrated assessment. NOAA Technical Memorandum NOS NCCOS 99. 57

  • Murdy EO, Musick JA (2013) Field guide to fishes of the Chesapeake Bay. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Musick JA, Mercer LP (1977) Seasonal distribution of black sea bass, Centropristis striata, in the Mid-Atlantic Bight with comments on the ecology and fisheries of the species. Trans Am Fish Soc 106(1):12–25

    Google Scholar 

  • Ndbc.noaa.gov (2016) “NDBC - Station BFTN7 Recent Data”. N.p., 2016. Web. 11 Feb. 2016

  • Neill WH, Magnuson JJ, Chipman GG (1972) Behavioral thermoregulation by fishes: a new experimental approach. Science 176:1443–1445

    PubMed  CAS  Google Scholar 

  • Nguyen KDT, Morley SA, Lai CH, Clark MS, Tan KS, Bates AE, Peck LS (2011) Upper temperature limits of tropical marine ectotherms: global warming implications. PLoS ONE 6:e29340

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ospina AF, Mora C (2004) Effect of body size on reef fish tolerance to extreme low and high temperatures. Environ Biol Fish 70:339–343

    Google Scholar 

  • Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915

    PubMed  CAS  Google Scholar 

  • Petersen MF, Steffensen JF (2003) Preferred temperature of juvenile Atlantic cod Gadus morhua with different haemoglobin genotypes at normoxia and moderate hypoxia. J Exp Biol 206(2):359–364

    PubMed  CAS  Google Scholar 

  • Pimiento C, Nifong JC, Hunter ME, Monaco E, Silliman BR (2013) Habitat use patterns of the invasive red lionfish Pterois volitans: a comparison between mangrove and reef systems in San Salvador, Bahamas. Mar Ecol 36:28–37

    Google Scholar 

  • Pörtner HO, Peck MA (2010) Climate change effects on fishes and fisheries: towards a cause and effect understanding. J Fish Biol 77:1745–1779

    PubMed  Google Scholar 

  • Pörtner HO, Lucassen M, Storch D (2005) Metabolic biochemistry: its role in thermal tolerance and in the capacities of physiological and ecological function. Fish Physiol 22:79–154

    Google Scholar 

  • Pörtner HO, Karl DM, Boyd PW, Cheung WWL, Lluch-Cota SE, Nojiri Y, Schmidt DN, Zavialov PO (2014) Ocean systems. In: Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (eds) Climate change 2014: impacts, adaptation, and vulnerability. Part A: global and sectoral aspects. Contribution of working group II to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 411–484

    Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. http://www.R-project.org/

  • Reynolds WW, Casterlin ME (1979) Behavioral thermoregulation and the “final preferendum” paradigm. Am Zool 19:211–224

    Google Scholar 

  • Reynolds WW, Casterlin ME (1980) Thermoregulatory behavior of a tropical reef fish, Zebrasoma flavescens. Oikos 34:356–358

    Google Scholar 

  • 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 Change Biol 20:1055–1066

    Google Scholar 

  • Segnini DB, Chung KS, Ciurcina P (1993) Rate of adaptation to temperature change in Mugil curema (Pisces: Mugilidae) from Venezuela. Rev Biol Trop 41:59–62

    Google Scholar 

  • Sloan TJ, Turingan RG (2014) The effects of temperature on the feeding performance of invasive fishes. Am J Life Sci 2:63–71

    Google Scholar 

  • Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002) Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Proc Natl Acad Sci 99:15497–15500

    PubMed  PubMed Central  CAS  Google Scholar 

  • USGS-NAS (2015) U.S. Geological Survey Non-indigenous aquatic species database. Gainesville. http://nas.er.usgs.gov. Accessed on 30 Apr 2015

  • Van Dijk PLM, Tesch C, Hardewig I, Portner HO (1999) Physiological disturbances at critically high temperatures: a comparison between stenothermal Antarctic and eurythermal temperate eelpouts (Zoarcidae). J Exp Biol 202:3611–3621

    PubMed  Google Scholar 

  • Vinagre C, Leal I, Mendonça V, Flores AA (2015) Effect of warming rate on the critical thermal maxima of crabs, shrimp and fish. J Therm Biol 47:19–25

    PubMed  Google Scholar 

  • Ward TD, Algera DA, Gallagher AJ, Hawkins E, Horodysky A, Jørgensen C, Killen SS, McKenzie DJ, Metcalfe JD, Peck MA, Vu M, Cooke SJ (2016) Understanding the individual to implement the ecosystem approach to fisheries management. Conserv Physiol 4(1):5

    Google Scholar 

  • Whitfield PE, Gardner T, Vives SP, Gilligan MR, Courtenay WR, Ray GC, Hare JA (2002) Biological invasion of the Indo-Pacific lionfish Pterois volitans along the Atlantic coast of North America. Mar Ecol Prog Ser 235:289–297

    Google Scholar 

  • Whitfield PE, Muñoz RC, Buckel CA, Degan BP, Freshwater DW, Hare JA (2014) Native fish community structure and Indo-Pacific lionfish Pterois volitans densities along a depth-temperature gradient in Onslow Bay, North Carolina, USA. Mar Ecol Prog Ser 509:241–254

    Google Scholar 

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Acknowledgements

The authors thank those who assisted with the collection of specimens, including the Reef Environmental Education Foundation (REEF) and its volunteers, especially Carlos and Allison Estapé. The lionfish image used in Fig. 1 was obtained courtesy of the Integration and Application Network, University of Maryland Center for Environmental Science (ian.umces.edu/symbols/).

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Authors and Affiliations

  1. Halmos College of Natural Sciences and Oceanography, Nova Southeastern University, 8000 North Ocean Drive, Dania Beach, FL, 33004, USA

    B. D. Barker & D. W. Kerstetter

  2. Department of Marine and Environmental Science, Hampton University, 100 East Queen Street, Hampton, VA, 23668, USA

    A. Z. Horodysky

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  1. B. D. Barker
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  2. A. Z. Horodysky
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  3. D. W. Kerstetter
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Correspondence to D. W. Kerstetter.

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The authors declare that they have no conflict of interest. Partial funding for this research was provided by the NSU President’s Faculty Research and Development Grant program to DWK and AZH. AZH received support from the NOAA Living Marine Resources Cooperative Science Center and the NSF Educational Partnership in Climate Change and Sustainability.

Ethical approval

Experimentation with the lionfish, schoolmaster snapper, and graysby grouper was conducted in compliance with ethical standards and under the approval of the NSU IACUC program, which issued the approval Control # 038-398-12-0723 to DWK.

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Barker, B.D., Horodysky, A.Z. & Kerstetter, D.W. Hot or not? Comparative behavioral thermoregulation, critical temperature regimes, and thermal tolerances of the invasive lionfish Pterois sp. versus native western North Atlantic reef fishes. Biol Invasions 20, 45–58 (2018). https://doi.org/10.1007/s10530-017-1511-4

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