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Temperate predators and seasonal water temperatures impact feeding of a range expanding tropical fish

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Abstract

Range expansions of species due to climate change threaten the function and composition of marine ecosystems globally, yet factors constraining or facilitating this redistribution are poorly understood. Native predators may constrain prey shifting poleward through consumption, or by restricting their feeding activity. However, the extent that native predators impact range-expanders will likely be structured by physiological mismatches between these groups, associated with water temperatures. We examined how temperate predators and seasonal water temperature affected foraging of the planktivorous tropical reef fish, Abudefduf vaigiensis, within temperate southeastern Australian waters, an emerging new range. Foraging excursions of A. vaigiensis were compared between predator-rich marine reserves and predator-depauperate fished reefs during summer and winter (~18 and 22 °C water, respectively). A. vaigiensis foraged with shorter excursions in marine reserves than fished reefs and higher excursions during summer than winter. Effects of predation risk and water temperature on A. vaigiensis foraging were isolated in an aquarium experiment. Groups were held at 18 or 22 °C and visually exposed to a temperate predator, a predator control (temperate herbivore) and an empty tank. Foraging excursions and feeding rates were reduced when exposed to predators at 22 °C, but did not differ between predator and the predator control or empty tank at 18 °C. Results suggest temperate predators may restrict range expansions of A. vaigiensis by reducing its’ food intake during summer months. But winter water temperatures may limit feeding, independent of predation risk. Protection of predators from fishing should improve resistance of some marine ecosystems to impacts of range expanding prey.

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References

  • Allen G, Steene R, Humann P, DeLoach N (2003) Reef fish identification: tropical Pacific. New World Publications, Jacksonville

    Google Scholar 

  • Baltz DM, Moyle PB (1993) Invasion resistance to introduced species by a native assemblage of California stream fishes. Ecol Appl 3:246–255. doi:10.2307/1941827

    Article  Google Scholar 

  • Barrios-O’Neill D, Dick JTA, Emmerson MC, Ricciardi A, MacIsaac HJ, Alexander ME, Bovy HC (2014) Fortune favours the bold: a higher predator reduces the impact of a native but not an invasive intermediate predator. J Anim Ecol 83:693–701. doi:10.1111/1365-2656.12155

    Article  Google Scholar 

  • Bates AE, Barrett NS, Stuart-Smith RD, Holbrook NJ, Thompson PA, Edgar GJ (2013) Resilience and signatures of tropicalization in protected reef fish communities. Nat Clim Change 4:62–67. doi:10.1038/nclimate2062

    Article  Google Scholar 

  • Bates AE, Pecl GT, Frusher S, Hobday AJ, Wernberg T, Smale DA, Sunday JM, Hill NA, Dulvy NK, Colwell RK (2014) Defining and observing stages of climate-mediated range shifts in marine systems. Glob Environ Change 26:27–38. doi:10.1016/j.gloenvcha.2014.03.009

    Article  Google Scholar 

  • Beck HJ (2015) Tropical fish recruitment success varies among temperate reef habitats, potentially impacting their range expansion. Ph.D. dissertation, University of Technology Sydney, Sydney, Australia

  • Beck HJ, Feary DA, Figueira WF, Booth DJ (2014) Assessing range-shifts of tropical reef fishes: a comparison of belt transect and roaming underwater census methods. Bull Mar Sci 90:705–721. doi:10.5343/bms.2013.1055

    Article  Google Scholar 

  • Beck HJ, Feary DA, Nakamura Y, Booth DJ (2016) Wave-sheltered embayments are recruitment hotspots for tropical fishes on temperate reefs. Mar Ecol Prog Ser. doi:10.3354/meps11599

  • Biro PA, Booth DJ (2009) Extreme boldness precedes starvation mortality in six-lined trumpeter (Pelates sexlineatus). Hydrobiologia 635:395–398. doi:10.1007/s10750-009-9902-x

    Article  Google Scholar 

  • Blois JL, Zarnetske PL, Fitzpatrick MC, Finnegan S (2013) Climate change and the past, present, and future of biotic interactions. Science 341:499–504. doi:10.1126/science.1237184

    Article  CAS  Google Scholar 

  • Booth DJ, Beretta GA (2004) Influence of recruit condition on food competition and predation risk in a coral reef fish. Oecologia 140:289–294. doi:10.1007/s00442-004-1608-1

    Article  Google Scholar 

  • Booth DJ, Hixon MA (1999) Food ration and condition affect early survival of the coral reef damselfish, Stegastes partitus. Oecologia 121:364–368. doi:10.1007/s004420050940

    Article  Google Scholar 

  • Booth DJ, Figueira WF, Gregson MA, Brown L, Beretta G (2007) Occurrence of tropical fishes in temperate southeastern Australia: role of the East Australian Current. Estuar Coast Shelf Sci 72:102–114. doi:10.1016/j.ecss.2006.10.003

    Article  Google Scholar 

  • Brown JS, Kotler BP (2004) Hazardous duty pay and the foraging cost of predation. Ecol Lett 7:999–1014. doi:10.1111/j.1461-0248.2004.00661.x

    Article  Google Scholar 

  • Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67. doi:10.1038/nature11148

    Article  CAS  Google Scholar 

  • Carlsson NO, Sarnelle O, Strayer DL (2009) Native predators and exotic prey—an acquired taste? Front Ecol Environ 7:525–532. doi:10.1890/080093

    Article  Google Scholar 

  • Cheung WW, Lam VW, Sarmiento JL, Kearney K, Watson R, Zeller D, Pauly D (2010) Large-scale redistribution of maximum fisheries catch potential in the global ocean under climate change. Glob Change Biol 16:24–35. doi:10.1111/j.1365-2486.2009.01995.x

    Article  Google Scholar 

  • Davis AJ, Lawton JH, Shorrocks B, Jenkinson LS (1998) Individualistic species responses invalidate simple physiological models of community dynamics under global environmental change. J Anim Ecol 67:600–612. doi:10.1046/j.1365-2656.1998.00223.x

    Article  Google Scholar 

  • DeRivera CE, Ruiz GM, Hines AH, Jivoff P (2005) Biotic resistance to invasion: native predator limits abundance and distribution of an introduced crab. Ecology 86:3364–3376. doi:10.1890/05-0479

    Article  Google Scholar 

  • Dick JT, Alexander ME, Jeschke JM, Ricciardi A, MacIsaac HJ, Robinson TB, Kumschick S, Weyl OL, Dunn AM, Hatcher MJ (2014) Advancing impact prediction and hypothesis testing in invasion ecology using a comparative functional response approach. Biol Invasions 16:735–753. doi:10.1007/s10530-013-0550-8

    Article  Google Scholar 

  • Dill LM, Fraser AH (1984) Risk of predation and the feeding behavior of juvenile coho salmon (Oncorhynchus kisutch). Behav Ecol Sociobiol 16:65–71. doi:10.1007/BF00293105

    Article  Google Scholar 

  • Dill LM, Heithaus MR, Walters CJ (2003) Behaviorally mediated indirect interactions in marine communities and their conservation implications. Ecology 84:1151–1157. doi:10.1890/0012-9658(2003)084[1151:BMIIIM]2.0.CO;2

    Article  Google Scholar 

  • Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, Carpenter SR, Essington TE, Holt RD, Jackson JB (2011) Trophic downgrading of planet earth. Science 333:301–306. doi:10.1126/science.1205106

    Article  CAS  Google Scholar 

  • Feary DA, Pratchett MS, Emslie MJ, Fowler AM, Figueira WF, Luiz OJ, Nakamura Y, Booth DJ (2014) Latitudinal shifts in coral reef fishes: why some species do and others do not shift. Fish Fish 15:593–615. doi:10.1111/faf.12036

    Article  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. doi:10.1111/j.1365-2486.2009.01934.x

    Article  Google Scholar 

  • Figueira WF, Biro P, Booth DJ, Valenzuela VC (2009) Performance of tropical fish recruiting to temperate habitats: role of ambient temperature and implications of climate change. Mar Ecol Prog Ser 384:231–239. doi:10.3354/meps08057

    Article  Google Scholar 

  • Froese R, Pauly D (2014) Accessed Aug 2014. www.fishbase.org/

  • Gaylord B, Gaines SD (2000) Temperature or transport? Range limits in marine species mediated solely by flow. Am Nat 155:769–789. doi:10.1086/303357

    Article  Google Scholar 

  • Gill A (2003) The dynamics of prey choice in fish: the importance of prey size and satiation. J Fish Biol 63:105–116. doi:10.1111/j.1095-8649.2003.00214.x

    Article  Google Scholar 

  • Gilman SE, Urban MC, Tewksbury J, Gilchrist GW, Holt RD (2010) A framework for community interactions under climate change. Trends Ecol Evol 25:325–331. doi:10.1016/j.tree.2010.03.002

    Article  Google Scholar 

  • Grigaltchik VS, Ward AJ, Seebacher F (2012) Thermal acclimation of interactions: differential responses to temperature change alter predator–prey relationship. Proc R Soc Lond Ser B Biol Sci 279:4058–4064. doi:10.1098/rspb.2012.1277

    Article  Google Scholar 

  • Harley CD (2011) Climate change, keystone predation, and biodiversity loss. Science 334:1124–1127. doi:10.1126/science.1210199

    Article  CAS  Google Scholar 

  • Harley CD, Randall Hughes A, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241. doi:10.1111/j.1461-0248.2005.00871.x

    Article  Google Scholar 

  • Hellmann JJ, Prior KM, Pelini SL (2012) The influence of species interactions on geographic range change under climate change. Ann N Y Acad Sci 1249:18–28. doi:10.1111/j.1749-6632.2011.06410.x

    Article  Google Scholar 

  • HilleRisLambers J, Harsch MA, Ettinger AK, Ford KR, Theobald EJ (2013) How will biotic interactions influence climate change–induced range shifts? Ann N Y Acad Sci 1297:112–125. doi:10.1111/nyas.12182

    Google Scholar 

  • Holt RD, Barfield M (2009) Trophic interactions and range limits: the diverse roles of predation. Proc R Soc Lond Ser B Biol Sci 276:1435–1442. doi:10.1098/rspb.2008.1536

    Article  Google Scholar 

  • Johansen J, Bellwood D, Fulton C (2008) Coral reef fishes exploit flow refuges in high-flow habitats. Mar Ecol Prog Ser 360:219–226. doi:10.3354/meps07482

    Article  Google Scholar 

  • Jordan A, Davies P, Ingleton T, Foulsham E, Neilson J, Pritchard T (2010) Seabed habitat mapping of the continental shelf of NSW. Department of Environment, Climate Change and Water NSW, Sydney, Australia

  • Karplus I, Katzenstein R, Goren M (2006) Predator recognition and social facilitation of predator avoidance in coral reef fish Dasyllus marginatus juveniles. Mar Ecol Prog Ser 319:215–223. doi:10.3354/meps319215

    Article  Google Scholar 

  • Keith SA, Herbert RJ, Norton PA, Hawkins SJ, Newton AC (2011) Individualistic species limitations of climate-induced range expansions generated by meso-scale dispersal barriers. Divers Distrib 17:275–286. doi:10.1111/j.1472-4642.2010.00734.x

    Article  Google Scholar 

  • Kuiter RH (1993) Coastal fishes of south-eastern Australia. University of Hawaii Press, Honolulu

    Google Scholar 

  • Li G, Liu Y, Frelich LE, Sun S (2011) Experimental warming induces degradation of a Tibetan alpine meadow through trophic interactions. J Appl Ecol 48:659–667. doi:10.1111/j.1365-2664.2011.01965.x

    Article  Google Scholar 

  • Liancourt P, Spence LA, Song DS, Lkhagva A, Sharkhuu A, Boldgiv B, Helliker BR, Petraitis PS, Casper BB (2013) Plant response to climate change varies with topography, interactions with neighbors, and ecotype. Ecology 94:444–453. doi:10.1890/12-0780.1

    Article  Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640. doi:10.1139/z90-092

    Article  Google Scholar 

  • Ling SD, Johnson CR (2012) Marine reserves reduce risk of climate-driven phase shift by reinstating size-and habitat-specific trophic interactions. Ecol Appl 22:1232–1245. doi:10.1890/11-1587.1

    Article  CAS  Google Scholar 

  • Ling SD, Johnson CR, Frusher SD, Ridgway KR (2009) Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift. Proc Natl Acad Sci USA 106:22341–22345. doi:10.1073/pnas.0907529106

    Article  CAS  Google Scholar 

  • Luiz OJ, Allen AP, Robertson DR, Floeter SR, Kulbicki M, Vigliola L, Becheler R, Madin JS (2013) Adult and larval traits as determinants of geographic range size among tropical reef fishes. Proc Natl Acad Sci USA 110:16498–16502. doi:10.1073/pnas.1304074110

    Article  CAS  Google Scholar 

  • Mackas DL, Denman KL, Abbott MR (1985) Plankton patchiness: biology in the physical vernacular. Bull Mar Sci 37:652–674

    Google Scholar 

  • Madin EMP, Gaines SD, Warner RR (2010) Field evidence for pervasive indirect effects of fishing on prey foraging behavior. Ecology 91:3563–3571. doi:10.1890/09-2174.1

    Article  Google Scholar 

  • Madin EMP, Ban NC, Doubleday ZA, Holmes TH, Pecl GT, Smith F (2011) Socio-economic and management implications of range-shifting species in marine systems. Glob Environ Change 22:137–146. doi:10.1016/j.gloenvcha.2011.10.008

    Article  Google Scholar 

  • Matassa CM, Trussell GC (2015) Effects of predation risk across a latitudinal temperature gradient. Oecologia 177:775–784. doi:10.1007/s00442-014-3156-7

    Article  Google Scholar 

  • McCormick MI, Holmes TH (2006) Prey experience of predation influences mortality rates at settlement in a coral reef fish, Pomacentrus amboinensis. J Fish Biol 68:969–974. doi:10.1111/j.0022-1112.2006.00982.x

    Article  Google Scholar 

  • Milazzo M, Mirto S, Domenici P, Gristina M (2013) Climate change exacerbates interspecific interactions in sympatric coastal fishes. J Anim Ecol 82:468–477. doi:10.1111/j.1365-2656.2012.02034.x

    Article  Google Scholar 

  • Nagelkerken I, Simpson S (2013) Who’s hot and who’s not: ocean warming alters species dominance through competitive displacement. J Anim Ecol 82:287–289. doi:10.1111/1365-2656.12053

    Article  Google Scholar 

  • Nakamura Y, Feary DA, Kanda M, Yamaoka K (2013) Tropical fishes dominate temperate reef fish communities within western Japan. PLoS One 8:e81107. doi:10.1371/journal.pone.0081107

    Article  Google Scholar 

  • O’Gorman EJ (2014) Integrating comparative functional response experiments into global change research. J Anim Ecol 83:525–527. doi:10.1111/1365-2656.12216

    Article  Google Scholar 

  • Olyarnik SV, Bracken ME, Byrnes JE, Hughes AR, Hultgren KM, Stachowicz JJ (2009) Ecological factors affecting community invasibility. In: Rilov G, Crooks J (eds) Biological invasions in marine ecosystems. Springer, Heidelberg, pp 215–238

    Chapter  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669. doi:10.1146/annurev.ecolsys.37.091305.110100

    Article  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. doi:10.1038/nature01286

    Article  CAS  Google Scholar 

  • Pinsky ML, Worm B, Fogarty MJ, Sarmiento JL, Levin SA (2013) Marine taxa track local climate velocities. Science 341:1239–1242. doi:10.1126/science.1239352

    Article  CAS  Google Scholar 

  • Poloczanska ES, Brown CJ, Sydeman WJ, Kiessling W, Schoeman DS, Moore PJ, Brander K, Bruno JF, Buckley LB, Burrows MT (2013) Global imprint of climate change on marine life. Nat Clim Change 3:919–925. doi:10.1038/nclimate1958

    Article  Google Scholar 

  • Pörtner H (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146. doi:10.1007/s001140100216

    Article  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. doi:10.1111/j.1095-8649.2010.02783.x

    Article  Google Scholar 

  • Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–509. doi:10.1890/04-0719

    Article  Google Scholar 

  • Rijnsdorp AD, Peck MA, Engelhard GH, Möllmann C, Pinnegar JK (2009) Resolving the effect of climate change on fish populations. ICES J Mar Sci 66:1570–1583. doi:10.1093/icesjms/fsp056

    Article  Google Scholar 

  • Risk MJ (1972) Fish diversity on a coral reef in the Virgin Islands. Atoll Res Bull 153:1–6. doi:10.5479/si.00775630.153.1

    Article  Google Scholar 

  • Schmitz OJ, Beckerman AP, O’Brien KM (1997) Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388–1399. doi:10.1890/0012-9658(1997)078[1388:BMTCEO]2.0.CO;2

    Article  Google Scholar 

  • Short AD, Trenaman N (1992) Wave climate of the Sydney region, an energetic and highly variable ocean wave regime. Mar Freshw Res 43:765–791. doi:10.1071/MF9920765

    Article  Google Scholar 

  • Sorte CJ, Williams SL, Carlton JT (2010) Marine range shifts and species introductions: comparative spread rates and community impacts. Glob Ecol Biogeogr 19:303–316. doi:10.1111/j.1466-8238.2009.00519.x

    Article  Google Scholar 

  • Stallings CD (2008) Indirect effects of an exploited predator on recruitment of coral-reef fishes. Ecology 89:2090–2095. doi:10.1890/07-1671.1

    Article  Google Scholar 

  • Thompson P, Baird M, Ingleton T, Doblin M (2009) Long-term changes in temperate Australian coastal waters: implications for phytoplankton. Mar Ecol Prog Ser 394:1–19. doi:10.3354/meps08297

    Article  CAS  Google Scholar 

  • Trussell GC, Ewanchuk PJ, Matassa CM (2006a) The fear of being eaten reduces energy transfer in a simple food chain. Ecology 87:2979–2984. doi:10.1890/0012-9658(2006)87[2979:TFOBER]2.0.CO;2

    Article  Google Scholar 

  • Trussell GC, Ewanchuk PJ, Matassa CM (2006b) Habitat effects on the relative importance of trait-and density-mediated indirect interactions. Ecol Lett 9:1245–1252. doi:10.1111/j.1461-0248.2006.00981.x

    Article  Google Scholar 

  • Underwood AJ, Kingsford MJ, Andrew NL (1991) Patterns in shallow subtidal marine assemblages along the coast of New South Wales. Aust J Ecol 16:231–249. doi:10.1111/j.1442-9993.1991.tb01050.x

    Article  Google Scholar 

  • Vergés A, Steinberg PD, Hay ME, Poore AG, Campbell AH, Ballesteros E, Heck KL, Booth DJ, Coleman MA, Feary DA (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc R Soc Lond Ser B Biol Sci 281:20140846. doi:10.1098/rspb.2014.0846

    Article  Google Scholar 

  • Wenger AS, Johansen JL, Jones GP (2012) Increasing suspended sediment reduces foraging, growth and condition of a planktivorous damselfish. J Exp Mar Biol Ecol 428:43–48. doi:10.1016/j.jembe.2012.06.004

    Article  Google Scholar 

  • Yang H, Wu M, Liu W, Zhang Z, Zhang N, Wan S (2011) Community structure and composition in response to climate change in a temperate steppe. Glob Change Biol 17:452–465. doi:10.1111/j.1365-2486.2010.02253.x

    Article  Google Scholar 

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Acknowledgments

HJB gratefully acknowledges funding from the Sydney Institute of Marine Science (SIMS) Doctoral Fellowship Program and the University of Technology, Sydney. DAF was funded by the University of Technology, Sydney, under the Chancellors Postdoctoral Fellowship scheme. EMPM was funded by the US National Science Foundation’s International Research Fellowship Program. We thank J. Donelson for helpful comments on the manuscript. All applicable institutional and/or national guidelines for the care and use of animals were followed. Animal ethics approval for the research was granted by the University of Technology Sydney (UTS) Animal Care and Ethics Committee (ACEC) (Permit 2011-036A). This is contribution 172 of the Sydney Institute of Marine Sciences.

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  1. School of Life Sciences, University of Technology Sydney, Broadway, Sydney, NSW, 2007, Australia

    Hayden J. Beck, David A. Feary, Ashley M. Fowler & David J. Booth

  2. Department of Biological Sciences, Macquarie University, North Ryde, Sydney, NSW, 2109, Australia

    Elizabeth M. P. Madin

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  1. Hayden J. Beck
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Beck, H.J., Feary, D.A., Fowler, A.M. et al. Temperate predators and seasonal water temperatures impact feeding of a range expanding tropical fish. Mar Biol 163, 70 (2016). https://doi.org/10.1007/s00227-016-2844-8

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