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Thermal environment and nutritional condition affect the efficacy of chemical alarm cues produced by prey fish

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Abstract

A wide variety of prey animals possess damage-released chemical alarm cues that evoke antipredator responses in both conspecifics and some heterospecifics. Several studies have indicated that food availability may influence body condition and in doing so, affect the production of alarm cues. We examined whether food availability (high and low) and temperature (27, 30 and 32 °C) interacted to affect the production of chemical alarm cues by juveniles of a marine tropical prey fish, Pomacentrus moluccensis. Results indicate that poorly-fed fish had depleted energy reserves with rising temperatures compared to well-fed fish. Fish with a poor feeding history also showed depressed growth rate across all temperature treatments. The alarm cues produced by experimental fish triggered stronger antipredator responses as temperature increased up to 30 °C, regardless of the feeding history or body condition of the donor. However, at 32 °C, alarm cues from poorly-fed fish did not elicit as effectively an antipredator response in conspecifics compared to those produced by well-fed fish. The results highlight that warming oceans, in isolation but also in conjunction with changes in food supply, may have a drastic impact on chemically-mediated predator-prey interactions.

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References

  • Arendt J, Hoang L (2005) Effect of food level and rearing temperature on burst speed and muscle composition of western spadefoot toad (Spea hammondii). Funct Ecol 19(6):982–987

    Article  Google Scholar 

  • Blom S, Andersson TB, Förlin L (2000) Effects of food deprivation and handling stress on head kidney 17α hydroxyprogesterone 21-hydroxylase activity, plasma cortisol and the activities of liver detoxification enzymes in rainbow trout. Aquat Toxicol 48(2):265–274

    Article  CAS  PubMed  Google Scholar 

  • Booth DJ, Beretta GA (2002) Changes in a fish assemblage after a coral bleaching event. Mar Ecol Prog Ser 245:205–212

    Article  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(1):99–113

    Article  Google Scholar 

  • Brown GE, Chivers DP, Smith RJF (1995) Fathead minnows avoid conspecific and heterospecific alarm pheromones in the feces of northern pike. J Fish Biol 47(3):387–393

    Google Scholar 

  • Brown GE, Foam PE, Cowell HE, Guevara-Fiore P, Chivers DP (2004) Production of chemical alarm cues in convict cichlids: the effects of diet, body condition and ontogeny. Ann Zool Fenn 41(3):487–499

    Google Scholar 

  • Carreau-Green ND, Mirza RS, Martinez ML, Pyle GG (2008) The ontogeny of chemically mediated antipredator responses of fathead minnows Pimephales promelas. J Fish Biol 73(10):2390–2401

    Article  Google Scholar 

  • Caruso G, Maricchiolo G, Micale V, Genovese L, Caruso R, Denaro MG (2010) Physiological responses to starvation in the European eel (Anguilla anguilla): effects on haematological, biochemical, non-specific immune parameters and skin structures. Fish Physiol Biochem 36(1):71–83

    Article  CAS  PubMed  Google Scholar 

  • Chivers DP, Smith RJF (1998) Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Ecoscience 5(3):338–352

    Google Scholar 

  • Chivers DP et al. (2007a) Epidermal 'alarm substance' cells of fishes maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation. Proc R Soc B 274(1625):2611–2619

    Article  PubMed  PubMed Central  Google Scholar 

  • Chivers DP, Zhao XX, Ferrari MCO (2007b) Linking morphological and behavioural defences: prey fish detect the morphology of conspecifics in the odour signature of their predators. Ethology 113(8):733–739

    Article  Google Scholar 

  • Chivers DP, Zhao XX, Brown GE, Marchant TA, Ferrari MCO (2008) Predator-induced changes in morphology of a prey fish: the effects of food level and temporal frequency of predation risk. Evol Ecol 22(4):561–574

    Article  Google Scholar 

  • Chivers DP, Dixson DL, White JR, McCormick MI, Ferrari MCO (2013) Degradation of chemical alarm cues and assessment of risk throughout the day. Ecol Evol 3(11):3925–3934

    Article  PubMed  PubMed Central  Google Scholar 

  • Clarke A, Fraser KPP (2004) Why does metabolism scale with temperature? Funct Ecol 18(2):243–251

    Article  Google Scholar 

  • Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68(5):893–905

    Article  Google Scholar 

  • Courtney Jones SK, Munn AJ, Penman TD, Byrne PG (2015) Long-term changes in food availability mediate the effects of temperature on growth, development and survival in striped marsh frog larvae: implications for captive breeding programmes. Contemp Phys 3(1):cov029

    Google Scholar 

  • Donelson JM, Munday PL, McCormick MI, Pankhurst NW, Pankhurst PM (2010) Effects of elevated water temperature and food availability on the reproductive performance of a coral reef fish. Mar Ecol Prog Ser 401:233–243

    Article  Google Scholar 

  • Englund G, Ohlund G, Hein CL, Diehl S (2011) Temperature dependence of the functional response. Ecol Lett 14(9):914–921

    Article  PubMed  Google Scholar 

  • Ferrari MCO, Wisenden BD, Chivers DP (2010) Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88(7):698–724

    Article  Google Scholar 

  • Green BS, Fisher R (2004) Temperature influences swimming speed, growth and larval duration in coral reef fish larvae. J Exp Mar Biol Ecol 299(1):115–132

    Article  Google Scholar 

  • Green BS, McCormick MI (1999) Influence of larval feeding history on the body condition of Amphiprion melanopus. J Fish Biol 55(6):1273–1289

    Article  Google Scholar 

  • Halbgewachs CF, Marchant TA, Kusch RC, Chivers DP (2009) Epidermal club cells and the innate immune system of minnows. Biol J Linn Soc 98(4):891–897

    Article  Google Scholar 

  • Handeland SO, Imsland AK, Stefansson SO (2008) The effect of temperature and fish size on growth, feed intake, food conversion efficiency and stomach evacuation rate of Atlantic salmon post-smolts. Aquaculture 283(1–4):36–42

    Article  Google Scholar 

  • Hayes MB, Jiao L, Tsao TH, King I, Jennings M, Hou C (2014) High temperature slows down growth in tobacco hornworms (Manduca sexta larvae) under food restriction. Instr Sci 22(3):424–430

    Google Scholar 

  • Hoey J, McCormick MI, Hoey AS (2007) Influence of depth on sex-specific energy allocation patterns in a tropical reef fish. Coral Reefs 26(3):603–613

    Article  Google Scholar 

  • IPCC (2013): Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Stocker, T.F., D. Qin, G.-K. Plattner, M. Tignor, S.K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex and P.M. Midgley (eds.)]. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, 1535 pp,

  • James CT, Wisenden BD, Goater CP (2009) Epidermal club cells do not protect fathead minnows against trematode cercariae: a test of the anti-parasite hypothesis. Biol J Linn Soc 98(4):884–890

    Article  Google Scholar 

  • Jimenez IM, Kuhl M, Larkum AWD, Ralph PJ (2011) Effects of flow and colony morphology on the thermal boundary layer of corals. J R Soc Interface 8(65):1785–1795

    Article  PubMed  PubMed Central  Google Scholar 

  • Jobling M (1997) Temperature and growth: modulation of growth rate via temperature change. In: Wood CM, McDonald DG (eds) Global warming: implications for freshwater and marine fish. Cambridge University Press, Cambridge, pp. 225–253

    Chapter  Google Scholar 

  • Larson JK, McCormick MI (2005) The role of chemical alarm signals in facilitating learned recognition of novel chemical cues in a coral reef fish. Anim Behav 69:51–57

    Article  Google Scholar 

  • Lienart G, Mitchell M, Ferrari M, McCormick M (2014) Temperature and food availability affect risk assessment in an ectotherm. Anim Behav 89:199–120

    Article  Google Scholar 

  • Lönnstedt OM, McCormick MI (2011a) Chemical alarm cues inform prey of predation threat: the importance of ontogeny and concentration in a coral reef fish. Anim Behav 82(2):213–218

    Article  Google Scholar 

  • Lönnstedt OM, McCormick MI (2011b) Growth history and intrinsic factors influence risk assessment at a critical life transition for a fish. Coral Reefs 30(3):805–812

    Article  Google Scholar 

  • Lönnstedt OM, McCormick MI (2015) Damsel in distress: captured damselfish prey emit chemical cues that attract secondary predators and improve escape chances. Proc R Soc B 282(1818):20152038

    Article  PubMed  Google Scholar 

  • Lönnstedt OM, McCormick MI, Chivers DP (2013) Predator-induced changes in the growth of eyes and false eyespots. Sci Rep 3:2259

    Article  PubMed  PubMed Central  Google Scholar 

  • Lough J (2007) Climate and climate change on the great barrier reef. In: Johnson JE, Marshall PA (eds) Climate change and the great barrier reef: a vulnerability assessment. Great Barrier Reef Marine Park Authority, Townsville, pp. 15–50

    Google Scholar 

  • Manek AK, Ferrari MCO, Sereda JM, Niyogi S, Chivers DP (2012) The effects of ultraviolet radiation on a freshwater prey fish: physiological stress response, club cell investment, and alarm cue production. Biol J Linn Soc 105(4):832–841

    Article  Google Scholar 

  • Manek AK, Ferrari MCO, Pollock RJ, Vicente D, Weber LP, Chivers DP (2013) Within and between population variation in epidermal club cell investment in a freshwater prey fish: a cautionary tale for evolutionary ecologists. PLoS One 8(3):e56689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manek AK, Ferrari MCO, Niyogi S, Chivers DP (2014) The interactive effects of multiple stressors on physiological stress responses and club cell investment in fathead minnows. Sci Total Environ 476-477:90–97

    Article  CAS  PubMed  Google Scholar 

  • McCabe RM, Estrade P, Middleton JH, Melville WK, Roughan M, Lenain L (2010) Temperature variability in a shallow, tidally isolated coral reef lagoon. J Geophys Res-Oceans 115:1–17

    Google Scholar 

  • McCormick MI, Larson JK (2007) Field verification of the use of chemical alarm cues in a coral reef fish. Coral Reefs 26(3):571–576

    Article  Google Scholar 

  • McCormick MI, Larson JK (2008) Effect of hunger on the response to, and the production of, chemical alarm cues in a coral reef fish. Anim Behav 75(6):1973–1980

    Article  Google Scholar 

  • McLeod IM et al. (2013) Climate change and the performance of larval coral reef fishes: the interaction between temperature and food availability. Contemp Phys 1:1–12

    Google Scholar 

  • McLeod IM, Jones RE, Jones GP, Takahashi M, McCormick MI (2015) Interannual variation in the larval development of a coral reef fish in response to temperature and associated environmental factors. Mar Biol 162:2379–2389

    Article  Google Scholar 

  • Mirza RS, Chivers DP (2000) Predator-recognition training enhances survival of brook trout: evidence from laboratory and field-enclosure studies. Can J Zool 78(12):2198–2208

    Article  Google Scholar 

  • Mirza RS, Chivers DP (2002) Brook charr (Salvelinus fontinalis) can differentiate chemical alarm cues produced by different age/size classes of conspecifics. J Chem Ecol 28(3):555–564

    Article  CAS  PubMed  Google Scholar 

  • Mirza RS, Chivers DP (2003) Fathead minnows learn to recognize heterospecific alarm cues they detect in the diet of a known predator. Behaviour 140:1359–1369

    Article  Google Scholar 

  • Mitchell MD, McCormick MI (2013) Ontogenetic differences in chemical alarm cue production determine antipredator responses and learned predator recognition. Behav Ecol Sociobiol 67(7):1123–1129

    Article  Google Scholar 

  • Mitchell MD, Cowman PF, McCormick MI (2012) Chemical alarm cues are conserved within the coral reef fish family Pomacentridae. PLoS One 7(10):e47428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okamoto DK, Schmitt RJ, Holbrook SJ, Reed DC (2012) Fluctuations in food supply drive recruitment variation in a marine fish. Proc R Soc B 279(1747):4542–4550

    Article  PubMed  PubMed Central  Google Scholar 

  • Pfeiffer W (1977) The distribution of fright reaction and alarm substance cells in fishes. Copeia 1977(4):653–665

    Article  Google Scholar 

  • Roessig JM, Woodley CM, Cech JJ, Hansen LJ (2004) Effects of global climate change on marine and estuarine fishes and fisheries. Rev Fish Biol Fish 14(2):251–275

    Article  Google Scholar 

  • Roh E, Mirza RS, Brown GE (2004) Quality or quantity? The role of donor condition in the production of chemical alarm cues in juvenile convict cichlids. Behaviour 141:1235–1248

    Article  Google Scholar 

  • Rummer JL et al. (2014) Life on the edge: thermal optima for aerobic scope of equatorial reef fishes are close to current day temperatures. Glob Chang Biol 20(4):1055–1066

    Article  PubMed  Google Scholar 

  • Smith JJ, Leduc AOHC, Brown GE (2008) Chemically mediated learning in juvenile rainbow trout. Does predator odour pH influence intensity and retention of acquired predator recognition? J Fish Biol 72(7):1750–1760

    Article  Google Scholar 

  • Stabell OB, Vegusdal A (2010) Socializing makes thick-skinned individuals: on the density of epidermal alarm substance cells in cyprinid fish, the crucian carp (Carassius carassius). J Comp Physiol A 196(9):639–647

    Article  Google Scholar 

  • Storch V, Juario JV (1983) The effect of starvation and subsequent feeding on the hepatocytes of Chanos chanos (Forsskal) fingerlings and fry. J Fish Biol 23(1):95–103

    Article  Google Scholar 

  • Wisenden BD, Smith RJF (1997) The effect of physical condition and shoalmate familiarity on proliferation of alarm substance cells in the epidermis of fathead minnows. J Fish Biol 50(4):799–808

    Article  Google Scholar 

  • Wisenden BD, Smith RJF (1998) A re-evaluation of the effect of shoalmate familiarity on the proliferation of alarm substance cells in ostariophysan fishes. J Fish Biol 53(4):841–846

    Article  Google Scholar 

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Acknowledgments

We thank Anne Hoggett and Lyle Vail of the Lizard Island Research Station for their logistic support and Miwa Takahashi and Lucy Holmes for field assistance. Funding was provided by a James Cook University grant, the ARC and ARC Centre of Excellence for Coral Reef Studies. This study was conduction in in accordance with James Cook University Animal Ethics; permit no. A2005 and A2080.

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  1. ARC Centre of Excellence for Coral Reef Studies, and College of Marine and Environmental Sciences, James Cook University, QLD, Townsville, Australia

    Govinda D. H. Lienart & Mark I. McCormick

  2. Department of Biomedical Sciences, WCVM, University of` Saskatchewan, Saskatoon, Canada

    Maud C. O. Ferrari

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  1. Govinda D. H. Lienart
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Correspondence to Govinda D. H. Lienart.

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Lienart, G.D.H., Ferrari, M.C.O. & McCormick, M.I. Thermal environment and nutritional condition affect the efficacy of chemical alarm cues produced by prey fish. Environ Biol Fish 99, 729–739 (2016). https://doi.org/10.1007/s10641-016-0516-7

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