Abstract
Assessment of predation risk is vital for the success of an individual. Primary cues for the assessment include visual and olfactory stimuli, but the relative importance of these sources of information for risk assessment has seldom been assessed for marine fishes. This study examined the importance of visual and chemical cues in assessing risk for the star goby, Asterropteryx semipunctatus. Visual and chemical cue intensities were used that were indicative of a high threat situation. The behavioural response elicited by both the visual cues of a predator (the rock cod, Cephalopholis boenak) and the chemical alarm cues from conspecifics were similar in magnitude, with responses including a decrease in feeding strikes and moves. A bobbing behaviour was exhibited when the predator was visible and not when only exposed to the chemical alarm cue. When visual and chemical cues were presented together they yielded a stronger antipredator response than when gobies were exposed solely to conspecific alarm cues. This suggests additivity of risk assessment information at the levels of threat used, however, the goby’s response is also likely to depend on the environmental and social context of the predator–prey encounter. This study highlights the importance of chemical cues in the assessment of predation risk for a coral reef fish.
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References
Amo L, López P, Martín J (2006) Can wall lizards combine chemical and visual cues to discriminate predatory from non-predatory snakes inside refuges? Ethology 112:478–484
Beukers-Stewart BD, Jones GP (2004) The influence of prey abundance on the feeding ecology of two piscivorous species of coral reef fish. J Exp Mar Biol Ecol 299:155–184
Brown GE (2003) Learning about danger: chemical alarm cues and local risk assessment in prey fishes. Fish Fish 4:227–234
Brown GE, Magnavacca G (2003) Predator inspection behaviour in a characin fish: an interaction between chemical and visual information? Ethology 109:739–750
Brown GE, Chivers DP (2006) Learning about danger: chemical alarm cues and predation risk assessment in fishes. In: Brown C, Laland K, Krause J (eds) Fish cognition and behaviour. Blackwell Science, Oxford, pp 49–69
Brown GE, Chivers DP, Smith RJF (1995) Fathead minnows avoid conspecific and heterospecific alarm pheromones in the faeces of northern pike. J Fish Biol 47:387–393
Brown GE, Adrian JC, Patton T, Chivers DP (2001) Fathead minnows learn to recognize predator odour when exposed to concentrations of artificial alarm pheromone below their behavioural-response threshold. Can J Zool 79:2239–2245
Brown GE, Gershaneck DL, Plata DL, Golub JL (2002) Ontogenetic changes in response to heterospecific alarm cues by juvenile largemouth bass are phenotypically plastic. Behaviour 139:913–927
Chivers DP, Smith RJF (1998) Chemical alarm signaling in aquatic predator–prey systems: a review and prospectus. Ecoscience 5:315–321
Chivers DP, Brown GE, Smith RJF (1996) The evolution of chemical alarm signals: attracting predators benefits alarm signal senders. Am Nat 148:649–659
Chivers DP, Mirza RS, Bryer PJ, Kiesecker JM (2001) Threat-sensitive predator avoidance by slimy sculpins: understanding the importance of visual versus chemical information. Can J Zool 79:867–873
Chivers DP, Mirza RS, Johnston JG (2002) Learned recognition of heterospecific alarm cues enhances survival during encounters with predators. Behaviour 139:929–938
Dugatkin LA, Godin J-GJ (1992) Predator inspection, shoaling and foraging under predation hazard in the Trinidadian guppy, Poecilia reticulata. Environ Biol Fish 34:265–276
Dupuch A, Magnan P, Dill LM (2004) Sensitivity of northern redbelly dace, Phoxinus eos, to chemical alarm cues. Can J Zool 82:407–415
Engstrom-Ost J, Lehtiniemi M (2004) Threat-sensitive predator avoidance by pike larvae. J Fish Biol 65:251–261
Ferrari MC, Messier O, Chivers DP (2006) The nose knows: minnows determine predator proximity and density through detection of predator odours. Anim Behav 72:927–932
Golub JL, Brown GE (2003) Are all signals the same? Ontogenetic change in the response to conspecific and heterospecific chemical alarm signals by juvenile green sunfish (Lepomis cyanellus). Behav Ecol Sociobiol 54:113–118
Hartman EJ, Abrahams MV (2000) Sensory compensation and the detection of predators: the interaction between chemical and visual information. Proc R Soc Lond B 267:571–575
Helfman GS (1989) Threat-sensitive predator avoidance in damselfish–trumpetfish interactions. Behav Ecol Sociobiol 24:47–58
Helfman GS, Collette BB, Facey DE (1997) The diversity of fishes. Blackwell Science, Massachusetts
Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394
Keppel G (1982) Design and analysis: a researcher’s handbook. Prentice-Hall, Englewood Cliffs
Kiesecker JM, Chivers DP, Blaustein AR (1996) The use of chemical cues in predator recognition by western toad tadpoles. Anim Behav 52:1237–1245
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
Licht T (1989) Discrimination between hungry and satiated predators: the response of guppies (Poecilia reticulata) from high and low predation sites. Ethology 87:238–243
Lima SL, Dill LM (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640
Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659
Losey GS, McFarland WN, Loew ER, Zamzow JP, Nelson PA, Marshall NJ (2003) Visual biology of Hawaiian coral reef fishes: I. Ocular transmission and visual pigments. Copeia 2003:433–454
Marshall NJ, Jennings K, McFarland WN, Loew ER, Losey GS (2003) Visual biology of Hawaiian coral reef fishes: III. Environmental light and an integrated approach to the ecology of reef fish vision. Copeia 2003:467–480
Mathis A, Smith RJF (1993) Chemical alarm signals increase the survival time of fathead minnows (Pimephales promelas) during encounters with northern pike (Esox lucius). Behav Ecol 4:260–265
Mathis A, Vincent F (2000) Differential use of visual and chemical cues in predator recognition and threat-sensitive predator-avoidance responses by larval newts (Notophthalmus viridescens). Can J Zool 78:1646–1652
McCormick MI (1994) Comparison of field methods for measuring surface topography and their associations with a tropical reef fish assemblage. Mar Ecol Prog Ser 112:87–96
McCormick MI, Larson JK (2007) Field verification of the use of chemical alarm cues in a coral reef fish. Coral Reefs. doi:10.1007/s00338-007-0221-2
Mirza R, Chivers D (2000) Predator-recognition training enhances survival of brook trout: evidence from laboratory and field-enclosure studies. Can J Zool 78:2198–2208
Mirza RS, Chivers DP (2001a) Do chemical alarm signals enhance survival in aquatic vertebrates? An analysis of the current research paradigm. In: Marchlewska-Koj A, Lepri JJ, Müller-Schwarze D (eds) Chemical signals in vertebrates, vol 9. Plenum Press, New York, pp 19–26
Mirza RS, Chivers DP (2001b) Are alarm cues conserved within salmonid fishes. J Chem Ecol 27:1641–1655
Mirza RS, Scott JJ, Chivers DP (2001) Differential responses of male and female red swordtails to chemical alarm cues. J Fish Biol 59:716–728
Murphy KE, Pitcher TJ (1997) Predator attack motivation influences the inspection behaviour of European minnows. J Fish Biol 50:407–417
Olivotto I, Mosconi G, Maradonna F, Cardinali M, Carnevali O (2002) Diplodus sargus interrenal-pituitary response: chemical communication in stressed fish. Gen Comp Endocrinol 127:66–70
Pollock MS, Chivers DP (2004) The effects of density on the learned recognition of heterospecific alarm cues. Ethology 110:341–249
Randall DJ, Allen GR, Steene RC (1990) Fishes of the great barrier reef and coral sea. Crawford House Press, Bathurst
Shohet AJ, Watt PJ (2004) Female association preferences based on olfactory cues in the guppy, Poecilia reticulata. Behav Ecol Sociobiol 55:363–369
Sih A (1980) Optimal behavior: can foragers balance two conflicting demands? Science 210:1041–1043
Smith RJF (1989) The response of Asterropteryx semipunctatus and Gnatholepis anjerensis (Pisces: Gobiidae) to chemical stimuli from injured conspecifics, an alarm response in gobies. Ethology 81:279–290
Smith RJF (1997) Avoiding and deterring predators. In: Godin JJ (ed) Behavioural ecology of teleost fishes. Oxford University Press, New York, pp 163–190
Smith ME (2000) Alarm response of Arius felis to chemical stimuli from injured conspecifics. J Chem Ecol 26:1635–1647
Smith RJF, Smith MJ (1989) Predator recognition behaviour in two species of gobiid fishes, Asterropteryx semipunctatus and Gnatholepis anjerensis. Ethology 83:19–30
Smith RJF, Lawrence BJ (1992) The response of a bumblebee goby, Brachygobius sabanus, to chemical stimuli from injured conspecifics. Environ Biol Fish 34:103–108
Smith ME, Belk MC (2001) Risk assessment in western mosquitofish (Gambusia affinis): do multiple cues have additive effects? Behav Ecol Sociobiol 51:101–107
Smith RJF, Lawrence BJ, Smith MJ (1991) Cross-reaction to skin extract between two gobies, Asterropteryx semipunctatus and Brachygobius sabanus. J Chem Ecol 17:2253–2259
Stauffer HP, Semlitsch RD (1993) Effects of visual, chemical and tactile cues of fish on the behavioural responses of tadpoles. Anim Behav 46:255–364
Sweatman HPA (1984) A field study of the predatory behaviour and feeding rate of a piscivorous coral reef fish, the lizardfish Synodus englemani. Copeia 1984:187–194
Tremaine RJ, Pollock MS, Friesen RG, Kusch RC, Chivers DP (2006) The response of prey fishes to chemical alarm cues: what recent field experiments reveal about the old testing paradigm. In: Mason RT, LeMaster MP, Müller-Schwarze D (eds) Chemical signals in vertebrates, vol 10. Plenum Press, New York, pp 328–333
Turner AM, Montgomery SL (2003) Spatial and temporal scales of predator avoidance: experiments with fish and snails. Ecology 84:616–622
Wisenden BD (2000) Olfactory assessment of predation risk in the aquatic environment. Philos Trans R Soc Lond B 355:1205–1208
Wisenden BD, Chivers DP, Brown GE, Smith RJF (1995) The role of experience in risk assessment: avoidance of areas chemically labelled with fathead minnow alarm pheromone by conspecifics and heterospecifics. Ecoscience 2:116–122
Zhao X, Chivers DP (2005) Response of juvenile goldfish (Carassius auratus) to chemical alarm cues: relationship between response intensity, response duration and the level of predation risk. In: Mason RT, LeMaster M, Müller-Schwarze D (eds) Chemical signals in vertebrates, vol 10. Plenum Press, New York, pp 334–341
Zhao X, Ferrar MCO, Chivers DP (2006) Threat-sensitive learning of predator odours by a prey fish. Behaviour 143:1103–1121
Acknowledgments
We thank K. Clifton for his help in the field, J. Larson for assistance in the laboratory and three anonymous reviewers for their insightful comments. This study was funded through the ARC Centre of Excellence for Coral Reef Studies. This study conformed to the ethics approval guidelines of JCU and operated under approval A1067.
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McCormick, M.I., Manassa, R. Predation risk assessment by olfactory and visual cues in a coral reef fish. Coral Reefs 27, 105–113 (2008). https://doi.org/10.1007/s00338-007-0296-9
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DOI: https://doi.org/10.1007/s00338-007-0296-9
Keywords
- Behaviour
- Chemical alarm cue
- Coral reef fish
- Olfaction
- Predation risk
- Visual cue