The role of chemical alarm cues in risk assessment and predator recognition in coral reef fishes

Mitchell, Matthew David (2012) The role of chemical alarm cues in risk assessment and predator recognition in coral reef fishes. PhD thesis, James Cook University.

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Through the removal of individuals, predation shapes the distribution and abundance of prey communities. Consequently, how prey species detect and respond to predation threats within their environment will determine survival and future fitness. The mere presence of predators in an environment has a significant effect on the life histories of prey individuals. The use of visual, olfactory and auditory cues allows prey to detect and learn about predators and their associated risks within their environment in a way that allows the development of predator specific antipredator responses. In complex environments, such as coral reefs, olfactory cues are thought to be especially important as increased complexity reduces access to visual cues. There is evidence to suggest that olfactory cues such as chemical alarm cues maybe used by a wide range of coral reef fishes, however there is lack of information regarding the role such cues play in risk perception and predator recognition. This study therefore investigates how coral reef fishes use chemical alarm cues to assess risk and learn to recognise predators and the risk they represent.

To understand how fishes use chemical alarm cues to assess risk, there is a need to understand what cues they are able to detect. How juvenile coral reefs fishes use cues from heterospecific prey guild members is unclear but use of heterospecific cues should enhance risk assessment. Chapter 2 tested if naïve juvenile fish have an innate recognition of heterospecific alarm cues and whether such recognition arises from phylogenetic conservation of chemical alarm cues. Naïve juvenile Amphiprion percula were tested to see if they displayed antipredator responses to chemical alarm cues from four closely related heterospecific species (family Pomacentridae), a distantly related sympatric species (Asterropteryx semipunctatus; family Gobidae) and a saltwater control. Juveniles displayed significant reductions in foraging rate when exposed to all four confamilial species and the intensity of the response was strongly correlated to the extent to which species were related to A. percula. These findings demonstrate that chemical alarm cues are conserved within the Pomacentridae family, as predicted by the phylogenetic relatedness hypothesis.

In the absence of innate predator recognition prey must learnt to recognise predators in an efficient manner, particularly when entering a novel environment. Predation pressure should therefore selectively promote mechanisms that enable the rapid identification of novel predators. Chapter 3 tested the ability of a juvenile marine fish, lemon damselfish (Pomacentrus moluccensis), to simultaneously learn the identity of multiple previously unknown predators. Individuals were conditioned with a „cocktail‟ of novel odours (from two predators and two non-predators) paired with either a conspecific alarm cue or a saltwater control and then tested the following day for recognition of the four odours individually and two novel odours (one predator and one non-predator). Individuals conditioned with the ‘cocktail’ and alarm cue responded to the individual ‘cocktail’ odours with an antipredator response but not the controls. These results demonstrate the ability to of juvenile fishes to process multiple sources of information regarding predator identities simultaneously and still recognise predators individually. The ability to rapidly assimilate information regarding predator identities should significantly enhance risk assessment and their chances of survival.

Learnt predator recognition, although potentially costly, provides animals with an adaptive mechanism to rapidly adjust to current levels of predation risk. Prey may reduce the costs associated with learning if they can use information learned about known predators to respond to cues from closely related predators with which they are unfamiliar. Chapter 4 demonstrated that, in a community where the ability to predict the predatory status novel species is low (i.e. high diversity of closely related predators and non-predators), prey fish generalise predator recognition to novel congeneric species but not confamilial species. P. moluccensis, conditioned to recognise the odour of a predatory moon wrasse, Thalassoma lunare, as a risky stimulus subsequently displayed antipredator responses not only to T. lunare odour, but also to the congeneric Thalassoma amblycephalum and Thalassoma hardwicke odours. Recognition was not extended to species beyond the genus level. Our results showed that P. moluccensis could not distinguish between predators and non-predators when generalising predator recognition. The extent to which prey generalise predator recognition appear to depend on the ability to accurately predict predator identities based on an innate knowledge of the functional diversity within the community to which previous generations have been exposed.

In communities of high biodiversity, the ability to distinguish predators from non-predators is crucial for prey success. Coral reef fishes enter new environments apparently naïve to the identity of both predators and non-predators. The remarkable efficiency of learning using chemical alarm cues means that recognition mistakes may occur if prey inadvertently learn that a species is a predator when it is not. Latent inhibition is a means by which prey that are pre-exposed to an unknown species in the absence of negative reinforcement can learn that the unknown animal is likely not a threat. Chapter 5 demonstrated that a common coral reef fish, P. moluccensis, can learn to recognize a predator as non-threatening through latent inhibition. Furthermore, we showed that we could override the latent inhibition effect by conditioning the prey to recognize the predator numerous times. These results highlight that prey fish are able to correct recognition mistakes by continually updating the information regarding the threat posed by other fishes in their vicinity.

Fishes are exposed to different suits of predators throughout ontogeny and they should therefore respond to and learn about predators using cues that are most relevant to their current situation. Chapter 6 tested whether juvenile spiny chromis, Acanthochromis polyacanthus, could distinguish between chemical alarm cues originating from conspecifics of different ontogenetic stages and whether cue origin affected its efficacy when learning about predators. Juveniles displayed a significant antipredator response to juvenile chemical alarm cues and subsequently only learned to recognise the predator after being conditioned with juveniles alarm cues. Juveniles failed to respond and learn from chemical alarm cues from larger individuals. This demonstrates that prey are highly selective in how they use information about predation risks from conspecifics, responding to and learning from only those cues that are relevant to their current developmental stage.

Item ID: 28960
Item Type: Thesis (PhD)
Keywords: predator-prey interactions; olfaction; cognition; chemical alarm cues; coral reef fishes
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Leahy, Susannah, McCormick, Mark I., Mitchell, Matthew D., and Ferrari, Maud C.O. (2011) To fear or to feed: the effects of turbidity on perception of risk by a marine fish. Biology Letters, 7 (6). pp. 811-813.

Mitchell, Matthew D., McCormick, Mark I., Ferrari, Maud C.O., and Chivers, Douglas P. (2011) Friend or foe? The role of latent inhibition in predator and non-predator labelling by coral reef fishes. Animal Cognition, 14 (5). pp. 707-714.

Date Deposited: 02 Sep 2013 05:58
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060201 Behavioural Ecology @ 34%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 33%
06 BIOLOGICAL SCIENCES > 0608 Zoology > 060801 Animal Behaviour @ 33%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 100%
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