Effects of temperature and food availability on the antipredator behaviour of juvenile coral reef fishes

Lienart, Govinda-Das Hugo (2016) Effects of temperature and food availability on the antipredator behaviour of juvenile coral reef fishes. PhD thesis, James Cook University.

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All organisms must obtain energy to survive, grow and reproduce. For species in the middle of food chains, such as juvenile coral reef fishes, energy acquisition can be particularly risky because individuals are often more vulnerable to predators while foraging. Thus, prey are under continuous pressure to optimize trade-offs between the benefits of antipredator behaviour and foraging behaviour. In addition, environmental conditions can also further cause shifts on how prey balance the costs and benefits of foraging in the light of predation risk. In particular, temperature and food availability might be expected to affect antipredator behaviour of animals through the profound impact they can have on the animal's physiology. However, the drivers and different pathways linking these environmental factors to changes in behaviour of prey animals when facing predation risk remain poorly investigated. The aim of this dissertation was to investigate the different pathways by which the thermal and feeding history of prey fish can impact antipredator behaviour. The series of laboratory-based studies use juvenile coral reef fishes (Pomacentridae) as model taxa.

The importance of a prey's feeding history has commonly been highlighted as a decisive factor in determining how prey respond to predation risk, with hungry prey accepting higher risk of predation while foraging to avoid risk of starvation. Surprisingly, while rising temperature can also impose higher energy demands for ectotherms such as fishes, no attempt has been made to test whether temperature interacts with food availability to further affect antipredator responses in prey. I explored this research question in Chapter 2. My data indicated that temperature in isolation does not influence the propensity to take risk under predation threat in well-fed fish. However, prey animals reared in condition of restrained food availability appeared to take more risks under predation threat with increasing temperature. As such, the results show that poorly and well-fed fish at 27 °C still displayed a detectable antipredator response to predation threat. However, at 30 °C (a thermal regime equivalent to the regional maximum summer temperature), poorly-fed fish, not well-fed foraged at a high rate even under the threat of predation. Interestingly, in Chapter 5 I found, based on level of energy reserves in the liver, supporting evidence that such risk-prone behaviour is very likely to be caused by a temperature-mediated increase in metabolic rate and the need for food to fuel the associated higher energy demands.

A rise in energy demands can lead prey to favor foraging at the expense of increasing exposure to predation threat. However, it can be expected that there will be an offset in the extent to which such risk-prone behaviour may happen with increasing sources of sensory information on predation threat. My experiment, in Chapter 3 is the first study to address this possibility. Although the observed behavioural patterns were not completely in line with the initial prediction, the results strongly suggest that additional sensory information on predation can lead to a further enhancement of the response, which is dependent on the prey's feeding history. Poorly and moderately-fed fish responded to a single predator cue, but further enhanced the intensity of their response to multiple predator cues. In contrast, well-fed fish displayed a fully-developed antipredator responses to any threat cue regardless of the nature of the sensory source or number of senses that informed the threat. The high vigilance of well-fed individuals is best explained by the asset-protection principle, which predicts that the more an individual stands to lose (i.e., high body reserves and larger body size), the more cautiously it should behave.

While higher-asset individuals may be more cautious, higher assets in the form of higher condition can in certain context-specific circumstances also lead to increased risk-taking behaviour in prey. In particular, it may be expected that as prey grow they will reduce their level of vigilance to small gape-limited predators as an adaptive mechanism to avoid losing foraging opportunities. It has been further proposed that predator-related information acquired by prey would become outdated and lose its relevancy more quickly in prey animals under high growth rate, since they outgrow their predators sooner than slow-growing individuals. In Chapter 4, I empirically tested this prediction by rearing predator-conditioned prey fish under different temperature mediated growth trajectories (27 °C vs. 30 °C) for 14 days and assessed weekly whether prey still responded to the initially acquired predator information. Although with time after the initial conditioning event all fish gradually decreased the intensity of their response to the learned predator cue, there were no significant differences in the decline of the response among the different growth trajectories. The temperature-mediated growth trajectories may have been too subtle to find detectable differences in behavioural patterns. However, these findings support the existence of an adaptive mechanism causing a decline in the informational value of a learned predator cue over time. This mechanism should give prey the ability to not persevere with maladaptive behaviour towards outdated or irrelevant information.

Temperature and food availability can also be expected to influence a prey's behavioural decision through alteration of the quality and/or quantity of the available predation-related cues to which they will be exposed. Several studies have highlighted that chemical alarm cues obtained from a poorly-fed donor prey are less effective in eliciting an alarm response in conspecifics than those obtained from fish with a good feeding history. The experiment in Chapter 5 is the first study to test how food availability can, concurrently with temperature, affect the properties alarm cues produced by a donor prey. The results indicate that the alarm cues produced by donor prey triggered a stronger antipredator response in conspecifics as rearing temperature increased from 27 °C up to 30 °C, regardless of the feeding history or body condition of the donors. However, at 32 °C, alarm cues from poorly-fed donor fish do not elicit an antipredator response as effectively in conspecifics compared to those produced by well-fed fish. These results clearly show that food supply and the thermal environment in which an organism lives can impact the effectiveness of the produced alarm cues to trigger antipredator responses in conspecifics.

This dissertation embodies a number of studies that have empirically identified, quantified and examined a series of pathways by which food availability and temperature may affect cost-benefit trade-offs between foraging and predator avoidance. Trends in the data were best explained by the animals' physiology, growth patterns and energy budget, and by the underlying impact of these on threat-sensitive and state-dependent behavioural mechanisms. While the current work assessed the individual effects of these pathways, it is clear that in the wild, such pathways will simultaneously occur to further lead to counterbalancing effects on a particular behavioural pattern. The resulting change in the intensity of the antipredator response can be expected to have rapid, widespread and diverse consequences ecological consequences. While further work is required, the current body of work demonstrates that small ecologically-relevant changes in temperature and food supply can independently and interactively determine the strength of predator-prey interaction within tropical aquatic ecosystems.

Item ID: 47533
Item Type: Thesis (PhD)
Keywords: anti-predator behaviour, body condition, chemical alarm cue, coral reef fishes, food availability, Pomacentridae, predation, risk assessment, senses, temperature
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Lienart, Govinda D.H., Mitchell, Matthew D., Ferrari, Maud C.O., and McCormick, Mark I. (2014) Temperature and food availability affect risk assessment in an ectotherm. Animal Behaviour, 89. pp. 199-204.

Chapter 5: Lienart, Govinda D.H., Ferrari, Maud C.O., and McCormick, Mark I. (2016) Thermal environment and nutritional condition affect the efficacy of chemical alarm cues produced by prey fish. Environmental Biology of Fishes, 99 (10). pp. 729-739.

Date Deposited: 05 Mar 2017 23:14
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 50%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060202 Community Ecology (excl Invasive Species Ecology) @ 50%
SEO Codes: 96 ENVIRONMENT > 9603 Climate and Climate Change > 960307 Effects of Climate Change and Variability on Australia (excl. Social Impacts) @ 100%
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