Predator-prey interactions and the importance of sensory cues in a changing world

Lönnstedt, Oona Margareta (2013) Predator-prey interactions and the importance of sensory cues in a changing world. PhD thesis, James Cook university.

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Despite the overwhelming importance of predation in coral reefs, there is a paucity of information on how predators interact with and impact prey populations, and behavioural mechanisms that underlie these interactions. Coral reefs undergo frequent disturbances from biological and environmental agents, and reef inhabitants must continuously adapt and react to their changing environment or die. As the environment changes, the ways in which prey assess the risk of predation are predicted to change as the lucidity of sensory cues will be strongly tied to prevailing habitat features. Making appropriate decisions in the face of predation risk dictates the fate of prey, and for tropical fish predation risk is highest at life history boundaries such as settlement. The overall focus of this study was to examine how the dynamic relationship between predatory fishes and their settlement stage fish prey is influenced by physical and biological disturbances.

The focus of Chapter 2 was to explore how feeding history influences the relative importance of olfactory and visual sensory modes of learning, and how the experience gained through these sensory modes influences behaviour and predator-related mortality in the field for a settlement stage coral reef damselfish. Both feeding history and experience interacted to have a strong influence on the propensity of newly settling Pomacentrus wardi to take risks in their natural environment. Pre-release teaching of two main reef predators to settlement-stage damselfish led to a ~65% survival after 3 days, while predator-naïve fish had <10% survival during the same period of time. This experiment highlights the importance of a flexible and rapid mechanism of learning the identity of predators for survival of young fish during the critical life-history transition between pelagic and benthic habitats.

Non-lethal impacts of predators may also have a major influence on the factors that affect the survival of prey individuals, by subverting growth potential, influencing colour patterns or long-term behaviour of new settlers. Chapter 3 examined whether and how the presence of predators indirectly influences prey growth, behaviour and survival in juvenile damselfish, Pomacentrus amboinensis. Interestingly, prey exposed to predators for 6 weeks grew deeper bodies and developed larger false eyespots and smaller eyes than fish exposed to herbivores or isolated. Furthermore, when reared with predators, prey hid more, fed less and had an overall lower activity rate than fish from control treatments. Prey from predator treatments also displayed a significantly higher survival once in the field. Clearly, phenotypically plastic development in prey morphology and coloration as well as conservative behaviours can result in dramatic increases in survival for marine prey.

The goal of Chapter 4 was to examine how experienced and naïve prey individuals respond to different cues that signify the presence of three very different predators (one a highly successful invasive predator, the red lionfish Pterois volitans). This study found that P. volitans has evolved to circumvent prey risk assessment abilities as it was virtually undetectable by prey. While experienced prey damselfish, Chromis viridis, responded with typical antipredator behaviours when exposed to two non-invasive species they failed to visibly react to either the scent or visual presentation of P. volitans. No other species has been found to be able to circumvent the sophisticated threat-learning mechanism that fishes possess, and the current findings could be one of the reasons that P. volitans is such a successful invader in the Caribbean reef ecosystem.

Habitat degradation is one of the "Big Five" drivers of biodiversity loss. However, the underlying mechanism for this loss and the cascading consequences of habitat degradation on the complex interrelationships between predators and their prey are poorly understood. Chapter 5 examines impacts of habitat degradation on risk assessment mechanisms of naïve prey. I found that risk assessment behaviours of new settlers are severely affected by coral degradation. Settlement stage damselfish (P. amboinensis) were exposed to visual and olfactory indicators of predation risk in healthy live, thermally bleached, and dead algal covered coral in a series of laboratory and field experiments. While fish still responded to visual cues in all habitats, they did not respond to olfactory indicators of risk in dead coral habitats, likely as a result of alteration or degradation of chemical cues. These cues are critical for learning and avoiding predators, and as the proportion of dead coral increases, a failure to respond to these crucial threat cues can have dramatic repercussions for survival and recruitment.

While it is known that ocean acidification impairs the ability of prey fish to detect olfactory signposts of risk, it is unknown whether visual information may compensate for the lack of olfactory abilities. Chapter 6 explored the effects that ocean acidification has on abilities of naïve prey (P. amboinensis) to respond to predators. While the visual response to a predator was affected by high CO₂, it was not entirely lost. Fish exposed to 850 μatm showed reduced antipredator responses, however, exposure to CO₂ did not fully impair responses of the prey to the sight of the predator. These results provide us with a glimmer of hope that fish can adapt and survive through selection in an otherwise very disturbed ecosystem.

The current body of work has provided us with a wider understanding of how biological and physical habitat disturbances can affect species interactions and crucial behavioural processes in a severely stressed ecosystem. I have demonstrated how some of the complex dynamics of coral reef systems will change as these environments continue to be put under stress. By furthering our understanding of the highly complex dynamics of predator-prey interactions we strengthen our ability to interpret the processes that regulate communities and can begin to understand how changes in our natural world will affect these crucial ecological processes.

Item ID: 40685
Item Type: Thesis (PhD)
Keywords: chemical alarm cues; coral degradation; coral reef fishes; coral reefs; learned predator recognition; ocean acidification; olfactory cues; Pomacentrus amboinensis; predation; predator; predator-prey interactions; prey feeding history; prey; Pseudochromis fuscus; sensory cues; sensory redundancy; visual cues
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Lönnstedt, Oona M., McCormick, Mark I., Meekan, Mark G., Ferrari, Maud C.O., and Chivers, Douglas P. (2012) Learn and live: predator experience and feeding history determines prey behaviour and survival. Proceedings of the Royal Society of London Series B, Biological Sciences, 279 (1736). pp. 2091-2098. Item availability may be restricted.

Chapter 3: Lonnstedt, Oona M., McCormick, Mark I., and Chivers, Douglas P. (2013) Predator-induced changes in the growth of eyes and false eyespots. Scientific Reports, 3. pp. 1-5.

Chapter 4: Lönnstedt, Oona M., and McCormick, Mark I. (2013) Ultimate predators: lionfish have evolved to circumvent prey risk assessment abilities. PLoS ONE, 8 (10). pp. 1-8.

Chapter 5: Lönnstedt, Oona I., McCormick, Mark I., and Chivers, Douglas P. (2012) Degraded environments alter prey risk assessment. Ecology and Evolution, 3 (1). pp. 38-47.

Chapter 6: Lönnstedt, Oona M., Munday, Philip L., McCormick, Mark I., Ferrari, Maud C.O., and Chivers, Douglas P. (2013) Ocean acidification and responses to predators: can sensory redundancy reduce the apparent impacts of elevated CO2 on fish? Ecology and Evolution, 3 (10). pp. 3565-3575.

Date Deposited: 01 Oct 2015 03:36
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060201 Behavioural Ecology @ 33%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 34%
05 ENVIRONMENTAL SCIENCES > 0501 Ecological Applications > 050101 Ecological Impacts of Climate Change @ 33%
SEO Codes: 96 ENVIRONMENT > 9603 Climate and Climate Change > 960307 Effects of Climate Change and Variability on Australia (excl. Social Impacts) @ 50%
97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 50%
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