The effect of parental and embryonic predator environments on offspring

Determining the role that predation plays in population and community dynamics is vital for understanding complex ecosystems, such as coral reefs. The presence of predatory species often varies greatly with both space and time, and as such, prey species need to be able to rapidly learn and adapt to a variety of constantly changing threats. Using chemical and visual stimuli, individuals can not only identify relevant predators, but also react to them in a graded manner, depending on the level of risk they represent. Considerable research has focused on predator prey relationships and how they influence population dynamics on coral reefs. Yet, to date, no one has studied the role parental effects or the olfactory capabilities of embryonic reef fishes play in the identification of predators by prey. Therefore, this study examines the impact of predator presence and perceived risk, by both parents and developing embryos, on offspring in coral reef damselfishes. Parental effects involve non-genetic (i.e., phenotypic) inheritance of traits, which can affect offspring development and behaviour. Previous research has shown that parental exposure to predation risk can both benefit offspring (e.g., increasing antipredator behaviours), or have maladaptive consequences (e.g., metabolic and functional disorders), effects which appear to be context and species dependent. However, none of this research has shown the transferral of specific predator information, nor identified the existence of transgenerational predator recognition. Hence, Chapter 2 investigated whether a common coral reef damselfish, Acanthochromis polyacanthus, was able to transfer their learned recognition of a predatory threat in their environment to their offspring via parental effects. Breeding pairs of A. polyacanthus were exposed to one of three visual and olfactory treatments: predator, herbivore and saltwater control. Increases in heart rate induced by the introduction of test odours demonstrated that the resultant embryonic offspring from the predator-treated parents reacted significantly more (almost twofold) to the parental predator than offspring from the other two treatments. Results also showed that the embryos were able to differentiate between the five test cues, showing innate recognition of threat odours, rather than a neophobic response. This chapter provides the first example of the transfer of specific predator information via parental effects in any species. Embryos of amphibian species have been shown to not only detect olfactory stimuli, but also use such cues to learn predatory threats before hatching. Thus, the next step in the study was to determine whether damselfish embryos could learn novel predator cues using associative learning (Chapter 3). Using the clownfish, Amphiprion melanopus, I conditioned embryos with a combination of a novel predator odour and a conspecific alarm cue. By quantifying reactions as changes in heart rates, I showed that individuals that were conditioned learned to identify the predator odour as a threat; the cue elicited an increase in heart rate that was almost double that of the preconditioning response. Additionally, I showed that the closer to the expected time of hatching, the larger the increase in heart rate induced by conspecific alarm cues. These findings suggest threat cues also play a vital role in early life stage anemonefish, which are already known to imprint on odours in their natal habitat. Predator-induced mortality rates are highest in early life stages; therefore, early recognition of threats can greatly increase survival chances. Some species of coral reef fishes have been frequently found to recruit back to their natal reefs. In this instance, there is a high chance of juveniles encountering their siblings, amongst other kin, after hatching. Kin recognition plays an important ecological role in that it allows individuals to protect their relatives and gene pool, and hence increase their inclusive fitness. Additionally, research has shown that affiliating with kin can enhance predator avoidance. Consequently, Chapter 4 investigated whether two species of damselfish, with differing life histories, recognised kin through their damage-released alarm cues. Results showed that both A. polyacanthus and A. melanopus can distinguish between their kin and other conspecifics, reacting more to alarm cues produced from the former. They also reacted more to cues from conspecifics than more phylogenetically distant heterospecifics. Early recognition of kin and cues from phylogenetically similar heterospecifics could decrease predator-induced mortality through cooperation with kin and/or avoiding predation through informed habitat selection. Predatory threats can vary markedly with changes in habitat and ontogeny, and individuals will continually experience new cues throughout their lives, especially in biodiverse habitats like coral reefs. The threat sensitive hypothesis states that individuals should show a stronger response to cues that represent greater risk. As such, Chapter 5 aimed to establish whether A. polyacanthus reacted in a threat sensitive manner to cues derived from conspecific donors from different life stages. This hypothesis was based on the premise that embryos and adults would be preyed upon by different species, due to predator gape limitations, rendering adult alarm cues less relevant than those from closer ontogenetic stages. Experiments found that A. polyacanthus embryos reacted in a graded manner, with embryo alarm cues eliciting a greater increase in the heart rate of embryos than damage-cues from juveniles or adults. Responding to damage-released cues based on the level of threat they represent can enable prey to prevent unnecessary energy expenditure avoiding predatory species that pose little or no threat. Conversely, if individuals deem a cue indicative of a threat that is not relevant to their particular life stage, this would incur energetic costs. This research demonstrates that embryonic damselfishes have very well-developed olfactory capabilities that they can use to recognise predators and/or chemical alarm cues of both conspecifics and heterospecifics before hatching. Furthermore, this recognition can be augmented with parental information and/or individual experience and learning. The existence of such refined mechanisms for identification of threats in the earliest life stages of the study organisms suggests that they serve a vital role in the chemosensory recognition of predatory threats.