Year

2021

Degree Name

Doctor of Philosophy

Department

School of Earth, Atmospheric and Life Sciences

Abstract

Conservation behaviour is an emerging discipline that seeks to use knowledge of the proximate and ultimate causes of animal behaviour to help direct wildlife conservation. Conservation breeding programs (CBPs; incorporating both captive breeding and release) are one important component of threatened species recovery; however, their success is often hindered by reproductive failures in captivity and poor post-release survival. There is growing recognition that knowledge of intersexual selection (female mate choice) and individual behavioural variation (encompassing animal personality, behavioural syndromes and behavioural plasticity) can play a critical role in improving CBP outcomes, due to the widespread effects of these behavioural phenomena on individual survival and reproductive success. However, strategies to integrate such knowledge into CBP management are often limited by a lack of information on the behaviour of a target species. The general aim of this thesis was to advance our understanding of the behaviour of two of Australia’s most critically endangered vertebrate species; the northern corroboree frog (Pseudophryne pengilleyi) and the southern corroboree frog (Pseudophryne corroboree), both of which are the subject of multi-institutional, large scale CBPs. Specifically, this thesis aimed to investigate patterns of: (1) individual behavioural variation and (2) intersexual selection to assist with the development of behaviour-based captive breeding and reintroduction strategies for these species. In Chapter 2, I provide a comprehensive review of animal personality and behavioural syndrome research in amphibians and outline the potential for this knowledge to improve amphibian CBP outcomes. Despite being the least researched vertebrate class in the animal personality field, I highlight that numerous amphibian species display animal personality and behavioural syndromes across multiple behavioural axes, and that amphibians represent a unique yet untapped model system for testing the proximate mechanisms underpinning the development of individual behavioural differences. Importantly, I emphasise that the integration of animal personality theory into amphibian CBPs has enormous potential to: (1) bolster captive breeding success by ensuring behavioural compatibility between paired mates, and (2) increase post-release success by facilitating the selection of optimal behavioural types for reintroduction. Following from the conceptual advances made in Chapter 2, in Chapter 3 I report the findings of a long-term manipulative diet experiment designed to elucidate the effect of nutritional conditions (defined by dietary carotenoid availability) at different life stages on the development of animal personality and behavioural plasticity in P. corroboree. This work revealed that individuals that did not receive carotenoids as larvae developed greater among-individual variance (personality) in exploration behaviour compared to those that did receive carotenoids; and individuals who did not receive carotenoids at either life stage developed greater within-individual variance (plasticity) in exploration behaviour than individuals that did receive carotenoids. These findings indicate that early life environment can have irreversible effects on the development of individual behavioural phenotypes, and suggest that variation in nutritional conditions experienced throughout life may be a proximate mechanism underpinning personality and plasticity differences in P. corroboree. In Chapter 4, I aimed to gain preliminary insights into variation in female mate preferences for male acoustic cues in P. corroboree. To achieve this I conducted repeated phonotaxis trials to determine whether females exhibit a population level preference for male advertisement call frequency, and whether females vary in their preferences over time. Females did not show a population-level preference for call frequency in the first trial; yet, individual females varied in their preferences over sequential trials, and in the last trial, low frequency advertisement calls were significantly preferred. These findings suggest that female P. corroboree prefer low frequency male calls after repeated exposure, and illustrate that females can exhibit reversible plasticity in mate preferences within a single reproductive cycle. In Chapter 5, I used a field study, combined with a genomic approach to assign parentage, to explore correlates of male mating success in the largest remaining wild population of P. pengilleyi. Taking a multivariate approach, I investigated whether mating success was predicted by multiple male phenotypic traits (age, body size, colouration, calls) as well as the soil moisture of male-constructed nests. Additionally, I explored whether infection with amphibian chytrid fungus (Batrachochytrium dendrobatidis, Bd), a virulent and globally distributed pathogen, influenced male calling behaviour and mating success. I found that mating probability was best predicted by male age. However, variation in total egg number was most strongly explained by the interaction between male Bd infection status and call pulse repetition rate. These findings suggest that female mate choice in P. pengilleyi is based on multiple cues, but that reproductive outcomes may be altered by the presence of Bd. Finally, in Chapter 6 I investigated whether combinations of male phenotypic traits predicted male mating and fertilisation success in P. corroboree breeding in a homogenous captive environment. I found that male mating and fertilisation success were predicted by a combination of interactions between multiple call traits (call frequency, rate and duration), as well as male age and body size. These results suggest that female P. corroboree use multiple phenotypic cues to discriminate amongst potential mates, and that they combine information from traits non-additively. Moreover, these findings suggest that females gain direct fertility benefits from their mate choice decisions. Collectively, the findings of this thesis: (1) demonstrate the exceptional level of behavioural variability exhibited by corroboree frogs, at both the among and within-individual level, and potential for this variation to be linked to captive environmental conditions, (2) provide the first information on the reproductive behaviour and patterns of female mate choice in two of Australia’s most critically endangered vertebrate species, (3) illustrate the complexity of female mate choice in these species, and that females likely use multiple cues to choose mates, and (4) highlight the potential for mate choice processes to be altered in natural environments by the presence of infectious disease. More broadly, this thesis contributes to the fast-growing field of animal personality, and advances our understanding of mechanisms underpinning behavioural variation. This thesis also advances our understanding of sexual selection processes in anurans, and adds to a growing literature on multimodal signaling and mate choice plasticity. From a conservation perspective, the advances made by this thesis provide a platform for conservation managers to develop behaviour-based management strategies for both P. corroboree and P. pengilleyi. I argue that incorporating the knowledge gained from this thesis into captive management may enhance reproductive output, facilitate the breeding of ‘unattractive’ but genetically valuable individuals, as well as improve post-release survivorship and recruitment. Importantly, this thesis also emphasises the need for conservation managers to consider the broad range of mechanisms through which Bd affects threatened amphibian populations worldwide. Ongoing conservation behaviour research in amphibians is needed to help improve amphibian conservation outcomes globally, and such work will also help further develop a conceptual framework for integrating knowledge of the proximate and ultimate causes of behaviour into endangered species management.

FoR codes (2008)

050202 Conservation and Biodiversity, 050211 Wildlife and Habitat Management, 0602 ECOLOGY

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Unless otherwise indicated, the views expressed in this thesis are those of the author and do not necessarily represent the views of the University of Wollongong.