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Pisces: Terapontidae) with Particular Reference to Ontogeny and Phylogeny

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Pisces: Terapontidae) with Particular Reference to Ontogeny and Phylogeny ResearchOnline@JCU This file is part of the following reference: Davis, Aaron Marshall (2012) Dietary ecology of terapontid grunters (Pisces: Terapontidae) with particular reference to ontogeny and phylogeny. PhD thesis, James Cook University. Access to this file is available from: http://eprints.jcu.edu.au/27673/ The author has certified to JCU that they have made a reasonable effort to gain permission and acknowledge the owner of any third party copyright material included in this document. If you believe that this is not the case, please contact [email protected] and quote http://eprints.jcu.edu.au/27673/ Dietary ecology of terapontid grunters (Pisces: Terapontidae) with particular reference to ontogeny and phylogeny PhD thesis submitted by Aaron Marshall Davis BSc, MAppSci, James Cook University in August 2012 for the degree of Doctor of Philosophy in the School of Marine and Tropical Biology James Cook University 1 2 Statement on the contribution of others Supervision was provided by Professor Richard Pearson (James Cook University) and Dr Brad Pusey (Griffith University). This thesis also includes some collaborative work. While undertaking this collaboration I was responsible for project conceptualisation, laboratory and data analysis and synthesis of results into a publishable format. Dr Peter Unmack provided the raw phylogenetic trees analysed in Chapters 6 and 7. Peter Unmack, Tim Jardine, David Morgan, Damien Burrows, Colton Perna, Melanie Blanchette and Dean Thorburn all provided a range of editorial advice, specimen provision, technical instruction and contributed to publications associated with this thesis. Greg Nelson-White, Pia Harkness and Adella Edwards helped compile maps. The project was funded by Internal Research Allocation and Graduate Research Scheme grants from the School of Marine and Tropical Biology, James Cook University (JCU). In-kind field collection was also funded in part by the Australian Government’s Natural Heritage Trust National Competitive Component and Land and Water Australia. In-kind support was also provided by TropWater (formerly Australian Centre for Tropical Freshwater Research) at JCU in the form of field equipment and sample collection. 3 4 Acknowledgments I would initially like to thank my supervisors Brad Pusey and Richard Pearson for their invaluable guidance, patience and support over the course of this project. Your capacity for insights and fixes to seemingly intractable challenges was always much appreciated. I am also immensely grateful to David Morgan and Colton Perna for providing many of the fish specimens so integral to this study, as well as useful discussion. Several other collaborators on various thesis topics provided tremendous and prompt support, encouragement and advice: Melanie Blanchette for her work ethic, organizational ability and eye for detail in both the field and laboratory; Tim Jardine for his expertise and enthusiasm about all things stable isotope- related; and Peter Unmack, without whose phylogenetic contributions this thesis would undoubtedly have suffered considerably. An array of people, including Damien Burrows, Michael Pusey, Mark Kennard, Dean Thorburn, Adam Kerezsy, Matthew Knott, Jason Shaffer, Ian Dixon, Mark Adams, Gerry Allen, Jon Armbruster, Michael Baltzly, Cindy Bessey, Joshua Brown, Chris Burridge, Stephen Caldwell, Adam Fletcher, David Galeotti, Chris Hallett, Michael Hammer, Jeff Johnson, Alfred Ko’ou, Andrew McDougall, Masaki Miya, Sue Morrison, Tim Page, Ikising Petasi, Ross Smith and the Hydrobiology team, and the staff from ERISS and Northern Territory Fisheries, are also all thanked for their efforts in helping to collect and/or providing specimens. Kent Hortle and Andrew Storey are thanked for provision of data and advice regarding Papuan species. Additional samples for genetic work were provided by the Australian, Northern Territory, Queensland, South Australian, Western Australian, and University of Kansas museums and by the Smithsonian National Museum of Natural History; thanks to their staff and donors for providing samples. I am grateful to Stephen Lewis, a great sounding board regarding manuscript submission, for his endless patience and effort in helping me compensate for my poor graphical abilities. I owe a debt of gratitude to both the pioneering and current fish and evolutionary biologists whose work has been a constant source of inspiration, especially Richard Vari, whose seminal work on the terapontids was an invaluable resource throughout my thesis. Thanks are also warranted to the numerous journal editors, anonymous reviewers and thesis examiners who revised the various data chapters/manuscripts making up this thesis. Their advice and critiques 5 greatly improved the quality of my research, and provided an invaluable learning experience with regard to better analyzing, interpreting and presenting of my data. Finally, I am forever indebted to my parents Steve and Kris at so many levels: for always encouraging and fostering an interest in the natural world; for their unwavering sacrifice and support towards my education; and for their invaluable help and company (as well as sustenance) in the field. Who would have thought all those childhood days spent in the backyard creek catching spangled perch (L. unicolor) with grasshoppers on bent pins would lead to this? Finally thank you so much to my own little family – Birony, Brooke, Sophie and Hayley. Thank you for the support, forbearance and comedic relief over many years, without which I could never have completed this work. 6 Abstract Ecological processes, such as major habitat and dietary diversification, are considered to play a major role in the adaptive radiation of many vertebrates. While the Australian continent’s long- term biogeographic isolation provides an ideal and relatively independent testing ground for associated hypotheses, ecological processes have received little attention in the context of the radiation of Australia’s freshwater fishes. This thesis therefore examines the role of dietary habits, habitat affiliation and ontogeny in one of Australia’s largest families of freshwater fishes, the terapontid grunters (Terapontidae), in the context of evolutionary theory. Stomach-content analyses (SCA) of 22 north-Australian terapontid species identified distinct ontogenetic dietary shifts in all species for which sufficient data were available, with many species passing through several discrete trophic categories during their life histories. Carnivory was prevalent in juvenile terapontids, with diets dominated by aquatic insect larvae and microcrustacea, followed by divergence into a broad spectrum of feeding groups comprising carnivory (including piscivory and lepidophagy), omnivory (including frugivory and consumption of allochthonous prey), specialized herbivory and detritivory in larger size classes. Stable isotope analyses (SIA) of fish tissues largely corroborated the size-related dietary shifts identified by SCA. The combination of SIA and SCA identified the important role of ontogenetic dietary shifts in the trophic ecology of terapontids in the Burdekin River. SIA was particularly useful in indicating that, for fish species with pronounced size-related dietary shifts, the basal carbon sources supporting those species can also change markedly with ontogeny. The ontogenetic dietary shifts revealed by both SIA and SCA were so profound that different size classes of certain species occupied different trophic as well as isotopic niches. Body size, and its relationship to allometric development of several morphological features, appears to be a significant constraint dictating the trophic habits of many terapontids at different life-history stages. Preliminary analyses identified the role of allometric growth (both positive and negative allometry) – in characters such as intestinal length, maxilla length and mouth width – in driving considerable ontogenetic divergence in interspecific morphological trajectories. Despite these complex associations between body size and growth of morphological variables, multivariate analyses showed that morphology has a significant relationship to diet, both within and between terapontid species, explaining ~50% of dietary 7 variation in the 22 studied species and their constituent ontogenetic trophic units. Many of the diet-morphology relationships evident in the terapontids parallel those documented in other fish assemblages around the globe: intestinal length and sub-terminal mouth orientation positively correlated with detritivory and consumption of aquatic algae; intestinal length negatively correlated with carnivory; and conical tooth shape, maxilla length, mouth width, head length and eye diameter all positively correlated with piscivory and prey size. The potential role of historical habitat transitions in the marked trophic diversification within the terapontids was investigated using a new molecular phylogeny (using mitochondrial and nuclear genes) incorporating 36 species. Ancestral habitat reconstruction indicated that ancestral terapontids were euryhaline, with a single transition to freshwater environments being ancestral to all contemporary Australasian freshwater species. Mapping of adult terapontid feeding modes on to the molecular phylogeny indicated that carnivorous dietary habits were displayed by ancestral terapontids, which subsequently diversified into a range of additional carnivorous, omnivorous, herbivorous and detritivorous diets following the invasion of fresh waters. The evolution
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