Dietary ecology of terapontid grunters (Pisces: Terapontidae) with particular reference to ontogeny and phylogeny

Davis, Aaron Marshall (2012) Dietary ecology of terapontid grunters (Pisces: Terapontidae) with particular reference to ontogeny and phylogeny. PhD thesis, James Cook University.

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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 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 of herbivorous-detritivorous diets – a rare evolutionary occurrence in most other fish lineages – is especially prevalent in Australia's freshwater terapontids, with plant and/or detrital material being predominant in around two-thirds of the species included in this study. Comparative analyses suggested that following the freshwater invasion, the single clade exhibited an increased rate of diversification, radiating at more than twice the background rate of the rest of the family. The marine-freshwater transition within the Terapontidae therefore appears to have resulted in much greater dietary radiation and lineage diversification in fresh waters than in euryhaline-marine habitats.

Ontogeny has also apparently played a major role in the evolutionary ecology and phylogenetic diversification of the Terapontidae, specifically in the role of intestinal length in dietary habits. Several different patterns of ontogenetic increase in intestinal length were evident in terapontid species, with increasing intestinal complexity during ontogeny driving this variability. Phylogenetically independent contrasts indicated that the interspecific differences in intestinal length resulting from these ontogenetic mechanisms explained ~60% of the variability in the proportion of plant-detrital material in terapontid diets. The ontogenetic development of intestinal complexity therefore appears to represent an important functional innovation driving the adaptive radiation of Australia's freshwater terapontids, facilitating the adoption of omnivorous, herbivorous and detritivorous diets.

Australia is notable for the lack of dietary diversification among its freshwater fishes. These results identify the terapontids as Australia's most trophically diverse fish family, with size-related dietary shifts a fundamental feature of individual species' dietary habits. Trophic studies of fish and food webs that ignore the possibility of size-related shifts in prey and basal sources are, therefore, simplistic and potentially flawed. This study has also demonstrated that selective pressures have driven terapontid morphology to converge with other ecologically comparable fishes across the globe. The capacity to modify intestinal morphology during ontogeny appears to have been an important facilitator of trophic diversification during the terapontid freshwater radiation. Australia's biogeographic history, specifically its lack of herbivorous-detritivorus primary freshwater fishes, may have provided the necessary 'ecological opportunity' for the adaptive radiation of the freshwater terapontids.

Item ID: 27673
Item Type: Thesis (PhD)
Keywords: biogeography, body size, comparative morphology, dietary ecology, dietary habits, diet-morphology relationships, evolutionary ecology, freshwater ecology, freshwater fish, habitat diversity, ontogeny, phylogenetics, terapontid grunters, Terapontidae, trophic diversity
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Davis, A.M., Pearson, R.G., Pusey, B.J., Perna, C., Morgan, D.L., and Burrows, D. (2011) Trophic ecology of northern Australia's terapontids: ontogenetic dietary shifts and feeding classification. Journal of Fish Biology, 78 (1). pp. 265-286.

Chapter 3: Davis, Aaron M., Pusey, Bradley J., and Pearson, Richard G. (2012) Contrasting intraspecific dietary shifts in two terapontid assemblages from Australia's wet-dry tropics. Ecology of Freshwater Fish, 21 (1). pp. 42-56.

Chapter 4: Davis, Aaron M., Pusey, Bradley, and Pearson, Richard G. (2012) Trophic ecology of terapontid fishes (Pisces: Terapontidae): the role of morphology and ontogeny. Marine and Freshwater Research, 63 (2). pp. 128-141.

Chapter 5: Davis, Aaron M., Blanchette, Melanie L., Pusey, Bradley J., Jardine, Tim D., and Pearson, Richard G. (2012) Gut content and stable isotope analyses provide complementary understanding of ontogenetic dietary shifts and trophic relationships among fishes in a tropical river. Freshwater Biology, 57 (10). pp. 2156-2172.

Chapter 6: Davis, A.M., Unmack, P.J., Pusey, B.J., Johnson, J.B., and Pearson, R.J. (2012) Marine-freshwater transitions are associated with the evolution of dietary diversification in terapontid grunters (Teleostei: Terapontidae). Journal of Evolutionary Biology, 25 (6). pp. 1163-1179.

Chapter 7: Davis, Aaron M., Unmack, Peter. J., Pusey, Bradley J., Pearson, Richard G., and Morgan, David L. (2013) Ontogenetic development of intestinal length and relationships to diet in an Australasian fish family (Terapontidae). BMC Evolutionary Biology, 13 . pp. 1-16.

Funders: School of Marine and Tropical Biology, James Cook University (JCU), Natural Heritage Trust National Competitive Component, Australian Government, Land and Water Australia
Date Deposited: 14 Jun 2013 02:28
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060204 Freshwater Ecology @ 50%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060309 Phylogeny and Comparative Analysis @ 50%
SEO Codes: 96 ENVIRONMENT > 9605 Ecosystem Assessment and Management > 960503 Ecosystem Assessment and Management of Coastal and Estuarine Environments @ 100%
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