Resource partitioning among five sympatric species of freshwater turtles from the wet–dry tropics of northern Australia
Michael A. Welsh A D , J. Sean Doody B and Arthur Georges C
+ Author Affiliations
- Author Affiliations
A Department of the Environment and Energy, GPO Box 787, Canberra, ACT 2601, Australia.
B University of Tennessee, Knoxville, TN 37996, USA.
C Institute for Applied Ecology, University of Canberra, ACT 2617, Australia.
D Corresponding author. Email: welshmick@gmail.com
Wildlife Research 44(3) 219-229 https://doi.org/10.1071/WR16202
Submitted: 2 November 2016 Accepted: 7 April 2017 Published: 1 June 2017
Abstract
Context: Resource partitioning of diet and microhabitat was examined for five sympatric species of freshwater turtles in the Daly River in the northern end of Northern Territory (Top End) in Australia. The Daly River supports a high diversity of freshwater turtles, making it the ideal place to study a freshwater turtle community.
Aims: To determine the dry-season diet and microhabitat use of Carettochelys insculpta, Elseya dentata, Chelodina oblonga, Emydura victoriae and Emydura subglobosa worrelli and examine intraspecific and interspecific niche overlap and ontogenetic dietary shift.
Methods: Gut contents were collected by stomach flushing, and microhabitat use was determined by recording where each turtle was first seen before capture. Diet and microhabitat use were compared using an index of relative importance. Niche overlap was measured with Horn’s overlap index.
Key results: Carettochelys insculpta is an opportunistic omnivore that feeds mostly on ribbonweed (Vallisneria spiralis) and aquatic snails. Elseya dentata is herbivorous, feeding primarily on aquatic algae. The diets of C. insculpta and E. dentata overlapped moderately, but the overall niche overlap was low because they occupied different microhabitats within the river. Chelodina oblonga fed very little, and may use the Daly River as a dry-season refuge. Emydura victoriae is molluscivorous, consuming more molluscs as it grows. This ontogenetic dietary shift was associated with megacephaly (extreme broadly expanded head that is too large to fit into the carapace) and expanded triturating surfaces. This specialisation allows adult E. victoriae to feed exclusively on molluscs and so their diet overlapped little with other species. Emydura subglobosa worrelli was omnivorous, consuming mostly freshwater sponge and apparently preferring more lentic water.
Conclusions: The freshwater turtles of the wet–dry tropics are usually reported as being heavily reliant on the seeds, fruits and leaves of riparian vegetation; however, the present study showed that the dry-season diet in perennial rivers is primarily of aquatic origin.
Implications: The study suggested that populations of C. insculpta, E. dentata and E. victoriae could be threatened by broad-scale development in northern Australia if there were substantive impacts on aquatic macrophytes and molluscs in the Daly River system.
References
Allanson, M., and Georges, A. (1999). Diet of Elseya purvisi and Elseya georgesi (Testudines: Chelidae), a sibling pair of freshwater turtles from eastern Australia. Chelonian Conservation and Biology 3, 473–477.Armstrong, G., and Booth, D. T. (2005). Dietary ecology of the Australian freshwater turtle (Elseya sp.: Chelonia: Chelidae) in the Burnett River, Queensland. Wildlife Research 32, 349–353.
| Dietary ecology of the Australian freshwater turtle (Elseya sp.: Chelonia: Chelidae) in the Burnett River, Queensland.Crossref | GoogleScholarGoogle Scholar |
Australian Government (2015). ‘Our North, Our Future: White Paper on Developing Northern Australia’. (Australian Government: Canberra.)
Berry, J. F. (1975). The population effects of ecological sympatry on musk turtles in northern Florida. Copeia 1975, 692–701.
Bjorndal, K. A., Bolten, A. B., Lagueux, C. J., and Jackson, D. R. (1997). Dietary overlap in three sympatric congeneric freshwater turtles (Pseudemys) in Florida. Chelonian Conservation and Biology 2, 430–433.
Cann, J. (1997). The northern yellow-faced turtle. Victorian Herpetological Society – Monitor 9, 24–35.
Cann, J. (1998). ‘Australian Freshwater Turtles.’ (Beaumont Publishing: Singapore.)
Chessman, B. C. (1978). Ecological studies of freshwater turtles in south-eastern Australia. Ph.D. Thesis, Department of Zoology, Monash University, Melbourne.
Chessman, B. C. (2011). Declines of freshwater turtles associated with climatic drying in Australia’s Murray–Darling Basin. Wildlife Research 38, 664–671.
| Declines of freshwater turtles associated with climatic drying in Australia’s Murray–Darling Basin.Crossref | GoogleScholarGoogle Scholar |
Cortés, E. (1997). A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Sciences 54, 726–738.
| A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes.Crossref | GoogleScholarGoogle Scholar |
Cortés, E. (1998). Methods of studying fish feeding. Canadian Journal of Fisheries and Aquatic Sciences 55, 2708.
| Methods of studying fish feeding.Crossref | GoogleScholarGoogle Scholar |
Dalrymple, G. H. (1977). Intraspecific variation in the cranial feeding mechanisms of turtles of the genus Trionix (Reptilia, Testudines, Trionychidae). Journal of Herpetology 11, 255–285.
| Intraspecific variation in the cranial feeding mechanisms of turtles of the genus Trionix (Reptilia, Testudines, Trionychidae).Crossref | GoogleScholarGoogle Scholar |
Doody, J. S., and Welsh, M. A. (2005). First glimpses into the reproductive ecology of the red-faced turtle, Emydura victoriae. Herpetofauna 35, 11–14.
Doody, J. S., Young, J. E., and Georges, A. (2002). Sex differences in activity and movements in the pig-nosed turtle Carettochelys insculpta, in the wet-dry tropics of Australia. Copeia 2002, 93–103.
| Sex differences in activity and movements in the pig-nosed turtle Carettochelys insculpta, in the wet-dry tropics of Australia.Crossref | GoogleScholarGoogle Scholar |
Doody, J. S., Georges, A., and Young, J. E. (2003). Twice every second year: reproduction in the pig-nosed turtle, Carettochelys insculpta, in the wet–dry tropics of Australia. Journal of Zoology 259, 179–188.
| Twice every second year: reproduction in the pig-nosed turtle, Carettochelys insculpta, in the wet–dry tropics of Australia.Crossref | GoogleScholarGoogle Scholar |
eXactoid (2008). Information available at http://www.exactoid.com/fisher/index.php [accessed 2008].
Fachin-Teran, A. F., Vogt, R. C., and Gomez, M. F. S. (1995). Food habits of an assemblage of five species of turtles in the Rio Guapore, Rondonia, Brazil. Journal of Herpetology 29, 536–547.
| Food habits of an assemblage of five species of turtles in the Rio Guapore, Rondonia, Brazil.Crossref | GoogleScholarGoogle Scholar |
Georges, A. (1982). Diet of the Australian freshwater turtle Emydura krefftii (Chelonia: Chelidae), in an unproductive lentic environment. Copeia 1982, 331–336.
Georges, A., and Adams, M. (1996). Electrophoretic delineation of species boundaries within the short-necked freshwater turtles of Australia (Testudines: Chelidae). Zoological Journal of the Linnean Society 118, 241–260.
| Electrophoretic delineation of species boundaries within the short-necked freshwater turtles of Australia (Testudines: Chelidae).Crossref | GoogleScholarGoogle Scholar |
Georges, A., and Kennett, R. (1989). Dry season distribution and ecology of Carettochelys insculpta (Chelonia: Carettochelydidae) in Kakadu National Park, northern Australia. Australian Wildlife Research 16, 323–335.
| Dry season distribution and ecology of Carettochelys insculpta (Chelonia: Carettochelydidae) in Kakadu National Park, northern Australia.Crossref | GoogleScholarGoogle Scholar |
Georges, A., and Rose, M. (1993). Conservation biology of the pig-nosed turtle, Carettochelys insculpta. Chelonian Conservation and Biology 1, 3–12.
Georges, A., and Wombey, J. C. (1993). Family Carettochelyidae. In ‘Fauna of Australia’. (Eds. C. G. Glasby, G. J. B. Ross and P. L. Beesley.) Chapter 22, pp. 1–8. (Australian Government Publishing Service: Canberra.)
Georges, A., Norris, R. H., and Wensing, L. (1986). Diet of the freshwater turtle Chelodina longicollis (Testudines: Chelidae) from the coastal dune lakes of the Jervis Bay territory. Australian Wildlife Research 13, 301–308.
| Diet of the freshwater turtle Chelodina longicollis (Testudines: Chelidae) from the coastal dune lakes of the Jervis Bay territory.Crossref | GoogleScholarGoogle Scholar |
Georges, A., Limpus, C. J., and Parmenter, C. J. (1993). Natural history of the Chelonia. In ‘Fauna of Australia’. (Eds. C. G. Glasby, G. J. B. Ross and P. L. Beesley.) Chapter 17, pp. 1–18. (Australian Government Publishing Service: Canberra.)
Georges, A., Doody, J. S., Young, J., and Cann, J. (2000). ‘The Australian Pig-Nosed Turtle.’ (University of Canberra: Canberra.)
Hart, D. R. (1983). Dietary and habitat shift with size of Red-eared Turtles (Pseudemys scripta) in a southern Louisiana population. Herpetologica 39, 285–290.
Hart, R. K., Claver, M. C., and Dickman, C. R. (2002). The index of relative importance: an alternative approach to reducing bias in descriptive studies of animal diets. Wildlife Research 29, 415–421.
| The index of relative importance: an alternative approach to reducing bias in descriptive studies of animal diets.Crossref | GoogleScholarGoogle Scholar |
Heaphy, J. L. (1990). The ecology of the pig-nosed turtle, Carettochelys insculpta, in northern Australia. Ph.D. Thesis, University of New South Wales, Sydney.
Holt, R. D. (1987). On the relation between niche overlap and competition: the effects of incommensurable niche dimensions. Oikos 48, 110–114.
| On the relation between niche overlap and competition: the effects of incommensurable niche dimensions.Crossref | GoogleScholarGoogle Scholar |
Hyslop, E. J. (1980). Stomach contents analysis: a review of methods and their application. Journal of Fish Biology 17, 411–429.
| Stomach contents analysis: a review of methods and their application.Crossref | GoogleScholarGoogle Scholar |
International Commission on Zoological Nomenclature (2013). Opinion 2315 (Case 3351) Chelodina oblonga Ogilby, 1890 (currently Macrochelodina oblonga; Reptilia, Testudines): precedence not granted over Chelodina oblonga Gray, 1841. Bulletin of Zoological Nomenclature 70, 57–60.
| Opinion 2315 (Case 3351) Chelodina oblonga Ogilby, 1890 (currently Macrochelodina oblonga; Reptilia, Testudines): precedence not granted over Chelodina oblonga Gray, 1841.Crossref | GoogleScholarGoogle Scholar |
Kenneth Dodd, C. (1990). Effects of habitat fragmentation on a stream-dwelling species, the flattened musk turtle Sternotherus depressus. Biological Conservation 54, 33–45.
| Effects of habitat fragmentation on a stream-dwelling species, the flattened musk turtle Sternotherus depressus.Crossref | GoogleScholarGoogle Scholar |
Kennett, R. (1994). Ecology of two species of freshwater turtle, Chelodina oblonga and Elseya dentata, from the wet–dry tropics of northern Australia. Ph.D Thesis, University of Queensland, Brisbane.
Kennett, R., and Georges, A. (1989). Turtles of the top end. Northern Territory Naturalist 11, 31.
Kennett, R., and Tory, O. (1996). Diet of two freshwater turtles, Chelodina oblonga and Elseya dentata (Testudines: Chelidae) from the wet–dry tropics of northern Australia. Copeia 1996, 409–419.
| Diet of two freshwater turtles, Chelodina oblonga and Elseya dentata (Testudines: Chelidae) from the wet–dry tropics of northern Australia.Crossref | GoogleScholarGoogle Scholar |
Kennett, R., Fordham, D. A., Alacs, E., Corey, B., and Georges, A. (2014). ‘Chelodina oblonga Gray 1841 – Northern Snake-necked Turtle.’ Chelonian Research Monographs 5. (Chelonian Research Foundation: Lunenburg, MA.)
Krebs, C. J. (1989). ‘Ecological Methodology.’ (Harper & Row Publishers: New York.)
Lees, K. (2008). Different ways of living in the same environment: niche partitioning in two species of freshwater turtle. B.Sc.(Hons) Thesis, James Cook University, Townsville, Qld.
Legler, J. M. (1972). The taxonomy, distribution, and ecology of Australian freshwater turtles (Testudines: Pleurodira: Chelidae). National Geographic Society Research Reports 1972, 391–404.
Legler, J. M. (1976). Feeding habits of some Australian short-necked tortoises. Victorian Naturalist 93, 40–43.
Legler, J. M. (1977). Stomach flushing: a technique for chelonian dietary studies. Herpetologica 33, 281–284.
Legler, J. M., and Georges, A. (1993). Family Chelidae. In ‘Fauna of Australia’. (Eds. C. G. Glasby, G. J. B. Ross and P. L. Beesley.) Chapter 21, pp. 1–27. (Australian Government Publishing Service: Canberra.)
Lindeman, P. V. (2000a). Resource use of five sympatric turtle species: effects of competition, phylogeny, and morphology. Canadian Journal of Zoology 78, 992–1008.
| Resource use of five sympatric turtle species: effects of competition, phylogeny, and morphology.Crossref | GoogleScholarGoogle Scholar |
Lindeman, P. V. (2000b). Evolution of the relative width of the head and aveolar surfaces in map turtles (Testudines: Emydidae: Graptemys). Biological Journal of the Linnean Society. Linnean Society of London 69, 549–576.
Marion, K. R., Cox, W. A., and Ernst, C. H. (1991). Prey of the flattened musk turtle, Sternotherus depressus. Journal of Herpetology 25, 385–387.
| Prey of the flattened musk turtle, Sternotherus depressus.Crossref | GoogleScholarGoogle Scholar |
Moll, D. (1990). Population sizes and foraging ecology in a tropical freshwater stream turtle community. Journal of Herpetology 24, 48–53.
Pettit, N., Bayliss, P., Davies, P., Hamilton, S., Warfe, D., Bunn, S., and Douglas, M. (2011). Seasonal contrasts in carbon resources and ecological processes on a tropical floodplain. Freshwater Biology 56, 1047–1064.
Pyke, G. H. (1984). Optimal foraging theory:a critical review. Annual Review of Ecology and Systematics 15, 523–575.
| Optimal foraging theory:a critical review.Crossref | GoogleScholarGoogle Scholar |
Ross, S. T. (1986). Resource partitioning in fish assemblages: a review of field studies. Copeia 1986, 352–388.
| Resource partitioning in fish assemblages: a review of field studies.Crossref | GoogleScholarGoogle Scholar |
Schult, J., and Townsend, S. (2012). River health in the Daly catchment. A report to the Daly River Management Advisory Committee. Northern Territory Department of Natural Resources, Environment, the Arts and Sport, Darwin.
Smith, E. P., and Zaret, T. M. (1982). Bias in estimating niche overlap. Ecology 63, 1248–1253.
| Bias in estimating niche overlap.Crossref | GoogleScholarGoogle Scholar |
Snedecor, G. W., and Cochran, W. G. (1984). ‘Statistical Methods.’ 7th edn. (The Iowa State University Press: Ames, IA.)
Spencer, R., Thomson, M. B., and Hume, I. D. (1998). The diet and digestive energetics of an Australian short-necked turtle, Emydura macquarii. Comparative Biochemistry and Physiology Part A 121, 341–349.
| The diet and digestive energetics of an Australian short-necked turtle, Emydura macquarii.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M7lslOntQ%3D%3D&md5=0f3945ec9e329d41048dbc883923b7feCAS |
Spencer, R., Georges, A., Lim, D., Welsh, M., and Reid, A. (2014). The risk of inter-specific competition in Australian short-necked turtles. Ecological Research 29, 767–777.
| The risk of inter-specific competition in Australian short-necked turtles.Crossref | GoogleScholarGoogle Scholar |
Thomson, S. (1996). ‘Field Keys to the Turtles of the Northern Territory.’ (University of Canberra: Canberra.)
Tucker, A. D. (1999). ‘Cumulative Effects of Dams and Weirs on Freshwater Turtles: Fitzroy, Kolan, Burnett and Mary Catchments.’ (Queensland Department of Natural Resources: Brisbane.)
Tucker, A. D., Guarino, E., Priest, T., and Greenhood, D. (1999). Effects of habitat type, body size, and season on foraging by the freshwater turtles Emydura krefftii, Elseya sp., and Elseya latisternum. In ‘Cumulative Effects of Dams and Weirs on Freshwater Turtles: Fitzroy, Kolan, Burnett and Mary Catchments’. (Ed. A. D. Tucker.) (Queensland Department of Natural Resources: Brisbane.)
Vogt, R. C. (1981). Food partitioning in three sympatric species of map turtle, genus Graptemys (Testudinata, Emydidae). American Midland Naturalist 105, 102–111.
| Food partitioning in three sympatric species of map turtle, genus Graptemys (Testudinata, Emydidae).Crossref | GoogleScholarGoogle Scholar |
Vogt, R. C., and Guzman, S. G. (1988). Food partitioning in a neotropical freshwater turtle community. Copeia 1988, 37–47.
| Food partitioning in a neotropical freshwater turtle community.Crossref | GoogleScholarGoogle Scholar |
Wilson, M., and Lawler, I. R. (2008). Diet and digestive performance of an urban population of the omnivorous freshwater turtle (Emydura krefftii) from Ross River, Queensland. Australian Journal of Zoology 56, 151–157.
| Diet and digestive performance of an urban population of the omnivorous freshwater turtle (Emydura krefftii) from Ross River, Queensland.Crossref | GoogleScholarGoogle Scholar |
