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Identifying critical habitat for freshwater turtles: integrating long-term monitoring tools to enhance conservation and management

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Abstract

The effective conservation and management of threatened species requires comprehensive knowledge about resource utilisation. Here we integrated tissue stable isotope analysis and biotelemetry to identify the predominant dietary resources of two sympatric species of freshwater turtle, and locate where those items were acquired. We deployed an array of underwater acoustic telemetry receivers to autonomously, simultaneously, and continuously, monitor the movements of the threatened Elseya albagula and Elusor macrurus, over a 12-month period. Stable isotope (SI) values (δ13C and δ15N) were measured within the carapace of each species, and compared with SI values within potential food items. The integration of movement information and carapace SI data revealed that whilst these species had overlapping home ranges, there was less than 5% probability of inter-species dietary niche overlap. E. macrurus acquired food items consisting of bivalves, gastropods and aquatic insects within rocky riffles whilst E. albagula fed on filamentous algae and crustaceans foraged from the muddy and vegetated shallow margins of deep water pools. Our findings differ from stomach content analysis and mark-recapture studies, which reported these species to have similar habitat and resource requirements. We argue that the observed disparity is because our methods provided a weighted measure of an individual’s dietary preference and habitat utilisation over a broad time-scale, whilst stomach content analysis and mark-recapture studies offer only a single observation of an individual’s dietary preference. The research demonstrates the utility of integrating passive acoustic telemetry and carapace stable isotope analysis for identifying critical habitat for freshwater turtles.

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References

  • Allanson M, Georges A (1999) Diet of Elseya purvisi and Elseya georgesi (Testudinata: chelidae), a sibling species pair of freshwater turtles, from eastern Australia. Chelonian Conserv Biol 3:473–477

    Google Scholar 

  • Aresco MJ (2010) Competitive interactions of two species of freshwater turtles, a generalist omnivore and herbivore, under low resource conditions. Herpetologica 66:259–268

    Article  Google Scholar 

  • Bailleul F, Authier M, Ducatez S, Roquet F, Charrassin JB, Cherel Y, Guinet C (2010) Looking at the unseen: combining animal bio-logging and stable isotopes to reveal a shift in the ecological niche of a deep diving predator. Ecography 33:709–719

    Article  Google Scholar 

  • Brooks LB, Harvey JT, Nichols WJ (2009) Tidal movements of East Pacific green turtle Chelonia mydas at a foraging area in Baja California Sur, Mexico. Mar Ecol Prog Ser 386:263–274

    Article  Google Scholar 

  • Buhlmann KA, Vaughan MR (1991) Ecology of the turtle Pseudemys concinna in the New River, West Virginia. J Herpetol 25:72–78

    Article  Google Scholar 

  • Bulte G, Blouin-Demers G (2008) Northern map turtles (Graptemys geographica) derive energy from the pelagic pathway through predation on zebra mussels (Dreissena polymorpha). Freshwater Biol 53:497–508

    Article  Google Scholar 

  • Burkholder DA, Heithaus MR, Thomson JA, Fourqurean JW (2011) Diversity in trophic interactions of green sea turtles Chelonia mydas on a relatively pristine coastal foraging ground. Mar Ecol Prog Ser 439:277–293

    Article  Google Scholar 

  • Campbell HA, Sullivan S, Read MA, Gordos MA, Franklin CE (2010) Ecological and physiological determinants of dive duration in the freshwater crocodile. Funct Ecol 24:103–111

    Article  Google Scholar 

  • Campbell HA, Watts ME, Dwyer RG, Franklin CE (2012) V-Track: software for analysing and visualising animal movement from acoustic telemetry detections. Mar Freshw Res 63:815–820

    Article  Google Scholar 

  • Campbell HA, Beyer HL, Dennis TE, Dwyer RG, Forester JD, Fukuda Y et al (2015) Finding our way: on the sharing and reuse of animal telemetry data in Australasia. Sci Total Environ 534:79–84

    Article  CAS  PubMed  Google Scholar 

  • Cann J (1998) Australian freshwater turtles. John Cann & Beaumont Publishing Pte Ltd., La Perouse

    Google Scholar 

  • Caron-Beaudoin E, Gentes ML, Patenaude-Monette M, Helie JF, Giroux JF, Verreault J (2013) Combined usage of stable isotopes and GPS-based telemetry to understand the feeding ecology of an omnivorous bird, the Ring-billed gull (Larus delawarensis). Can J Zool 91:689–697

    Article  CAS  Google Scholar 

  • Ceriani SA, Roth JD, Evans DR, Weishampel JF, Ehrhart LM (2012) Inferring foraging areas of nesting loggerhead turtles using satellite telemetry and stable isotopes. PLoS ONE 7:12

    Article  Google Scholar 

  • Christensen RJ, Chow-Fraser P (2014) Use of GPS loggers to enhance radio-tracking studies of semi-aquatic freshwater turtles. Herpetol Conserv Biol 9:18–28

    Google Scholar 

  • Cunjak RA, Roussel JM, Gray MA, Dietrich JP, Cartwright DF, Munkittrick KR, Jardine TD (2005) Using stable isotope analysis with telemetry or mark-recapture data to identify fish movement and foraging. Oecologia 144:636–646

    Article  CAS  PubMed  Google Scholar 

  • Department of the Environment (2016a) Elusor macrurus in species profile and threats database, Department of the Environment, Canberra. Available from: http://www.environment.gov.au/sprat. Accessed 25 Jan 2016

  • Department of the Environment (2016b) Elseya albagula in species profile and threats database, Department of the Environment, Canberra. http://www.environment.gov.au/sprat. Accessed 25 Jan 2016

  • Dwyer RG, Campbell HA, Irwin TR, Franklin CE (2015) Does the telemetry technology matter? Comparing estimates of aquatic animal space-use generated from GPS-based and passive acoustic tracking. Mar Freshw Res 66:654–664

    Article  Google Scholar 

  • Eckler JT, Breisch AR, Behler JL (1990) Radio telemetry techniques applied to the bog turtle (Clemmys muhlenbergii, Schoepff 1801). New York State Museum, Albany

    Google Scholar 

  • Finlay JC, Khandwala S, Power ME (2002) Spatial scales of carbon flow in a river food web. Ecology 83:1845–1859

    Article  Google Scholar 

  • Flakus SP (2002) Ecology of the Mary River turtle, Elusor macrurus. Masters Thesis, The University of Queensland

  • Fry B (2006) Stable Isotope Ecology. Springer, New York

    Book  Google Scholar 

  • Georges A (1982) Diet of the Australian freshwater turtle Emydura krefftii (Chelonia: Chelidae), in an unproductive lentic environment. Copeia 1982:331–336

    Article  Google Scholar 

  • Godley BJ, Thompson DR, Waldron S, Furness RW (1998) The trophic status of marine turtles as determined by stable isotope analysis. Mar Ecol Prog Ser 166:277–284

    Article  Google Scholar 

  • Gordos MA, Hamann M, Schauble CS, Limpus CJ, Franklin CE (2007) Diving behaviour of Elseya albagula from a naturally flowing and hydrologically altered habitat. J Zool 272:458–469

    Article  Google Scholar 

  • Hamann M, Schauble CS, Limpus DJ, Emerick SP, Limpus CJ (2007) Management plan for the conservation of Elseya sp. (Burnett River) in the Burnett River Catchment. Report to the Queenslnd Environmental Protection Agency. ISBN 978-0-9803613-0-8

  • Hanson JO, Salisbury SW, Campbell HA, Dwyer RG, Jardine TD, Franklin CE (2015) Feeding across the food web: the interaction between diet, movement, and body size. Austral Ecol 40(3):275–286

    Article  Google Scholar 

  • Hardin G (1960) The competitive exclusion principle. Science 131:1292–1297

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann M, Hilton-Taylor C, Angulo A, Bohm M, Brooks TM, Butchart SHM, Carpenter KE et al (2010) The impact of conservation on the status of the world’s vertebrates. Science 330:1503–1509

    Article  CAS  PubMed  Google Scholar 

  • Hutchinson GE (1957) Cold spring harbor symposium on quantitative biology. Concluding Remarks 22:415–427

    Google Scholar 

  • IUCN 2015. The IUCN Red List of threatened species. Version 2015-4. http://www.iucnredlist.org

  • Jardine TD, Pettit NE, Warfe DM, Pusey BJ, Ward DP, Douglas MM, Davies PM, Bunn SE (2012) Consumer-resource coupling in wet-dry tropical rivers. J Anim Ecol 81:310–322

    Article  PubMed  Google Scholar 

  • Kennard MJ, Pusey BJ, Harch BD, Dore E, Arthington AH (2006) Estimating local stream fish assemblage attributes: sampling effort and efficiency at two spatial scales. Mar Freshw Res 57:635–653

    Article  Google Scholar 

  • Kie JG, Matthiopoulos J, Fieberg J, Powell RA, Cagnacci F, Mitchell MS, Gaillard JM, Moorcroft PR (2010) The home-range concept: are traditional estimators still relevant with modern telemetry technology? Philos Trans Soc B 365:2221–2231

    Article  Google Scholar 

  • Lara NRF, Marques TS, Montelo KM, de Ataides AG, Verdade LM, Malvasio A, de Camargo PB (2012) A trophic study of the sympatric Amazonian freshwater turtles Podocnemis unifilis and Podocnemis expansa (Testudines, Podocnemidae) using carbon and nitrogen stable isotope analyses. Can J Zool 90:1394–1401

    Article  CAS  Google Scholar 

  • Limpus CJ (2008) Freshwater turtles in the Mary River: review of biological data for turtles in the Mary River, with emphasis on Elusor macrurus and Elseya albagula). Queensland Government, Brisbane. https://www.ehp.qld.gov.au/wildlife/pdf/mary-river-turtles.pdf

  • MacDonald BD, Lewison RL, Madrak SV, Seminoff JA, Eguchi T (2012) Home ranges of East Pacific green turtles Chelonia mydas in a highly urbanized temperate foraging ground. Mar Ecol Prog Ser 461:211–221

    Article  Google Scholar 

  • MacDonald BD, Madrak SV, Lewison RL, Seminoff JA, Eguchi T (2013) Fine scale diel movement of the east Pacific green turtle, Chelonia mydas, in a highly urbanized foraging environment. J Exp Mar Biol Ecol 443:56–64

    Article  Google Scholar 

  • Markle CE, Chow-Fraser P (2014) Habitat selection by the Blanding’s turtle (Emydoidea blandingii) on a protected island in Georgian Bay, Lake Huron. Chelonian Conserv Biol 13:216–226

    Article  Google Scholar 

  • Marques TS, Tassoni M, Ferronato BO, Guardia I, Verdade LM, de Camargo PB (2011) Isotopic signatures (delta C-13 and delta N-15) of muscle, carapace and claw in Phrynops geoffroanus (Testudines: Chelidae). Zoologia 28:407–410

    Article  Google Scholar 

  • Matich P, Heithaus MR, Layman CA (2011) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J Anim Ecol 80:294–305

    Article  PubMed  Google Scholar 

  • Micheli-Campbell MA, Campbell HA, Connell MJ, Dwyer RG, Franklin CE (2013) Integrating telemetry with a predictive model to assess habitat preferences and juvenile survival in an endangered freshwater turtle. Fresh Biol 58:2253–2263

    Google Scholar 

  • Pajuelo M, Bjorndal KA, Reich KJ, Arendt MD, Bolten AB (2012) Distribution of foraging habitats of male loggerhead turtles (Caretta caretta) as revealed by stable isotopes and satellite telemetry. Mar Biol 159:1255–1267

    Article  Google Scholar 

  • Papastamatiou YP, Friedlander AM, Caselle JE, Lowe CG (2010) Long-term movement patterns and trophic ecology of blacktip reef sharks (Carcharhinus melanopterus) at Palmyra Atoll. J Exp Mar Biol Ecol 386:94–102

    Article  Google Scholar 

  • Pearson SH, Avery HW, Kilham SS, Velinsky DJ, Spotila JR (2013) Stable isotopes of C and N reveal habitat dependent dietary overlap between native and introduced turtles Pseudemys rubriventris and Trachemys scripta. PLoS ONE 8:e62891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pusey BJ, Kennard MJ, Arthington AH (2004) Freshwater fishes of North-Eastern Australia. CSIRO Publishing, Collingwood

    Google Scholar 

  • R Core Team (2016). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

  • Rogers VM (2000) Dietary ecology including dietary resource partitioning of four species of chelid turtle in a tributary of the Fitzroy River, central Queensland. Honours Thesis, Central Queensland University

  • Rosenblatt A, Nifong J, Heithaus M, Mazzotti F, Cherkiss M, Jeffery B, Elsey R et al (2015) Factors affecting individual foraging specialization and temporal diet stability across the range of a large “generalist” apex predator. Oecologia 178:5–16

    Article  PubMed  Google Scholar 

  • Scales KL, Lewis JA, Lewis JP, Castellanos D, Godley BJ, Graham RT (2011) Insights into habitat utilisation of the hawksbill turtle, Eretmochelys imbricata (Linnaeus, 1766), using acoustic telemetry. J Exp Mar Biol Ecol 407:122–129

    Article  Google Scholar 

  • Seminoff JA, Bjorndal KA (2007) Bolten AB (2007) Stable carbon and nitrogen isotope discrimination and turnover in pond sliders Trachemys scripta: insights for trophic study of freshwater turtles. Copeia 3:534–542

    Article  Google Scholar 

  • Slavenko A, Itescu Y, Ihlow F, Meiri S (2016) Home is where the shell is: predicting turtle home range sizes. J Anim Ecol 85:106–114

    Article  PubMed  Google Scholar 

  • Spencer RJ, Georges A, Lim D, Welsh M, Reid AM (2014) The risk of inter-specific competition in Australian short-necked turtles. Ecol Res 29:767–777

    Article  Google Scholar 

  • Stokes KL, Fuller WJ, Glen F, Godley BJ, Hodgson DJ, Rhodes KA, Snape RTE, Broderick AC (2014) Detecting green shoots of recovery: the importance of long-term individual-based monitoring of marine turtles. Anim Conserv 17:593–602

    Article  Google Scholar 

  • Stokes KL, Broderick AC, Canbolat AF, Candan O, Fuller WJ, Glen F, Levy Y et al (2015) Migratory corridors and foraging hotspots: critical habitats identified for Mediterranean green turtles. Divers Distrib 21:665–674

    Article  Google Scholar 

  • Swanson HK, Lysy M, Power M, Stasko AD, Johnson JD, Reist JD (2015) A new probabilistic method for quantifying n-dimensional ecological niches and niche overlap. Ecology 96:318–324

    Article  PubMed  Google Scholar 

  • Tempel DJ, Gutiérrez RJ (2013) Relation between occupancy and abundance for a territorial species, the California spotted owl. Conserv Biol 27:1087–1095

    Article  PubMed  Google Scholar 

  • Thomson S, Georges A, Lijmpus CJ (2006) A new species of freshwater turtle in the genus Elseya (Testudines: Chelidae) from central coastal Queensland, Australia. Chelonian Conserv Biol 5:74–86

    Article  Google Scholar 

  • Thums M, Whiting SD, Reisser JW, Pendoley KL, Pattiaratchi CB, Harcourt RG, McMahon CR, Meekan MG (2013) Tracking sea turtle hatchlings - A pilot study using acoustic telemetry. J Exp Mar Biol Ecol 440:156–163

    Article  Google Scholar 

  • Tucker AD (2000) Cumulative effects of dams and weirs on freshwater turtles: Fitzroy, Kolan, Burnett and Mary catchments. Queensland Department of Natural Resources, Brisbane

    Google Scholar 

  • Tucker AD, Guarino F, Priest TE (2012) Where lakes were once rivers: contrasts of freshwater turtle diets in dams and rivers of Southeastern Queensland. Chelonian Conserv Biol 11:12–23

    Article  Google Scholar 

  • Vander Zanden HB, Bjorndal KA, Reich KJ, Bolten AB (2010) Individual specialists in a generalist population: results from a long-term stable isotope series. Biol Lett 6:711–714

    Article  PubMed  PubMed Central  Google Scholar 

  • Vogt RC, Guzman SG (1988) Food partitioning in a neotropical freshwater turtle community. Copeia 1988:37–47

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

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Acknowledgements

This research was funded by an International Postgraduate Research Scholarship (IPRS) awarded to M.A.M.C. by the Australian Federal Government and The University of Queensland, an Australian Research Council Linkage Grant to CEF (LP0992220) with Tiaro & District Landcare Group as industry partners, a Queensland Government Everyone’s Environment Grant, and support from SEQwater. All procedures were conducted in accordance with The University of Queensland Animal Ethics Committee (SBS/301/12/URG) and a Queensland Department of Environment and Heritage Scientific Purposes Permit (WISP02255909).

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Authors and Affiliations

  1. School of Biological Sciences, The University of Queensland, St. Lucia, QLD, 4072, Australia

    Mariana A. Micheli-Campbell, Ross G. Dwyer, Craig E. Franklin & Hamish A. Campbell

  2. Tiaro & District Landcare Group, Tiaro, QLD, 4650, Australia

    Marilyn J. Connell

  3. Australian Rivers Institute, Griffith University, Nathan, QLD, 4111, Australia

    Brian Fry, Mark J. Kennard & Juan Tao

  4. Research Institute for the Environment and Livelihoods, School of Environment, Charles Darwin University, Darwin, NT, 0909, Australia

    Mariana A. Micheli-Campbell, Marilyn J. Connell & Hamish A. Campbell

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  1. Mariana A. Micheli-Campbell
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Correspondence to Hamish A. Campbell.

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Communicated by Dirk Sven Schmeller.

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Micheli-Campbell, M.A., Connell, M.J., Dwyer, R.G. et al. Identifying critical habitat for freshwater turtles: integrating long-term monitoring tools to enhance conservation and management. Biodivers Conserv 26, 1675–1688 (2017). https://doi.org/10.1007/s10531-017-1325-9

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