Abstract
Freshwater turtles have an extraordinary physiological ability to endure dive times that can range from days to months using aquatic respiration. In cryptodires (e.g., white-lipped mud turtle Kinosternon leucostomum) aquatic respiration is via buccal or cutaneous routes whereas in pleurodires (e.g., Fitzroy River turtle Rheodytes leukops), it is achieved primarily via specialized cloacal bursae. This study records the voluntary diving performance of the western sawshelled turtle Myuchelys bellii in Bald Rock Creek from the temperate zone of the Murray–Darling Basin of Australia. Myuchelys bellii has a moderately specialized cloacal bursae morphology compared to other pleurodiran turtles and displays impressive dive durations spanning more than 15 days during the winter months. This is attributed to its ability to maintain aerobic dives via its cloacal bursae and low water temperatures in winter. Myuchelys bellii seasonal and diel diving performance, including its crepuscular habit, is comparable to R. leukops and Elseya albagula. This study also recorded the first aquatic hibernation at depth (>3 m) for any freshwater turtle; and only the second pleurodire to demonstrate aquatic hibernation as an overwintering strategy. Observed thermoregulation behavior in M. bellii is believed to provide multiple life history benefits.
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References
Bagatto B, Henry RP (1999) Aerial and aquatic respiration in the snapping turtle, Chelydra serpentina. J Herpetol 33:490–492
Bagatto B, Guyer C, Hauge B, Henry RP (1997) Bimodal respiration in two species of central American turtles. Copeia 1997:834–839
Boyer DR (1965) Ecology of the basking habit in turtles. Ecol 46:99–118
Butler PJ, Jones DR (1997) Physiology of diving birds and mammals. Physiol Rev 77:837–899
Butler PJ, Milsom WK, Woakes AJ (1984) Respiratory, cardiovascular and metabolic adjustments during steady state swimming in the green turtle, Chelonia mydas. Comp Physiol B 154:167–174
Caligiuri M, Robin ED, Hance AJ, Robin DA, Lewiston N, Theodore J (1981) Prolonged diving and recovery in the freshwater turtle, Pseudemys scripta: II magnitude of depression of O2 requirements and the relation to body O2 stores. Comp Biochem Physiol A 70(3):365–369
Cann J (1998) Australian Freshwater Turtles. Beaumont Publishing, Singapore
Cann J, Legler JM (1994) The Mary River Tortoise: A new genus and species of short-necked chelid from Queensland, Australia (Testudines: Pleurodira). Chelonian Conserv Biol 1:81–96
Carrière M, Rollinson N, Suley AN, Brooks RJ (2008) Thermoregulation when the growing season is short: sex-biased basking patterns in a northern population of painted turtles (Chrysemys picta). J Herpetol 42(1):206–209
Chessman B (1987) Atmospheric and aquatic basking of the Australian freshwater turtle Emydura macquarii (Gray) (Testudines: Chelidae). Herpetologica 43(3):301–306
Clark NJ, Gordos MA, Franklin CE (2008a) Diving behaviour, aquatic respiration and blood respiratory properties: a comparison of hatchling and juvenile Australian turtles. J Zool (Lond) 275:399–406
Clark NJ, Gordos MA, Franklin CE (2008b) Thermal plasticity of diving behaviour, aquatic respiration, and locomotor performance in the Mary River turtle Elusor macrurus. Physiol Biochem Zool 81(3):301–309
Clark NJ, Gordos MA, Franklin CE (2009) Implications of river damming: the influence of aquatic hypoxia on the diving physiology and behaviour of the endangered Mary River turtle. Anim Conserv 12:147–154
Crocker CE, Ultsch GR, Jackson DC (1999) The physiology of diving in a north-temperate and three tropical turtle species. J Comp Physiol B 169:249–255
Crocker CE, Graham TE, Ultsch GR, Jackson DC (2000) Physiology of common map turtles (Graptemys geographica) hibernating in the Lamolille River, Vermont. J Exp Zool 286(2):143–148
DonnerWright DM, Bozek MA, Probst JR, Anderson EM (1999) Responses of turtle assemblage to environmental gradients in the St. Croix River in Minnesota and Wisconsin. USA Can J Zool 77(6):989–1000
Doody JS, Sims RA, Georges A (2001) Use of thermal springs for aquatic basking by the pig-nosed turtle, Carettochelys insculpta. Chelonian Conserv Biol 4:81–87
Dunson WA (1967) Sodium fluxes in freshwater turtles. J Exp Zool 165:171–182
FitzGibbon SI (1998) The diving physiology and dive behaviour of an undescribed turtle from the Mary River, Queensland (Elseya sp.). Thesis, University of Queensland
FitzGibbon SI, Franklin CE (2010) The importance of the cloacal bursae as the primary site of aquatic respiration in the freshwater turtle, Elseya albagula. Aust Zool 35(2):276–282
Gatten RE (1980) Aerial and aquatic oxygen uptake by freely diving snapping turtles (Chelydra serpentina). Oecologia 46(2):266–271
Gordos MA, Franklin CE (2002) Diving behaviour of two Australian bimodally respiring turtles, Rheodytes leukops and Emydura macquarii, in a natural setting. J Zool (Lond) 258:335–342
Gordos MA, Franklin CE, Limpus CJ (2003a) Seasonal changes in the diving performance of the bimodally respiring freshwater turtle Rheodytes leukops in a natural setting. Can J Zool 81(4):617–625
Gordos MA, Franklin CE, Limpus CJ (2003b) Seasonal changes in the diel surfacing behavior of the bimodally respiring turtle Rheodytes leukops. Can J Zool 81:1614–1622
Gordos MA, Franklin CE, Limpus CJ (2004a) Effect of water depth and water velocity upon the surfacing frequency of the bimodally respiring freshwater turtle, Rheodytes leukops. J Exp Biol 207:3099–3107
Gordos MA, Franklin CE, Limpus CJ, Wilson G (2004b) Blood-respiratory and acid-base changes during extended diving in the bimodally respiring freshwater turtle Rheodytes leukops. J Comp Physiol B 174:347–354
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 (Lond) 272:458–469
Graham TE, Forsberg JE (1991) Aquatic oxygen uptake by naturally wintering wood turtles Clemmys insculpta. Copeia 1991(3):836–838
Gray JE (1844) Catalogue of the tortoises, crocodiles and amphibianians in the collection of the British museum. Edward Newman, London
Grigg GC, Johansen K, Harlow P, Beard LA, Taplin LE (1986) Facultative aestivation in a tropical freshwater turtle Chelodina rugosa. Comp Biochem Physiol A Physiol 82:321–323
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. Queensland Environmental Protection Agency, Brisbane
Hochsheid S, Bentivegna F, Hamza A, Hays GC (2010) When surfacers do not dive: multiple significance of extended surface times in marine turtles. J Exp Biol 213:1328–1337
Jackson DC (1968) Metabolic depression and oxygen depletion in the diving turtle. J App Physiol 24:503–509
Jackson DC (1976) Non-pulmonary CO2 loss during diving in the turtle, Pseudemys scripta elegans. Comp Biochem Physiol A Physiol 55(3):237–241
Jackson DC, Allen J, Strupp PK (1976) The contribution of non-pulmonary surfaces to CO2 loss in 6 species of turtles at 20°C. Comp Biochem Physiol A Physiol 55(3):243–246
Jackson DC, Herbert CV, Ultsch GR (1984) The comparative physiology of diving North American freshwater turtles. II. Plasma ion balance during prolonged anoxia. Physiol Zool 57(6):632–640
Jackson DC, Taylor SE, Asare VS, Villarnovo D, Gall JM, Reese SA (2007) Comparative shell buffering properties correlate with anoxia tolerance in freshwater turtles. Am J Reg Integr Comp Physiol 292:R1008–R1015
Jeffree RA, Jones MK (1992) Accumulation of radiocalcium from the aquatic medium via the cloaca and buccopharynx of Australian freshwater turtles (Chelidae). Comp Biochem Physiol A Physiol 102(1):85–91
Kennett RM, Christian K (1994) Metabolic depression in aestivating long-necked turtles (Chelodina rugosa). Physiol Zool 67:1087–1102
Kennett RM, Roe JH, Hodges K, Georges A (2009) Chelodina longicollis (Shaw 1794): Eastern long-necked turtle, Common long-necked turtle, Common snake-necked turtle. Chelonian Res Monogr 5:31.1–31.8
King P, Heatwole H (1994a) Non-pulmonary respiratory surfaces of the chelid turtle Elseya latisternum. Herpetologica 50:262–265
King P, Heatwole H (1994b) Partitioning of aquatic oxygen uptake among different respiratory surfaces in a freely diving pleurodiran turtle, Elseya latisternum. Copeia 1994(3):802–806
King JM, Kuchling G, Bradshaw SD (1998) Thermal environment, behavior, and body condition of wild Pseudemydura umbrina (Testudines: Chelidae) during late winter and early spring. Herpetologica 54(1):103–112
Legler JM, Cann J (1980) A new genus and species of chelid turtle from Queensland, Australia. Contrib Sci (Nat Hist Mus Los Angeles County) 324:1–18
Legler JM, Georges A (1993) Family Chelidae. In fauna of Australia (Vol. 2, Chapter 21). Australian Government Publishing Service, Canberra
Limpus CJ, Limpus DJ, Hamann M (2002) Freshwater turtle populations in the area to be flooded by the Walla Weir, Burnett River, Queensland: baseline study. Mem Queensl Mus 48(1):155–168
Linderman PV (2000) Resource use of five sympatric turtle species: effects of competition, phylogeny, and morphology. Can J Zool 78:992–1008
Maginniss LA, Ekelund SA, Ultsch GR (2004) Blood oxygen transport in common map turtles during simulated hibernation. Physiol Biochem Zool 77(2):232–241
Manning B, Grigg GC (1997) Basking is not of thermoregulatory significance in the “basking” freshwater turtle Emydura signata. Copeia 1997(3):579–584
Mathie NJ, Franklin CE (2006) The influence of body size on the diving behaviour and physiology of the bimodally respiring turtle, Elseya albagula. J Comp Physiol B 176:739–747
Meeks LM, Ultsch GR (1990) Overwintering behavior of snapping turtles. Copeia 1990(3):880–884
Morreale SJ, Gibbons JW (1986) Habitat suitabilitiy index models: slider turtle. 14 Washington, DC
Penney DG (1987) Frogs and turtles: different ectotherm overwintering strategies. Comp Biochem Physiol A Physiol 86(4):609–615
Peterson CC, Greenshields D (2001) Negative test for cloacal drinking in a semi-aquatic turtle (Trachmeys scripta), with comments on the functions of cloacal bursae. J Exp Zool 290:247–254
Pratt KL, Wilson RS, Blomberg SP, Franklin CE (2009) Diving and digestion: the effect of an elevated metabolic rate on submergence in an aquatic ectotherm. In: Integr Comp Biol 49:3138–3138. Presented at the Annual meeting of the Society for Integrative and Comparative Biology, UK: Oxford University Press
Priest TE (1997) Bimodal respiration and diving behaviour of the Fitzroy River turtle Rheodytes leukops. Thesis, University of Queensland, Brisbane
Priest TE, Franklin CE (2002) Effect of water temperature and oxygen levels on the diving behavior of two freshwater turtles: Rheodytes leukops and Emydura macquarii. J Herpetol 36(4):555–561
Reese SA, Jackson DC, Ultsch GR (2002) The physiology of overwintering in a turtle that occupies multiple habitats, the common snapping turtle (Chelydra serpentina). Physiol Biochem Zool 75(5):432–438
Reese SA, Stewart ER, Crocker CE, Jackson DC, Ultsch GR (2004a) Geographic variation of the physiological response to overwintering in the painted turtle (Chrysemys picta). Physiol Biochem Zool 77(4):619–630
Reese SA, Ultsch GR, Jackson DC (2004b) Lactate accumulation, glycogen depletion, and shell composition of hatchling turtles during simulated aquatic hibernation. J Exp Zool 207:2889–2895
Roe JH, Georges A (2007) Heterogeneous wetland complexes, buffer zones and travel corridors: landscape management for freshwater reptiles. Biol Conserv 135:67–76
Roe JH, Georges A (2008) Maintenance of variable responses for coping with wetland drying in freshwater turtles. Ecol 89(2):485–494
Saunders DK, Roberts AC, Ultsch GR (2000) Blood viscosity and hematological changes during prolonged submergence in normoxic water of northern and southern musk turtles (Sternotherus odoratus). J Exp Zool 287:459–466
Schofield G, Bishop CM, Katselidis KA, Dimopoulos P, Pantis JD, Hays GC (2009) Microhabitat selection by sea turtles in a dynamic thermal marine environment. J Anim Ecol 78(1):14–21
Spencer RJ, Thompson MB, Hume ID (1998) The diet and digestive energetics of an Australian short-necked turtle, Emydura macquarii. Comp Biochem Physiol A Mol Integr Physiol 121(4):341–349
Stone PA, Dobie JL, Henry RP (1992) Cutaneous surface area and bimodal respiration in soft-shelled (Trionyx spiniferus), stinkpot (Sternotherus odoratus), and mud turtles (Kinosternum subrubrum). Physiol Zool 65(2):311–330
Storey EM, Kayes SM, De Vries I, Franklin CE (2008) Effect of water depth, velocity and temperature on the sufacing frequency of the bimodally respiring turtle Elseya albagula. Funct Ecol 22:840–846
Thomson S, Georges A (2009) Myuchelys gen. nov.: a new genus for Elseya latisternum and related forms of Australian freshwater turtle (Testudines: Pleurodira: Chelidae). Zootaxa 2053:32–42
Tucker AD, Limpus CJ, Priest TE, Cay J, Glen C, Guarino E (2001) Home ranges of Fitzroy River turtles (Rheodytes leukops) overlap riffle zones: potential concerns related to river regulation. Biol Conserv 102:171–181
Ultsch GR (1988) Blood gases, hematocrit, plasma ion concentrations, and acid-base status of musk turtles (Sternotherus odoratus) during simulated hibernation. Physiol Zool 61(1):78–94
Ultsch GR, Jackson DC (1982) Long-term submergence at 3°C of the turtle, Chrysemys picta bellii, in normoxic and severely hypoxic water. I. Survival, gas exchange and acid base status. J Exp Biol 96:11–28
Ultsch GR, Herbert CV, Jackson DC (1984) The comparative physiology of diving in North American freshwater turtles. I. Submergence tolerance, gas exchange, and acid-base balance. Physiol Zool 57(6):620–631
Ultsch GR, Hanley RW, Bauman TR (1985) Responses to anoxia during simulated hibernation in northern and southern painted turtles. Ecol 66(2):388–395
Ultsch GR, Carwile ME, Crocker CE, Jackson DC (1999) The physiology of hibernation among painted turtles: the eastern painted turtle Chrysemys picta picta. Physiol Biochem Zool 72(4):493–501
van Dam RP, Diez CE (1996) Diving behaviour of immature hawksbills (Eretmochelys imbricata) in a Caribbean cliff-wall habitat. Mar Biol 127:171–178
Webb GJW (1978) Observations on basking in some Australian turtles (Reptilia: Testudines: Chelidae). Herpetologica 34:39–42
Acknowledgments
I am grateful to many volunteers who provided assistance in the field. I thank Col Limpus and Duncan Limpus for laparoscopy procedures to determine the experimental turtles’ sex and maturity. I also particularly thank Rod Hobson, Michael Wood, Jolene McLellan, John Cowburn, Neal Holmes, Ian Elms, Bill Goble and David McCarthy. I also thank Karl Vernes and anonymous reviewers for their comments on the draft manuscript. Matt Gordos deserves special mention for allowing me access to his custom dive analysis program. The University of New England Research Grant supported this study. The Queensland Department of Environment and Resource Management (DERM) provided housing and staff support for the fieldwork undertaken in Girraween National Park. Field procedures were undertaken in accordance with DERM Animal Ethics Committee (EPA2006/11/20–22).
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Fielder, D.P. Seasonal and diel dive performance and behavioral ecology of the bimodally respiring freshwater turtle Myuchelys bellii of eastern Australia. J Comp Physiol A 198, 129–143 (2012). https://doi.org/10.1007/s00359-011-0694-x
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DOI: https://doi.org/10.1007/s00359-011-0694-x