Register      Login
Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

Freshwater turtle hatchlings that stay in the nest: strategists or prisoners?

Bruce C. Chessman
+ Author Affiliations
- Author Affiliations

7 Dalrymple Crescent, Pymble, NSW 2073, Australia. Email: brucechessman@gmail.com

Australian Journal of Zoology 66(1) 34-40 https://doi.org/10.1071/ZO17054
Submitted: 29 August 2017  Accepted: 8 November 2017   Published: 30 November 2017

Abstract

Hatchlings of several species of freshwater turtles have been reported to remain in subterranean nests for extended periods following hatching from the egg. It has been suggested that this delayed emergence, including overwintering in the nest in populations at temperate latitudes, is an evolved adaptation that enables hatchlings to enter the aquatic environment at the most propitious time for survival and growth. I monitored nests of a temperate-zone population of the freshwater Australian eastern long-necked turtle (Chelodina longicollis) for up to a year after nest construction in fine-grained soils adjacent to oxbow lakes and farm ponds. An estimated 84% of nests were preyed on, probably mainly by non-native red foxes (Vulpes vulpes), whereas hatchlings emerged from autumn to spring from an estimated 5% of nests. The remaining 11% of nests were neither preyed on nor had emergence by a year after nest construction. Live hatchlings were present in some nests with no emergence up to 10 months after nest construction, but substantial numbers of dead hatchlings were present beyond nine months. It therefore seems unlikely that emergence occurs more than a year after nest construction. Delayed emergence of this species in this environment appears less likely to be an adaptive strategy than to be a consequence of imprisonment in the nest by hard soil that is difficult for hatchlings to excavate.

Additional keywords: Chelodina longicollis, delayed emergence, predation, overwintering.


References

Baker, P. J., Costanzo, J. P., Herlands, R., Wood, R. C., and Lee, R. E. (2006). Inoculative freezing promotes winter survival in hatchling diamondback terrapin, Malaclemys terrapin. Canadian Journal of Zoology 84, 116–124.
Inoculative freezing promotes winter survival in hatchling diamondback terrapin, Malaclemys terrapin.Crossref | GoogleScholarGoogle Scholar |

Beck, R. G. (1991). The common long-necked tortoise Chelodina longicollis: a comparative study of the morphology and field behaviour of disjunct populations. South Australian Naturalist 66, 4–22.

Breitenbach, G. L., Congdon, J. D., and van Loben Sels, R. C. (1984). Winter temperatures of Chrysemys picta nests in Michigan: effects on hatchling survival. Herpetologica 40, 76–81.

Buhlmann, K. A., and Coffman, G. (2001). Fire ant predation of turtle nests and implications for the strategy of delayed emergence. Journal of the Elisha Mitchell Scientific Society 117, 94–100.

Cagle, F. R. (1944). Activity and winter changes of hatchling Pseudemys. Copeia 1944, 105–109.
Activity and winter changes of hatchling Pseudemys.Crossref | GoogleScholarGoogle Scholar |

Carroll, D. M., and Ultsch, G. R. (2007). Emergence season and survival in the nest of hatchling turtles in south central New Hampshire. Northeastern Naturalist 14, 307–310.
Emergence season and survival in the nest of hatchling turtles in south central New Hampshire.Crossref | GoogleScholarGoogle Scholar |

Chessman, B. C. (1978). Ecological studies of freshwater turtles in south-eastern Australia. Ph.D. Thesis, Monash University, Melbourne.

Congdon, J. D., and Gibbons, J. W. (1985). Egg components and reproductive characteristics of turtles: relationships to body size. Herpetologica 41, 194–205.

Costanzo, J. P., Litzgus, J. D., Iverson, J. B., and Lee, R. E. (2001). Cold-hardiness and evaporative water loss in hatchling turtles. Physiological and Biochemical Zoology 74, 510–519.
Cold-hardiness and evaporative water loss in hatchling turtles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MznvFCktA%3D%3D&md5=286d3ff43b22e7f8637b108189ed7d1aCAS |

Costanzo, J. P., Lee, R. E., and Ultsch, G. R. (2008). Physiological ecology of overwintering in hatchling turtles. The Journal of Experimental Zoology 309A, 297–379.
Physiological ecology of overwintering in hatchling turtles.Crossref | GoogleScholarGoogle Scholar |

DePari, J. A. (1996). Overwintering in the nest chamber by hatchling painted turtles, Chrysemys picta, in northern New Jersey. Chelonian Conservation and Biology 2, 5–12.

Dinkelacker, S. A., Costanzo, J. P., Iverson, J. B., and Lee, R. E. (2004). Cold-hardiness and dehydration resistance of hatchling Blanding’s turtles (Emydoidea blandingii): implications for overwintering in a terrestrial habitat. Canadian Journal of Zoology 82, 594–600.
Cold-hardiness and dehydration resistance of hatchling Blanding’s turtles (Emydoidea blandingii): implications for overwintering in a terrestrial habitat.Crossref | GoogleScholarGoogle Scholar |

Dinkelacker, S. A., Costanzo, J. P., Iverson, J. B., and Lee, R. E. (2005a). Survival and physiological responses of hatchling Blanding’s turtles (Emydoidea blandingii) to submergence in normoxic and hypoxic water under simulated winter conditions. Physiological and Biochemical Zoology 78, 356–363.
Survival and physiological responses of hatchling Blanding’s turtles (Emydoidea blandingii) to submergence in normoxic and hypoxic water under simulated winter conditions.Crossref | GoogleScholarGoogle Scholar |

Dinkelacker, S. A., Costanzo, J. P., and Lee, R. E. (2005b). Anoxia tolerance and freeze tolerance in hatchling turtles. Journal of Comparative Physiology B: Biochemical, Systems, and Environmental Physiology 175, 209–217.
Anoxia tolerance and freeze tolerance in hatchling turtles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M7ns1GltQ%3D%3D&md5=2ada95f08ce078698b5d96c107cbd09cCAS |

Dragon, J. (2014). Habitat selection, movement, and survival of hatchling wood turtles (Glyptemys insculpta) in an atypical habitat. M.Sc. Thesis, George Mason University, Fairfax, VA, USA.

Ehrenfeld, D. W. (1979). Behavior associated with nesting. In ‘Turtles: Perspectives and Research’. (Eds M. Harless and H. Morlock.) pp. 417–434. (John Wiley and Sons: New York.)

Ferronato, B. O., Roe, J. H., and Georges, A. (2015). First record of hatchling overwintering inside the natal nest of a chelid turtle. Australian Journal of Zoology 63, 287–291.
First record of hatchling overwintering inside the natal nest of a chelid turtle.Crossref | GoogleScholarGoogle Scholar |

Gibbons, J. W. (2013). A long-term perspective of delayed emergence (aka overwintering) in hatchling turtles: some they do and some they don’t, and some you just can’t tell. Journal of Herpetology 47, 203–214.
A long-term perspective of delayed emergence (aka overwintering) in hatchling turtles: some they do and some they don’t, and some you just can’t tell.Crossref | GoogleScholarGoogle Scholar |

Gibbons, J. W., and Nelson, D. H. (1978). The evolutionary significance of delayed emergence from the nest by hatchling turtles. Evolution 32, 297–303.
The evolutionary significance of delayed emergence from the nest by hatchling turtles.Crossref | GoogleScholarGoogle Scholar |

Hammer, D. A. (1969). Parameters of a marsh snapping turtle population Lacreek Refuge, South Dakota. Journal of Wildlife Management 33, 995–1005.
Parameters of a marsh snapping turtle population Lacreek Refuge, South Dakota.Crossref | GoogleScholarGoogle Scholar |

Harrington, K. H. (1933). Breeding habits of the Australian long-necked tortoise. South Australian Naturalist 15, 25–27.

Hartweg, N. (1944). Spring emergence of painted turtle hatchlings. Copeia 1944, 20–22.
Spring emergence of painted turtle hatchlings.Crossref | GoogleScholarGoogle Scholar |

Janzen, F. J., Tucker, J. K., and Paukstis, G. L. (2000). Experimental analysis of an early life-history stage: avian predation selects for larger body size of hatchling turtles. Journal of Evolutionary Biology 13, 947–954.
Experimental analysis of an early life-history stage: avian predation selects for larger body size of hatchling turtles.Crossref | GoogleScholarGoogle Scholar |

Janzen, F. J., Tucker, J. K., and Paukstis, G. L. (2007). Experimental analysis of an early life-history stage: direct or indirect selection on body size of hatchling turtles? Functional Ecology 21, 162–170.
Experimental analysis of an early life-history stage: direct or indirect selection on body size of hatchling turtles?Crossref | GoogleScholarGoogle Scholar |

Kennett, R., Christian, K., and Bedford, G. (1998). Underwater nesting by the Australian freshwater turtle Chelodina rugosa: effect of prolonged immersion and eggshell thickness on incubation period, egg survivorship, and hatchling size. Canadian Journal of Zoology 76, 1019–1023.
Underwater nesting by the Australian freshwater turtle Chelodina rugosa: effect of prolonged immersion and eggshell thickness on incubation period, egg survivorship, and hatchling size.Crossref | GoogleScholarGoogle Scholar |

Kennett, R., Roe, J., Hodges, K., and Georges, A. (2009). Chelodina longicollis (Shaw 1794) – eastern long-necked turtle, common long-necked turtle, common snake-necked turtle. In ‘Conservation Biology of Freshwater Turtles and Tortoises: a Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group’. (Eds A. G. J. Rhodin, P. C. H. Pritchard, P. P. van Dijk, R. A. Saumure, K. A. Buhlmann, J. B. Iverson, and R. A. Mittermeier.) Chelonian Research Monographs 5, 031.1–031.8.

Lindeman, P. V. (1991). Survivorship of overwintering hatchling painted turtles, Chrysemys picta, in northern Idaho. Canadian Field-Naturalist 105, 263–266.

Lovich, J. E., Ernst, C. H., Ernst, E. M., and Riley, J. E. (2014). A 21-year study of seasonal and interspecific variation of hatchling emergence in a Nearctic freshwater turtle community: to overwinter or not to overwinter? Herpetological Monographs 28, 93–109.
A 21-year study of seasonal and interspecific variation of hatchling emergence in a Nearctic freshwater turtle community: to overwinter or not to overwinter?Crossref | GoogleScholarGoogle Scholar |

McCooey, H. J. (1887). Notes on the method adopted by the female of the common freshwater tortoise, Chelodina longicollis in the excavation of the burrows in which her eggs are to be deposited. Proceedings of the Linnean Society of New South Wales 2, 107–108.
Notes on the method adopted by the female of the common freshwater tortoise, Chelodina longicollis in the excavation of the burrows in which her eggs are to be deposited.Crossref | GoogleScholarGoogle Scholar |

Moll, E. O., and Legler, J. M. (1971). The life history of a neotropical slider turtle, Pseudemys scripta (Schoepff), in Panama. Bulletin of the Los Angeles County Museum of Natural History Science , 1–102.

Nagle, R. D., Burke, V. J., and Congdon, J. D. (1998). Egg components and hatchling lipid reserves: parental investment in kinosternid turtles from the southeastern United States. Comparative Biochemistry and Physiology B: Comparative Biochemistry 120, 145–152.
Egg components and hatchling lipid reserves: parental investment in kinosternid turtles from the southeastern United States.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M%2FgsVSmsw%3D%3D&md5=b28e1e4e7e61f7ec1a8af50a50967be8CAS |

Nagle, R. D., Kinney, O. M., Congdon, J. D., and Beck, C. W. (2000). Winter survivorship of hatchling painted turtles (Chrysemys picta) in Michigan. Canadian Journal of Zoology 78, 226–233.
Winter survivorship of hatchling painted turtles (Chrysemys picta) in Michigan.Crossref | GoogleScholarGoogle Scholar |

Nagle, R. D., Plummer, M. V., Congdon, J. D., and Fischer, R. U. (2003). Parental investment, embryo growth, and hatchling lipid reserves in softshell turtles (Apalone mutica) from Arkansas. Herpetologica 59, 145–154.
Parental investment, embryo growth, and hatchling lipid reserves in softshell turtles (Apalone mutica) from Arkansas.Crossref | GoogleScholarGoogle Scholar |

Nagle, R. D., Lutz, C. L., and Pyle, A. L. (2004). Overwintering in the nest by hatchling map turtles (Graptemys geographica). Canadian Journal of Zoology 82, 1211–1218.
Overwintering in the nest by hatchling map turtles (Graptemys geographica).Crossref | GoogleScholarGoogle Scholar |

Obbard, M. E., and Brooks, R. J. (1981). Fate of overwintered clutches of the common snapping turtle (Chelydra serpentina) in Algonquin Park, Ontario. Canadian Field-Naturalist 95, 350–352.

Packard, G. C. (1997). Temperatures during winter in nests with hatchling painted turtles (Chrysemys picta). Herpetologica 53, 89–95.

Packard, G. C., and Packard, M. J. (2004). To freeze or not to freeze: adaptations for overwintering by hatchlings of the North American painted turtle. The Journal of Experimental Biology 207, 2897–2906.
To freeze or not to freeze: adaptations for overwintering by hatchlings of the North American painted turtle.Crossref | GoogleScholarGoogle Scholar |

Packard, G. C., Fasano, S. L., Attaway, M. B., Lohmiller, L. D., and Lynch, T. L. (1997a). Thermal environment for overwintering hatchlings of the painted turtle (Chrysemys picta). Canadian Journal of Zoology 75, 401–406.
Thermal environment for overwintering hatchlings of the painted turtle (Chrysemys picta).Crossref | GoogleScholarGoogle Scholar |

Packard, G. C., Tucker, J. K., Nicholson, D., and Packard, M. J. (1997b). Cold tolerance in hatchling slider turtles (Trachemys scripta). Copeia 1997, 339–345.
Cold tolerance in hatchling slider turtles (Trachemys scripta).Crossref | GoogleScholarGoogle Scholar |

Packard, G. C., Packard, M. J., Lang, J. W., and Tucker, J. K. (1999). Tolerance for freezing in hatchling turtles. Journal of Herpetology 33, 536–543.
Tolerance for freezing in hatchling turtles.Crossref | GoogleScholarGoogle Scholar |

Packard, G. C., Packard, M. J., and Lang, J. W. (2000). Why hatchling Blanding’s turtles don’t overwinter inside their nest. Herpetologica 56, 367–374.

Parmenter, C. J. (1976). The natural history of the Australian freshwater turtle Chelodina longicollis Shaw (Testudinata, Chelidae). Ph.D. Thesis, University of New England, Armidale.

Parmenter, C. J. (1985). Reproduction and survivorship of Chelodina longicollis (Testudinata: Chelidae). In ‘Biology of Australasian Frogs and Reptiles’. (Eds G. Grigg, R. Shine, and H. Ehmann.) pp. 53–61. (Royal Zoological Society of New South Wales: Sydney.)

Paterson, J. E., Steinberg, B. D., and Litzgus, J. D. (2012). Revealing a cryptic life-history stage: differences in habitat selection and survivorship between hatchlings of two turtle species at risk (Glyptemys insculpta and Emydoidea blandingii). Wildlife Research 39, 408–418.
Revealing a cryptic life-history stage: differences in habitat selection and survivorship between hatchlings of two turtle species at risk (Glyptemys insculpta and Emydoidea blandingii).Crossref | GoogleScholarGoogle Scholar |

Paterson, J. E., Steinberg, B. D., and Litzgus, J. D. (2014). Effects of body size, habitat selection and exposure on hatchling turtle survival. Journal of Zoology 294, 278–285.
Effects of body size, habitat selection and exposure on hatchling turtle survival.Crossref | GoogleScholarGoogle Scholar |

Reese, S. A., Ultsch, G. R., and Jackson, D. C. (2004). Lactate accumulation, glycogen depletion, and shell composition of hatchling turtles during simulated aquatic hibernation. The Journal of Experimental Biology 207, 2889–2895.
Lactate accumulation, glycogen depletion, and shell composition of hatchling turtles during simulated aquatic hibernation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnslSrs7k%3D&md5=198d1b1b8303cdc88ddf6f228d87d106CAS |

Riley, J. L., and Litzgus, J. D. (2014). Cues used by predators to detect freshwater turtle nests may persist late into incubation. Canadian Field-Naturalist 128, 179–188.
Cues used by predators to detect freshwater turtle nests may persist late into incubation.Crossref | GoogleScholarGoogle Scholar |

Riley, J. L., Tattersall, G. J., and Litzgus, J. D. (2014). Potential sources of intra-population variation in the overwintering strategy of painted turtle (Chrysemys picta) hatchlings. The Journal of Experimental Biology 217, 4174–4183.
Potential sources of intra-population variation in the overwintering strategy of painted turtle (Chrysemys picta) hatchlings.Crossref | GoogleScholarGoogle Scholar |

Robley, A., Howard, K., Lindeman, M., Cameron, R., Jardine, A., and Hiscock, D. (2016). The effectiveness of short-term fox control in protecting a seasonally vulnerable species, the eastern long-necked turtle (Chelodina longicollis). Ecological Management & Restoration 17, 63–69.
The effectiveness of short-term fox control in protecting a seasonally vulnerable species, the eastern long-necked turtle (Chelodina longicollis).Crossref | GoogleScholarGoogle Scholar |

Roe, J. H., Georges, A., and Green, B. (2008). Energy and water flux during terrestrial estivation and overland movement in a freshwater turtle. Physiological and Biochemical Zoology 81, 570–583.
Energy and water flux during terrestrial estivation and overland movement in a freshwater turtle.Crossref | GoogleScholarGoogle Scholar |

Rowe, J. W., Holy, L., Ballinger, R. E., and Stanley-Samuelson, D. (1995). Lipid provisioning of turtle eggs and hatchlings: total lipid, phospholipid, triacylglycerol and triacylglycerol fatty acids. Comparative Biochemistry and Physiology B: Comparative Biochemistry 112, 323–330.
Lipid provisioning of turtle eggs and hatchlings: total lipid, phospholipid, triacylglycerol and triacylglycerol fatty acids.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK28%2FktlamsQ%3D%3D&md5=3d1a8e6ec0ff89a7d2876e43a022f5a6CAS |

Rubinsky, B., Hong, J. S., and Storey, K. B. (1994). Freeze tolerance in turtles: visual analysis by microscopy and magnetic resonance imaging. The American Journal of Physiology 267, R1078–R1088.
| 1:CAS:528:DyaK2MXhvFWgtbo%3D&md5=07b4934de981efbc593953c94bb5af66CAS |

Rusli, M. U., and Booth, D. T. (2016). Bigger clutch sizes save offspring energy during nest escapes. Behavioral Ecology and Sociobiology 70, 607–616.
Bigger clutch sizes save offspring energy during nest escapes.Crossref | GoogleScholarGoogle Scholar |

Sims, P. A., Packard, G. C., and Chapman, P. L. (2001). The adaptive strategy for overwintering by hatchling snapping turtles (Chelydra serpentina). Journal of Herpetology 35, 514–517.
The adaptive strategy for overwintering by hatchling snapping turtles (Chelydra serpentina).Crossref | GoogleScholarGoogle Scholar |

Spencer, R.-J. (2002). Experimentally testing nest site selection: fitness trade-offs and predation risk in turtles. Ecology 83, 2136–2144.
Experimentally testing nest site selection: fitness trade-offs and predation risk in turtles.Crossref | GoogleScholarGoogle Scholar |

Spencer, R.-J., and Thompson, M. B. (2005). Experimental analysis of the impact of foxes on freshwater turtle populations. Conservation Biology 19, 845–854.
Experimental analysis of the impact of foxes on freshwater turtle populations.Crossref | GoogleScholarGoogle Scholar |

St Clair, R. C., and Gregory, P. T. (1990). Factors affecting the northern range limit of painted turtles (Chrysemys picta): winter acidosis or freezing? Copeia 1990, 1083–1089.
Factors affecting the northern range limit of painted turtles (Chrysemys picta): winter acidosis or freezing?Crossref | GoogleScholarGoogle Scholar |

Storey, K. B., Storey, J. M., Brooks, S. P. J., Churchill, T. A., and Brooks, R. J. (1988). Hatchling turtles survive freezing during winter hibernation. Proceedings of the National Academy of Sciences of the United States of America 85, 8350–8354.
Hatchling turtles survive freezing during winter hibernation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkvFyh&md5=744f288cbb0d3de9d778e96bccd5b099CAS |

Thompson, M. B. (1983). Populations of the Murray River tortoise, Emydura (Chelodina): the effect of egg predation by the red fox, Vulpes vulpes. Australian Wildlife Research 10, 363–371.
Populations of the Murray River tortoise, Emydura (Chelodina): the effect of egg predation by the red fox, Vulpes vulpes.Crossref | GoogleScholarGoogle Scholar |

Tucker, J. K., and Packard, G. C. (1998). Overwinter survival by hatchling sliders (Trachemys scripta) in west-central Illinois. Journal of Herpetology 32, 431–434.
Overwinter survival by hatchling sliders (Trachemys scripta) in west-central Illinois.Crossref | GoogleScholarGoogle Scholar |

Tucker, J. K., and Paukstis, G. L. (1999). Post-hatching substrate moisture and overwintering hatchling turtles. Journal of Herpetology 33, 608–615.
Post-hatching substrate moisture and overwintering hatchling turtles.Crossref | GoogleScholarGoogle Scholar |

Tucker, J. K., Filoramo, N. I., Paukstis, G. L., and Janzen, F. J. (1998). Residual yolk in captive and wild-caught hatchlings of the red-eared slider turtle (Trachemys scripta elegans). Copeia 1998, 488–492.
Residual yolk in captive and wild-caught hatchlings of the red-eared slider turtle (Trachemys scripta elegans).Crossref | GoogleScholarGoogle Scholar |

Vestjens, W. J. M. (1969). Nesting, egg-laying and hatching of the snake-necked tortoise at Canberra, A.C.T. Australian Zoologist 15, 141–149.

Walde, A. D., Bider, J. R., Masse, D., Saumure, R. A., and Titman, R. D. (2007). Nesting ecology and hatching success of the wood turtle, Glyptemys insculpta, in Quebec. Herpetological Conservation and Biology 2, 49–60.

Weisrock, D. W., and Janzen, F. J. (1999). Thermal and fitness-related consequences of nest location in painted turtles (Chrysemys picta). Functional Ecology 13, 94–101.
Thermal and fitness-related consequences of nest location in painted turtles (Chrysemys picta).Crossref | GoogleScholarGoogle Scholar |

Wilbur, H. M. (1975). The evolutionary and mathematical demography of the turtle Chrysemys picta. Ecology 56, 64–77.
The evolutionary and mathematical demography of the turtle Chrysemys picta.Crossref | GoogleScholarGoogle Scholar |

Willette, D. A. S., Tucker, J. K., and Janzen, F. J. (2005). Linking climate and physiology at the population level for a key life-history stage of turtles. Canadian Journal of Zoology 83, 845–850.
Linking climate and physiology at the population level for a key life-history stage of turtles.Crossref | GoogleScholarGoogle Scholar |