Optimising the hatching success of artificially incubated eggs for use in a conservation program for the western saw-shelled turtle (Myuchelys bellii)
Louise M. Streeting A * , Deborah S. Bower A , Martin L. Dillon A B , Phil Spark C , Michael Gough D , Adam Skidmore E , Paul G. McDonald A , Hannah Delaney A , Adrienne Burns A , Sandy Watson A , Duminda S. B. Dissanayake F , Arthur Georges F and Donald T. McKnight A GA School of Environmental and Rural Science, University of New England, Armidale, NSW 2350, Australia.
B Northern Tablelands Local Land Services, Armidale, NSW 2350, Australia.
C North West Ecological Services, Tamworth, NSW 2340, Australia.
D Latisternum, Dubbo, NSW 2830, Australia.
E Taronga Conservation Society Australia, Mosman, NSW 2088, Australia.
F Institute for Applied Ecology, University of Canberra, Canberra, ACT 2601, Australia.
G Department of Environment and Genetics, School of Agriculture, Biomedicine and Environment, La Trobe University, Wodonga, Vic. 3690, Australia.
Australian Journal of Zoology 70(2) 74-82 https://doi.org/10.1071/ZO22014
Submitted: 30 March 2022 Accepted: 24 October 2022 Published: 9 December 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Artificial incubation of eggs and the release of hatchlings into the wild is a common conservation intervention designed to augment threatened turtle populations. We investigate a range of incubation temperatures to establish an optimal temperature for maximum hatching success of western saw-shelled turtle (Myuchelys bellii) eggs. We report on the influence of incubation temperature on incubation duration and hatching success and describe two experimental incubation methods which, for the same incubation temperature (27°C), resulted in 77% and 97% hatching success, respectively. Eggs were incubated at constant temperatures (27°C, 28°C and 29°C) to determine the influence of temperature on incubation period, hatchling morphology and external residual yolk. Incubation duration was negatively correlated with incubation temperature. We report on the morphology of eggs and hatchlings and show that their dimensions are positively correlated with maternal adult size and mass. A constant incubation temperature of 27°C produced the highest hatching success and smallest external residual yolk on hatching and is therefore recommended for incubation of eggs for population reinforcement programs. Our study is the first to optimise artificial incubation procedures for M. bellii and will be a valuable resource for M. bellii and other threatened freshwater turtle conservation initiatives.
Keywords: artificial incubation, Bell’s turtle, conservation, endangered species, freshwater turtle, head-starting, population augmentation, population reinforcement, wildlife management.
References
Bates, D, Mächler, M, Bolker, B, and Walker, S (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.| Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |
Bennett, AM, Steiner, J, Carstairs, S, Gielens, A, and Davy, CM (2017). A question of scale: replication and the effective evaluation of conservation interventions. Facets 2, 892–909.
| A question of scale: replication and the effective evaluation of conservation interventions.Crossref | GoogleScholarGoogle Scholar |
Birchard GF (2004) Effects of incubation temperature. In ‘Reptilian incubation: environment, evolution and behaviour’. (Ed. DC Deeming) pp. 103–123. (Nottingham University Press: Nottingham)
Booth, DT (1998). Effects of incubation temperature on the energetics of embryonic development and hatchling morphology in the Brisbane river turtle Emydura signata. Journal of Comparative Physiology B 168, 399–404.
| Effects of incubation temperature on the energetics of embryonic development and hatchling morphology in the Brisbane river turtle Emydura signata.Crossref | GoogleScholarGoogle Scholar |
Booth, DT (2000). Incubation of eggs of the Australian broad-shelled turtle, Chelodina expansa (Testudinata: Chelidae), at different temperatures: effects on pattern of oxygen consumption and hatchling morphology. Australian Journal of Zoology 48, 369–378.
| Incubation of eggs of the Australian broad-shelled turtle, Chelodina expansa (Testudinata: Chelidae), at different temperatures: effects on pattern of oxygen consumption and hatchling morphology.Crossref | GoogleScholarGoogle Scholar |
Booth, DT (2002). Incubation of rigid-shelled turtle eggs: do hydric conditions matter? Journal of Comparative Physiology B 172, 627–633.
| Incubation of rigid-shelled turtle eggs: do hydric conditions matter?Crossref | GoogleScholarGoogle Scholar |
Booth, DT (2006). Influence of incubation temperature on hatchling phenotype in reptiles. Physiological and Biochemical Zoology 79, 274–281.
| Influence of incubation temperature on hatchling phenotype in reptiles.Crossref | GoogleScholarGoogle Scholar |
Booth, DT (2014). Longer incubation periods are energetically costly for turtle embryos. Annual Research & Review in Biology 4, 2931–2937.
| Longer incubation periods are energetically costly for turtle embryos.Crossref | GoogleScholarGoogle Scholar |
Booth, DT (2018). Incubation temperature induced phenotypic plasticity in oviparous reptiles: Where to next? Journal of Experimental Zoology Part A: Ecological and Integrative Physiology 329, 343–350.
| Incubation temperature induced phenotypic plasticity in oviparous reptiles: Where to next?Crossref | GoogleScholarGoogle Scholar |
Booth, DT, and Yu, CY (2009). Influence of the hydric environment on water exchange and hatchlings of rigid-shelled turtle eggs. Physiological and Biochemical Zoology 82, 382–387.
| Influence of the hydric environment on water exchange and hatchlings of rigid-shelled turtle eggs.Crossref | GoogleScholarGoogle Scholar |
Bower, DS, Hodges, KM, and Georges, A (2013). Salinity of incubation media influences embryonic development of a freshwater turtle. Journal of Comparative Physiology B 183, 235–241.
| Salinity of incubation media influences embryonic development of a freshwater turtle.Crossref | GoogleScholarGoogle Scholar |
Burke, RL (2015). Head-starting turtles: learning from experience. Herpetological Conservation and Biology 10, 299–308.
Cann J (1998) ‘Freshwater turtles of Australia.’ (Beaumont Publishing: Singapore)
Carstairs, S, Paterson, JE, Jager, KL, Gasbarrini, D, Mui, AB, and Davy, CM (2019). Population reinforcement accelerates subadult recruitment rates in an endangered freshwater turtle. Animal Conservation 22, 589–599.
| Population reinforcement accelerates subadult recruitment rates in an endangered freshwater turtle.Crossref | GoogleScholarGoogle Scholar |
Chessman, BC (2015). Distribution, abundance and population structure of the threatened western saw-shelled turtle, Myuchelys bellii, in New South Wales, Australia. Australian Journal of Zoology 63, 245–252.
| Distribution, abundance and population structure of the threatened western saw-shelled turtle, Myuchelys bellii, in New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |
Congdon, JD, and Gibbons, JW (1987). Morphological constraint on egg size: a challenge to optimal egg size theory? Proceedings of the National Academy of Sciences of the United States of America 84, 4145–4147.
| Morphological constraint on egg size: a challenge to optimal egg size theory?Crossref | GoogleScholarGoogle Scholar |
Congdon, JD, Fischer, RU, and Gatten, RE (1995). Effects of incubation temperatures on characteristics of hatchling American alligators. Herpetologica 51, 497–504.
Dissanayake, DSB, Streeting, LM, Georges, A, and Bower, DS (2022). A male-specific sex marker for the endangered western sawshelled turtle (Myuchelys bellii) using in silico whole-genome subtraction. Conservation Genetics Resources 14, 231–236.
| A male-specific sex marker for the endangered western sawshelled turtle (Myuchelys bellii) using in silico whole-genome subtraction.Crossref | GoogleScholarGoogle Scholar |
Eiby, YA, and Booth, DT (2011). Determining optimal incubation temperature for a head-start program: the effect of incubation temperature on hatchling Burnett River snapping turtles (Elseya albagula). Australian Journal of Zoology 59, 18–25.
| Determining optimal incubation temperature for a head-start program: the effect of incubation temperature on hatchling Burnett River snapping turtles (Elseya albagula).Crossref | GoogleScholarGoogle Scholar |
Fielder, DP, Limpus, DJ, and Limpus, CJ (2014). Reproduction and population ecology of the vulnerable western sawshelled turtle, Myuchelys bellii, in the Murray–Darling Basin, Australia. Australian Journal of Zoology 62, 463–476.
| Reproduction and population ecology of the vulnerable western sawshelled turtle, Myuchelys bellii, in the Murray–Darling Basin, Australia.Crossref | GoogleScholarGoogle Scholar |
Fielder D, Chessman B, Georges A (2015) Myuchelys bellii (Gray 1844) – Western Saw-shelled Turtle, Bell’s Turtle. In ‘Conservation biology of freshwater turtles and tortoises: a compilation project of the IUCN/SSC tortoise and freshwater turtle specialist group’. Chelonian research monographs, vol. 5. (Eds AGJ Rhodin, PCH Pritchard, PP van Dijk, RA Saumure, KA Buhlmann, JB Iverson, RA Mittermeier) pp. 088.1–088.7. (IUCN SSC) https://doi.org/10.3854/crm.5.088.bellii.v1.2015
Fox J, Weisberg S (2011) ‘An R companion to applied regression.’ 2nd edn (Sage: Thousand Oaks, California)
Georges, A (1988). Sex determination is independent of incubation temperature in another chelid turtle, Chelodina longicollis. Copeia 1988, 248–254.
| Sex determination is independent of incubation temperature in another chelid turtle, Chelodina longicollis.Crossref | GoogleScholarGoogle Scholar |
Georges, A, and McInnes, S (1998). Temperature fails to influence hatchling sex in another genus and species of chelid turtle, Elusor macrurus. Journal of Herpetology 32, 596–598.
| Temperature fails to influence hatchling sex in another genus and species of chelid turtle, Elusor macrurus.Crossref | GoogleScholarGoogle Scholar |
Heppell, SS, Crowder, LB, and Crouse, DT (1996). Models to evaluate headstarting as a management tool for long-lived turtles. Ecological Applications 6, 556–565.
| Models to evaluate headstarting as a management tool for long-lived turtles.Crossref | GoogleScholarGoogle Scholar |
Hothorn, T, Bretz, F, and Westfall, P (2008). Simultaneous inference in general parametric models. Biometrical Journal 50, 346–363.
| Simultaneous inference in general parametric models.Crossref | GoogleScholarGoogle Scholar |
IUCN (2021) The IUCN Red List of Threatened Species. Version 2021-3. Available at https://www.iucnredlist.org [Accessed 13 March 2022]
Iverson, JB, Lindeman, PV, and Lovich, JE (2019). Understanding reproductive allometry in turtles: a slippery “slope”. Ecology and Evolution 9, 11891–11903.
| Understanding reproductive allometry in turtles: a slippery “slope”.Crossref | GoogleScholarGoogle Scholar |
Janzen, FJ (1993). An experimental analysis of natural selection on body size of hatchling turtles. Ecology 74, 332–341.
| An experimental analysis of natural selection on body size of hatchling turtles.Crossref | GoogleScholarGoogle Scholar |
Kennett R, Roe J, Hodges K, Georges A (2009) Chelodina longicollis (Shaw 1794) – eastern long-necked turtle, common longnecked 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’. Chelonian research monographs, vol. 5 (Eds AGJ Rhodin, PCH Pritchard, PP van Dijk, RA Saumure, KA Buhlmann, JB Iverson, RA Mittermeier) pp. 031.1–031.8. (IUCN SSC)
Lawson, L, and Rollinson, N (2021). A simple model for the evolution of temperature-dependent sex determination explains the temperature sensitivity of embryonic mortality in imperiled reptiles. Conservation Physiology 9, coab020.
| A simple model for the evolution of temperature-dependent sex determination explains the temperature sensitivity of embryonic mortality in imperiled reptiles.Crossref | GoogleScholarGoogle Scholar |
Limpus, CJ, Baker, V, and Miller, JD (1979). Movement induced mortality of loggerhead eggs. Herpetologica 35, 335–338.
Martinez, PA, Ezaz, T, Valenzuela, N, Georges, A, and Marshall Graves, JA (2008). An XX/XY heteromorphic sex chromosome system in the Australian chelid turtle Emydura macquarii: a new piece in the puzzle of sex chromosome evolution in turtles. Chromosome Research 16, 815–825.
| An XX/XY heteromorphic sex chromosome system in the Australian chelid turtle Emydura macquarii: a new piece in the puzzle of sex chromosome evolution in turtles.Crossref | GoogleScholarGoogle Scholar |
Mazzoleni, S, Augstenová, B, Clemente, L, Auer, M, Fritz, U, Praschag, P, Protiva, T, Velenský, P, Kratochvíl, L, and Rovatsos, M (2020). Sex is determined by XX/XY sex chromosomes in Australasian side-necked turtles (Testudines: Chelidae). Scientific Reports 10, 4276.
| Sex is determined by XX/XY sex chromosomes in Australasian side-necked turtles (Testudines: Chelidae).Crossref | GoogleScholarGoogle Scholar |
McCosker, JR (2002). Chelodina expansa (broad shell river turtle) and Emydura signata (Brisbane shortneck turtle) reproduction. Herpetological Review 33, 189–199.
McKnight, DT, Hollender, EC, Howell, HJ, Carr, JL, Buhlmann, KA, and Ligon, DB (2018). Egg and clutch sizes of western chicken turtles (Deirochelys reticularia miaria). Acta Herpetologica 13, 191–194.
| Egg and clutch sizes of western chicken turtles (Deirochelys reticularia miaria).Crossref | GoogleScholarGoogle Scholar |
Micheli-Campbell, MA, Campbell, HA, Cramp, RL, Booth, DT, and Franklin, CE (2011). Staying cool, keeping strong: incubation temperature affects performance in a freshwater turtle. Journal of Zoology 285, 266–273.
| Staying cool, keeping strong: incubation temperature affects performance in a freshwater turtle.Crossref | GoogleScholarGoogle Scholar |
Nelson, NJ, Thompson, MB, Pledger, S, Keall, SN, and Daugherty, CH (2004). Egg mass determines hatchling size, and incubation temperature influences post-hatching growth, of tuatara Sphenodon punctatus. Journal of Zoology 263, 77–87.
| Egg mass determines hatchling size, and incubation temperature influences post-hatching growth, of tuatara Sphenodon punctatus.Crossref | GoogleScholarGoogle Scholar |
Niehaus, AC, Angilletta, MJ, Sears, MW, Franklin, CE, and Wilson, RS (2012). Predicting the physiological performance of ectotherms in fluctuating thermal environments. Journal of Experimental Biology 215, 694–701.
| Predicting the physiological performance of ectotherms in fluctuating thermal environments.Crossref | GoogleScholarGoogle Scholar |
Noble, DWA, Stenhouse, V, and Schwanz, LE (2018). Developmental temperatures and phenotypic plasticity in reptiles: a systematic review and meta-analysis. Biological Reviews 93, 72–97.
| Developmental temperatures and phenotypic plasticity in reptiles: a systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar |
Packard, GC, Taigen, TL, Packard, MJ, and Boardman, TJ (1981). Changes in mass of eggs of softshell turtles (Trionyx spiniferus) incubated under hydric conditions simulating those of natural nests. Journal of Zoology 193, 81–90.
| Changes in mass of eggs of softshell turtles (Trionyx spiniferus) incubated under hydric conditions simulating those of natural nests.Crossref | GoogleScholarGoogle Scholar |
Packard, GC, Packard, MJ, Miller, K, and Boardman, TJ (1987). Influence of moisture, temperature, and substrate on snapping turtle eggs and embryos. Ecology 68, 983–993.
| Influence of moisture, temperature, and substrate on snapping turtle eggs and embryos.Crossref | GoogleScholarGoogle Scholar |
Páez, VP, Lipman, A, Bock, BC, and Heppell, SS (2015). A plea to redirect and evaluate conservation programs for South America’s podocnemidid river turtles. Chelonian Conservation and Biology 14, 205–216.
| A plea to redirect and evaluate conservation programs for South America’s podocnemidid river turtles.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2018) ‘R: A language and environment for statistical computing (Version 3.5.0).’ R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/ [Accessed 5 March 2021]
Reichling, SB, and Gutzke, WHN (1996). Phenotypic consequences of incubation environment in the African elapid genus Aspidelaps. Zoo Biology 15, 301–308.
| Phenotypic consequences of incubation environment in the African elapid genus Aspidelaps.Crossref | GoogleScholarGoogle Scholar |
Santori, C, Spencer, R-J, Thompson, MB, Whittington, CM, and Van Dyke, JU (2021). Hatchling short-necked turtles (Emydura macquarii) select aquatic vegetation habitats, but not after one month in captivity. Aquatic Ecology 55, 85–96.
| Hatchling short-necked turtles (Emydura macquarii) select aquatic vegetation habitats, but not after one month in captivity.Crossref | GoogleScholarGoogle Scholar |
Seigel RA, Dodd CK Jr (2000) Manipulation of turtle populations for conservation: halfway technologies or viable options? In ‘Turtle conservation’. (Ed. MW Klemmens) pp. 218–238 (Smithsonian Institution Press: Washington, DC)
Spencer, R-J, Van Dyke, JU, and Thompson, MB (2017). Critically evaluating best management practices for preventing freshwater turtle extinctions. Conservation Biology 31, 1340–1349.
| Critically evaluating best management practices for preventing freshwater turtle extinctions.Crossref | GoogleScholarGoogle Scholar |
Streeting LM, Spark PD, Nesbitt B, Nesbitt J, Baker L, Dillon ML (2021) ‘Bell’s turtle nest protection guidelines.’ (Local Land Services: New South Wales)
Streeting LM, Bower DS, Dillon ML, Spark P, Gough M, Skidmore A, McDonald PG, Delaney H, Burns A, Watson S, Dissanayake DSB, Georges A, McKnight DT (2022) Data for: Optimising the hatching success of artificially incubated eggs for use in a conservation program for the western saw-shelled turtle (Myuchelys bellii). Dryad, Dataset. https://doi.org/10.5061/dryad.0cfxpnw69
Thompson, MB (1983). Populations of the Murray River tortoise, Emydura (Chelodina): the effect of egg predation by the red fox, Vulpes vulpes. 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 |
Thompson MB (1985) Functional significance of the opaque white patch in eggs of Emydura macquarii. In ‘Biology of Australasian frogs and reptiles’. (Eds G Grigg, R Shine, HE Ehmann) pp. 387–395. (Australian Zoological Society of New South Wales: Sydney)
Thompson, MB (1988). Influence of incubation temperature and water potential on sex determination in Emydura macquarii (Testudines: Pleurodira). Herpetologica 44, 86–90.
Turtle Taxonomy Working Group [Rhodin AGJ, Iverson JB, Bour R, Fritz U, Georges A, Shaffer HB, van Dijk PP] (2021) Turtles of the world: annotated checklist and atlas of taxonomy, synonymy, distribution, and conservation status. In ‘Conservation biology of freshwater turtles and tortoises: a compilation project of the IUCN/SSC tortoise and freshwater turtle specialist group. 9th edn. Chelonian research monographs, vol. 8. (Eds AGJ Rhodin, JB Iverson, PP van Dijk, CB Stanford, EV Goode, KA Buhlmann, RA Mittermeier) pp. 1–472. (IUCN SSC) Available at https://doi.org/10.3854/crm.8.checklist.atlas.v9.2021
Van Dyke, JU, Ferronato, BDO, and Spencer, R-J (2018). Current conservation status of Australian freshwater turtles. Australian Journal of Zoology 66, 1–3.
| Current conservation status of Australian freshwater turtles.Crossref | GoogleScholarGoogle Scholar |
Van Dyke, JU, Spencer, R-J, Thompson, MB, Chessman, B, Howard, K, and Georges, A (2019). Conservation implications of turtle declines in Australia’s Murray River system. Scientific Reports 9, 1998.
| Conservation implications of turtle declines in Australia’s Murray River system.Crossref | GoogleScholarGoogle Scholar |
Venables WN, Ripley BD (2002) ‘Modern applied statistics with S.’ 4th edn. (Springer: New York)
Warner DA (2011) Chapter 1 – Sex determination in reptiles. In ‘Hormones and reproduction of vertebrates: reptiles’. vol. 3 (Eds DO Norris, KH Lopez) pp. 1–38. (Academic Press: Amsterdam)