Abstract
Hatchling turtles typically emerge from underground nests in groups, so the nest escape process may represent another example of animals sharing a task (in this case, digging out of a nest) to save on individual energy expenditure. Previous studies have reported the energetic cost of embryonic development across chelonian taxa, but none has quantified the extra amount of energy needed to escape the nest. Brisbane river turtle (Emydura macquarii signata) hatchlings were found to fuel this activity by using approximately 50 % of their residual yolk energy content. An open-flow respirometry system was used to quantify the effect of clutch size on an individual’s energetic cost while digging out of the nest. The energetic cost of nest escaping 15 cm upward in the fine moist sand was calculated to be between 0.34 and 2.32 kJ per individual depending upon the number of hatchlings digging together. The energetic cost decreased as the number of individuals digging together increased and thus supports the ‘social facilitation’ hypothesis which suggests hatchlings cooperate to share the workload of digging out of the nest amongst clutch mates to reduce individual energy expenditure. The reduced energetic cost associated with large cohorts was chiefly caused by the shorter time taken to dig out of the nest by larger numbers of individuals. We conclude that synchronous digging activity of many individuals during nest escape evolved not only to facilitate quicker nest emergence but also reduce the energetic cost to individuals.
Similar content being viewed by others
References
Baldwin J, Gyuris E, Mortimer K, Patak A (1989) Anaerobic metabolism during dispersal of green and loggerhead turtle hatchlings. Comp Biochem Physiol A 94:663–665
Bennett JM, Taplin LE, Grigg GC (1986) Sea water drinking as a homeostatic response to dehydration in hatchling loggerhead turtles Caretta caretta. Comp Biochem Physiol A 83:507–513
Booth DT (1998a) Egg size, clutch size, and reproductive effort of the Australian broad-shelled river turtle, Chelodina expansa. J Herpetol 32:592–596
Booth DT (1998b) Effects of incubation temperature on the energetics of embryonic development and hatchling morphology in the Brisbane river turtle Emydura signata. J Comp Physiol B 168:399–404
Booth DT (1999) Size, water and energy content of eggs of the freshwater turtles, Emydura signata and Chelodina expansa. Proc Linnean Soc NSW 1999:53–59
Booth DT (2003) Composition and energy density of eggs from two species of freshwater turtle with twofold ranges in egg size. Comp Biochem Physiol A 134:129–137
Booth DT (2010) The natural history of nesting in two Australian freshwater turtles. Aust Zool 35:198–203
Booth DT, Astill K (2001) Incubation temperature, energy expenditure and hatchling size in the green turtle (Chelonia mydas), a species with temperature-sensitive sex determination. Aust J Zool 49:389–396
Bustard HR (1967) Mechanism of nocturnal emergence from the nest in green turtle hatchlings. Nature 214:317
Bustard HR (1972) Sea turtles: natural history and conservation. Collins, London
Carr A, Hirth H (1961) Social facilitation in green turtle siblings. Anim Behav 9:68–70
Carr A, Ogren L (1959) The ecology and migrations of sea turtles, 3 Dermochelys in Costa Rica. Am Mus Novit 1958:1–29
Clusella Trullas S, Spotila JR, Paladino FV (2006) Energetics during hatchling dispersal of the olive ridley turtle Lepidochelys olivacea using doubly labeled water. Physiol Biochem Zool 79:389–399
Dehn M (1990) Vigilance for predators: detection and dilution effects. Behav Ecol Sociobiol 26:337–342
Dial BE (1987) Energetics and performance during nest emergence and the hatchling frenzy in loggerhead sea turtles (Caretta caretta). Herpetol Leag 43:07–15
Doody JS (2011) Environmentally cued hatching in reptiles. Integr Comp Biol 51:49–61
Dorgan KM (2015) The biomechanics of burrowing and boring. J Exp Biol 218:176–183
Ebensperger LA, Bozinovic F (2000) Energetics and burrowing behaviour in the semifossorial degu Octodon degus (Rodentia: Octodontidae). J Zool Lond 252:179–186
Eftimie R, de Vries G, Lewis MA (2007) Complex spatial group patterns result from different animal communication mechanisms. Proc Natl Acad Sci USA 104:6974–6979
Fish FE (1995) Kinematics of ducklings swimming in formation: consequences of position. J Exp Zool 273:1–11
Gilbert C, Blanc S, Le Maho Y, Ancel A (2008) Energy saving processes in huddling emperor penguins: from experiments to theory. J Exp Biol 211:1–8
Gilbert C, McCafferty D, Le Maho Y, Martrette JM, Giroud S, Blanc S, Ancel A (2010) One for all and all for one: the energetic benefits of huddling in endotherms. Biol Rev 85:545–569
Hamann M, Jessop TS, Schäuble CS (2007) Fuel use and corticosterone dynamics in hatchling green sea turtles (Chelonia mydas) during natal dispersal. J Exp Mar Biol Ecol 353:13–21
Hansell M (1993) The ecological impact of animal nests and burrows. Funct Ecol 7:5–12
Hays GC, Speakman JR, Hayes JP (1992) The pattern of emergence by loggerhead turtle (Caretta caretta) hatchlings on Cephalonia, Greece. Herpetologica 48:396–401
Horrocks JA, Scott NM (1991) Nest site location and nest success in the Hawksbill turtle Eretmochelys imbricata in Barbados West-Indies. Mar Ecol Prog Ser 69:1–8
Houghton JDR, Hays GC (2001) Asynchronous emergence by loggerhead turtle (Caretta caretta) hatchlings. Naturwissenschaften 88:133–136
Koch AU, Guinea ML, Whiting SD (2007) Effects of sand erosion and current harvest practices on incubation of the flatback sea turtle (Natator depressus). Aust J Zool 55:97–105
Kraemer J, Bennett S (1981) Utilization of posthatching yolk in loggerhead sea turtles, Caretta caretta. Copeia 1981:406–411
Lighton JRB (2008) Measuring metabolic rates: a manual for scientists. Oxford University Press, New York
Lovegrove B (1989) The cost of burrowing by the social mole rats (Bathyergidae) Cryptomys damarensis and Heterocephalus glaber: the role of soil moisture. Physiol Zool 62:449–469
Moran K, Bjorndal K, Bolten A (1999) Effects of the thermal environment on the temporal pattern of emergence of hatchling loggerhead turtles Caretta caretta. Mar Ecol Prog Ser 189:251–261
Mrosovsky N (1968) Nocturnal emergence of hatchling sea turtles: control by thermal inhibition of activity. Nature 220:1338–1339
Pereira CM, Booth DT, Bradley AJ, Limpus CJ (2012) Blood concentrations of lactate, glucose and corticosterone in dispersing hatchling sea turtles. Biol Open 2:63–67
Pignati M, Fernandes L, Miorando P, Pezzuti J (2013) Hatching and emergence patterns in the yellow-spotted river turtle, Podocnemis unifilis (Testudines: Podocnemididae), in the Várzea floodplains of the lower Amazon River. Chelonian Conserv Biol 12:127–133
Salmon M, Reising M (2014) Emergence rhythms of hatchling marine turtles: is a time sense involved? Chelonian Conserv Biol 13:282–285
Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment, 5th edn. Cambridge University Press, Cambridge
Seymour RS (1973) Physiological correlates of forced activity and burrowing in the spadefoot toad, Scaphiopus hammondii. Copeia 1973:103–115
Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108:499
Speake BK, Thompson MB (2000) Lipids of the eggs and neonates of oviparous and viviparous lizards. Comp Biochem Physiol A 127:453–467
Speake BK, Thompson MB, Thacker FE, Bedford GS (2003) Distribution of lipids from the yolk to the tissues during development of the water python (Liasis fuscus). J Comp Physiol B 173:541–547
Spencer RJ, Janzen FJ (2011) Hatching behavior in turtles. Integr Comp Biol 51:100–110
Spencer R, Thompson M, Banks P (2001) Hatch or wait? A dilemma in reptilian incubation. Oikos 93:401–406
Thompson M (1989) Patterns of metabolism in embryonic reptiles. Respir Physiol 76:243–256
Trenchard H, Ratamero E, Richardson A, Perc M (2015) A deceleration model for bicycle peloton dynamics and group sorting. Appl Math Comput 251:24–34
Triplett N (1899) The dynamogenic factors in pacemaking and competition. Am J Psychol 9:507–533
Voelkl B, Portugal SJ, Unsöld M, Usherwood JR, Wilson AM, Fritz J (2015) Matching times of leading and following suggest cooperation through direct reciprocity during V-formation flight in ibis. Proc Natl Acad Sci USA 112:201413589
Witherington B, Bjorndal K, McCabe C (1990) Temporal pattern of nocturnal emergence of loggerhead turtle hatchlings from natural nests. Copeia 1990:1165–1168
Withers PC (1992) Comparative animal physiology. Saunders College Publishing, New York
Withers PC, Jarvis JU (1980) The effect of huddling on thermoregulation and oxygen consumption for the naked mole-rat. Comp Biochem Physiol A 66:215–219
Zitterbart DP, Wienecke B, Butler JP, Fabry B (2011) Coordinated movements prevent jamming in an emperor penguin huddle. PLoS ONE 6:e20260
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
This study was approved by The University of Queensland Animal Ethics Committee (AEC approval number: AE02252), and eggs were collected under permit no: WISP12887113 granted by the Department of Environment and Heritage Protection, Queensland Government.
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Communicated by T. Madsen
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(WMV 9482 kb)
Rights and permissions
About this article
Cite this article
Rusli, M.U., Booth, D.T. Bigger clutch sizes save offspring energy during nest escapes. Behav Ecol Sociobiol 70, 607–616 (2016). https://doi.org/10.1007/s00265-016-2079-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-016-2079-1