Advertisement

Oecologia

pp 1–14 | Cite as

Ontogenetic shifts in the nesting behaviour of female crocodiles

  • Cameron J. Baker
  • Craig E. Franklin
  • Hamish A. Campbell
  • Terri R. Irwin
  • Ross G. DwyerEmail author
Behavioral ecology – original research

Abstract

Body size and age are crucial factors influencing reproductive capacity and success. As females grow, their reproductive investment and success often increase due to improved overall physiological condition and experience gained through successive reproductive events. While much of this work has been conducted on birds and mammals, surprisingly little is known on how body size affects nesting decisions in other long-lived vertebrates. We monitored the movements and nesting behaviour of 57 wild female estuarine crocodiles Crocodylus porosus over a 10-year period (and across consecutive nesting seasons) using externally mounted satellite tags, implanted acoustic transmitters and a network of submerged acoustic receivers. Applying Hidden Markov models to the telemetry-derived location data revealed that female nesting behaviours could be split into three distinct states: (i) ranging movements within home ranges and at nesting sites; (ii) migrations to and from nesting sites; (iii) and nesting/nest guarding. We found that during migration events, larger females migrated further and remained away from dry season territories for longer periods than smaller individuals. Furthermore, not only were migratory movements stimulated by increases in rainfall, larger females migrated to nest sites at lower rainfall thresholds than smaller females. We provide some of the first evidence of body size influencing nesting decisions in an ectothermic vertebrate, with shifts likely resulting from an increased willingness to invest in nest protection among larger and more experienced females.

Keywords

Estuarine crocodile Hidden Markov modelling Nest-site selection Parental investment Telemetry 

Notes

Acknowledgements

This study was supported by the Australian Research Council linkage scheme with Australia Zoo and CSIRO as industry partners. We thank Australia Zoo staff for their aid in the capture and tagging process and Gordon C. Grigg for his reviews of the manuscript. All procedures were carried out with approval from The University of Queensland Animal Ethics Committee (SIB/302/08/ARC, SBS/204/11/ARC/AUST ZOO (NF), SBS/215/14/AUST ZOO/ARC) and Queensland Environment Protection Agency Permits (WISP00993703, WISP05268508, WISP13189313).

Author contribution statement

CB, RD, HC and CF conceived the ideas and designed methodology; All authors collected the data; CB and RD led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Funding

Funder: Australian Research Council-Linkage Grant, grant number: LP140100222.

Supplementary material

442_2019_4382_MOESM1_ESM.pdf (305 kb)
Supplementary material 1 (PDF 304 kb)

References

  1. Alagaili A, Bennett NC, Mohammed O, Hart D (2017) The reproductive biology of the Ethiopian hedgehog, Paraechinus aethiopicus, from central Saudi Arabia: the role of rainfall and temperature. J Arid Environ 145:1–9CrossRefGoogle Scholar
  2. Angilletta MJ, Sears MW, Pringle RM (2009) Spatial dynamics of nesting behavior: lizards shift microhabitats to construct nests with beneficial thermal properties. Ecology 90:2933–2939CrossRefGoogle Scholar
  3. Barneche DR, Robertson DR, White CR, Marshall DJ (2018) Fish reproductive-energy output increases disproportionately with body size. Science 360:642–645CrossRefGoogle Scholar
  4. Bartón K (2018) MuMIn: multi-model inference. R package version 1.42.1. https://CRAN.R-project.org/package=MuMIn
  5. Bekoff M, Diamond J, Mitton JB (1981) Life-history patterns and sociality in canids: body size, reproduction, and behavior. Oecologia 50:386–390CrossRefGoogle Scholar
  6. Bowen KD, Spencer R-J, Janzen FJ (2005) A comparative study of environmental factors that affect nesting in Australian and North American freshwater turtles. J Zool 267:397–404CrossRefGoogle Scholar
  7. Brien ML, Read MA, McCallum HI, Grigg GC (2008) Home range and movements of radio-tracked estuarine crocodiles (Crocodylus porosus) within a non-tidal waterhole. Wildl Res 35:140–149CrossRefGoogle Scholar
  8. Briggs-Gonzalez V, Bonenfant C, Basille M, Cherkiss MS, Beauchamp JS, Mazzotti FJ (2017) Life histories and conservation of long-lived reptiles, an illustration with the American crocodile (Crocodylus acutus). J Anim Ecol 68:1102–1113.  https://doi.org/10.1111/1365-2656.12723 CrossRefGoogle Scholar
  9. Broussard DR, Stephen Dobson F, Murie J (2008) Previous experience and reproductive investment of female Columbian ground squirrels. J Mamm 89:145–152CrossRefGoogle Scholar
  10. Burnham KP, Anderson DR (2002) model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  11. Campbell HA et al (2010) Estuarine crocodiles ride surface currents to facilitate long-distance travel. J Anim Ecol 79:955–964CrossRefGoogle Scholar
  12. Campbell HA, Watts ME, Dwyer RG, Franklin CE (2012) VTrack: software for analysing and visualising animal movement from acoustic telemetry detections. Mar Freshw Res 63:815–820CrossRefGoogle Scholar
  13. Campbell HA, Dwyer RG, Irwin TR, Franklin CE (2013) Home range utilisation and long-range movement of estuarine crocodiles during the breeding and nesting season. PLoS One 8:e62127CrossRefGoogle Scholar
  14. Combrink X, Warner KK, Downs CT (2017) Nest-site selection, nesting behaviour and spatial ecology of female Nile crocodiles (Crocodylus niloticus) in South Africa. Behav Proc 137:101–112CrossRefGoogle Scholar
  15. Curio E (1983) Why do young birds reproduce less well? Ibis 125:400–404CrossRefGoogle Scholar
  16. Dean B et al (2012) Behavioural mapping of a pelagic seabird: combining multiple sensors and a hidden Markov model reveals the distribution of at-sea behaviour. J R Soc Interface 10:20120570CrossRefGoogle Scholar
  17. Dwyer RG et al (2015a) An open web-based system for the analysis and sharing of animal tracking data. Anim Biotelem 3:1CrossRefGoogle Scholar
  18. Dwyer RG, Campbell HA, Irwin TR, Franklin CE (2015b) Does the telemetry technology matter? Comparing estimates of aquatic animal space-use generated from GPS-based and passive acoustic tracking. Mar Freshw Res 66:654–664CrossRefGoogle Scholar
  19. Elsey RM, Trosclair PL III, Glenn TC (2008) Nest-site fidelity in American alligators in a Louisiana coastal marsh. Southeast Nat 7:737–743CrossRefGoogle Scholar
  20. Forslund P, Pa̎rt T (1995) Age and reproduction in birds—hypotheses and tests. Trends Ecol Evol 10:374–378CrossRefGoogle Scholar
  21. Franklin CE, Read MA, Kraft PG, Liebsch N, Irwin SR, Campbell HA (2009) Remote monitoring of crocodilians: implantation, attatchment and release methods for transmitters and data-loggers. Mar Freshw Res 60:284–292CrossRefGoogle Scholar
  22. Fukuda Y, Saalfeld K (2014) Abundance of saltwater crocodile hatchlings is related to rainfall in the preceding wet season in Northen Australia. Herpetologica 40:439–448CrossRefGoogle Scholar
  23. Grubeber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodal inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711.  https://doi.org/10.1111/j.1420-9101.2010.02210.x CrossRefGoogle Scholar
  24. 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 in estuarine crocodiles (Crocodylus porosus). Austral Ecol 40:275–286CrossRefGoogle Scholar
  25. Hipfner JM, Gaston AJ (2002) Growth of nestling thick-billed murres (Uria lomvia) in relation to parental experience and hatching date. Am Ornithol Soc 119:827–832Google Scholar
  26. Kay WR (2004) Movements and home ranges of radio-tracked Crocodylus porosus in the Cambridge Gulf region of Western Australia. Wildl Res 31:495–508CrossRefGoogle Scholar
  27. King RB, Stanford KM, Jones PC, Bekker K (2016) Size matters: individaul variation in ectotherm growth and asymptotic size. PLoS One 11:e0146299.  https://doi.org/10.1371/journal.pone.0146299 CrossRefGoogle Scholar
  28. Kozłowski J (1992) Optimal allocation of resources to growth and reproduction: implications for age and size at maturity. Trends Ecol Evol 7:15–19CrossRefGoogle Scholar
  29. Lazaridis E (2014) Lunar: lunar phase & distance, seasons and other environmental factors (version 0.1-04). https://statistics.lazaridis.eu (April 2018)
  30. Lyon B, Dwyer R, Pillans R, Campbell H, Franklin C (2017) Distribution, seasonal movements and habitat utilisation of an endangered shark, Glyphis glyphis, from northern Australia. Mar Ecol Prog Ser 573:203–213CrossRefGoogle Scholar
  31. Magnusson WE (1979) Incubation period of Crocodylus porosus. J Herpetol 13:362–363CrossRefGoogle Scholar
  32. Michelot T, Langrock R, Patterson TA (2016) moveHMM: an R package for the statistical modelling of animal movement data using hidden Markov models. Methods Ecol Evol 7:1308–1315CrossRefGoogle Scholar
  33. Monadjem A, Bamford AJ (2009) Influence of rainfall on timing and success of reproduction in Marabou Storks Leptoptilos crumeniferus. Ibis 151:344–351CrossRefGoogle Scholar
  34. Pärt T (2001) Experimental evidence of environmental effects on age–specific reproductive success: the importance of resource quality. Proc R Soc Lond B Biol Sci 268:2267–2271CrossRefGoogle Scholar
  35. Pettorelli N, Pelletier F, von Hardenberg A, Festa-Bianchet M, Côté SD (2007) Early onset of vegetation growth vs. rapid green-up: impacts on juvenile mountain ungulates. Ecology 88:381–390CrossRefGoogle Scholar
  36. Pfaller JB, Limpus CJ, Bjorndal KA (2009) Nest-site selection in individual loggerhead turtles and consequences for doomed-egg relocation. Conserv Biol 23:72–80CrossRefGoogle Scholar
  37. Pike DA (2008) Environmental correlates of nesting in loggerhead turtles, Caretta caretta. Anim Behav 76:603–610CrossRefGoogle Scholar
  38. Pinherio J, Bates D, DebRoy S, Sarkar D, R Core Team (2016) Package ‘nlme’: linear and nonlinear mixed effects models., 3.1-118 edn. R packageGoogle Scholar
  39. Ponsero A, Joly P (1998) Clutch size, egg survival and migration distance in the agile frog (Rana dalmatina) in a floodplain. Arch Hydrobiol 142:343–352CrossRefGoogle Scholar
  40. Pradel R, Choquet R, Béchet A (2012) Breeding experience might be a major determinant of breeding probability in long-lived species: the case of the greater flamingo. PLoS One 7:e51016.  https://doi.org/10.1371/journal.pone.0051016 CrossRefGoogle Scholar
  41. QDEH (1995) Conservation and Management of Crocodylus porosus in Queensland 1995–1997. Queensland Department of Environment and Heritage, BrisbaneGoogle Scholar
  42. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  43. Robertson RJ, Rendell WB (2001) A long-term study of reproductive performance in tree swallows: the influence of age and senescence on output. J Anim Ecol 70:1014–1031CrossRefGoogle Scholar
  44. Santangelo N (2015) Female breeding experience affects parental care strategies of both parents in a monogamous cichlid fish. Anim Behav 104:31–37CrossRefGoogle Scholar
  45. Schaper SV, Dawson A, Sharp PJ, Gienapp P, Caro SP, Visser ME (2012) Increasing temperature, not mean temperature, is a cue for avian timing of reproduction. Am Nat 179:E55–E69CrossRefGoogle Scholar
  46. Shine R (1989) Parental care in reptiles. In: Gans C, Huey RB (eds) Biology of the reptilia, vol 16. Ecology B: defense and life history. Brata Books, Ann Arbor, MI, pp 275–331Google Scholar
  47. Shine R, Charnov EL (1992) Patterns of survival, growth and maturation in snakes and lizards. Am Nat 139:1257–1269CrossRefGoogle Scholar
  48. Snyder RJ, Perdue BM, Zhang Z, Maple TL, Charlton BD (2016) Giant panda maternal care: a test of the experience constraint hypothesis. Sci Rep 6:27509.  https://doi.org/10.1038/srep27509 CrossRefGoogle Scholar
  49. Somaweera R, Brien ML, Shine R (2013) The role of predation in shaping crocodilian natural history. Herpetol Monogr 27:23–51.  https://doi.org/10.1655/HERPMONOGRAPHS-D-11-00001 CrossRefGoogle Scholar
  50. Stahler DR, MacNulty DR, Wayne RK, vonHoldt B, Smith DW (2013) The adaptive value of morphological, behavioural and life-history traits in reproductive female wolves. J Anim Ecol 82:222–234.  https://doi.org/10.1111/j.1365-2656.2012.02039.x CrossRefGoogle Scholar
  51. Taylor P, Li F, Holland A, Martin M, Rosenblatt AE (2016) Growth rates of black caiman (Melanosuchus niger) in the Rupununi region of Guyana. Amphibia-Reptilia 37:9–14.  https://doi.org/10.1163/15685381-00003024 CrossRefGoogle Scholar
  52. Tejedo M (1992) Effects of body size and timing of reproduction on reproductive success in female natterjack toads (Bufo calarnita). J Zool 228:545–555CrossRefGoogle Scholar
  53. Therrien J-F, Pinaud D, Gauthier G, Lecomte N, Bildstein KL, Bety J (2015) Is pre-breeding prospecting behaviour affected by snow cover in the irruptive snowy owl? A test using state-space modelling and environmental data annotated via Movebank. Mov Ecol 3:1CrossRefGoogle Scholar
  54. Thomas DW, Blondel J, Perret P, Lambrechts MM, Speakman JR (2001) Energetic and fitness costs of mismatching resource supply and demand in seasonally breeding birds. Science 291:2598–2600CrossRefGoogle Scholar
  55. Thorbjarnarson JB (1996) Reproductive characteristics of the order Crocodylia. Herpetologica 52:8–24Google Scholar
  56. Tibblin P, Forsman A, Borger T, Larsson P (2016) Causes and consequences of repeatability, flexibility and individual fine-tuning of migratory timing in pike. J Anim Ecol 85:136–145.  https://doi.org/10.1111/1365-2656.12439 CrossRefGoogle Scholar
  57. Tucker AD, Limpus CJ, McDonald KR, McCallum HI (2006) Growth dynamics of freshwater crocodiles (Crocodylus johnstoni) in the Lynd River, Queensland. Aust J Zool 54:409–415.  https://doi.org/10.1071/ZO06099 CrossRefGoogle Scholar
  58. Vandeperre F, Methven DA (2007) Do bigger fish arrive and spawn at the spawning grounds before smaller fish: cod (Gadus morhua) predation on beach spawning capelin (Mallotus villosus) from coastal Newfoundland. Estuar Coast Shelf Sci 71:391–400CrossRefGoogle Scholar
  59. Webb G, Manolis C (1989) Australian crocodiles a natural history. Reed New Holland, SydneyGoogle Scholar
  60. Webb G, Messel H, Magnusson WE (1977) The nesting of Crocodylus porosus in Arnhem land, Northern Australia. Copeia 1977:238–249CrossRefGoogle Scholar
  61. Whitehead PJ, Saalfeld K (2000) Nesting phenology of magpie geese (Anseranas semipalmata) in monsoonal northern Australia: responses to antecedent rainfall. J Zool 251:495–508CrossRefGoogle Scholar
  62. Wilkinson PM, Rhodes WE (1997) Growth rates of American Alligators in Coastal South Carolina. J Wildl Manag 61:397–402CrossRefGoogle Scholar
  63. Zhao Q, Xu M, Fränti P (2008) Knee point detection on bayesian information criterion tools with artificial intelligence, 2008. In: ICTAI’08. 20th ieee international conference on, vol. 2. IEEE, pp 431–438Google Scholar
  64. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) GLM and GAM for count data. Mixed effects models and extensions in ecology with R. Springer New York, New York, pp 209–243Google Scholar
  65. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14.  https://doi.org/10.1111/j.2041-210X.2009.00001.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.The School of Biological SciencesThe University of QueenslandBrisbaneAustralia
  2. 2.School of the EnvironmentCharles Darwin UniversityDarwinAustralia
  3. 3.Australia ZooBeerwahAustralia

Personalised recommendations