, Volume 190, Issue 3, pp 511–522 | Cite as

Anthropogenic nest sites provide warmer incubation environments than natural nest sites in a population of oviparous reptiles near their northern range limit

  • Elizabeth Ann FrancisEmail author
  • Patrick D. Moldowan
  • Megan A. Greischar
  • Njal Rollinson
Highlighted Student Research


Oviposition site choice affects a host of offspring phenotypes and directly impacts maternal fitness. Recent evidence suggests that oviparous reptiles often select nest sites where the landscape has been altered by anthropogenic activity, whereas natural nest sites are less often used. We leverage a long-term study of snapping turtle (Chelydra serpentina) to identify natural nest sites and anthropogenic nest sites and to compare habitat variables among nest site types. Natural and anthropogenic nest sites did not differ in average canopy closure, distance to nearest water, substrate composition, or aspect. However, anthropogenic nest sites had less ground-level vegetation and greater soil brightness, and were 3.3 °C warmer than natural nests during incubation. We used the Schoolfield model of poikilotherm development to assess differences in development rate between natural and anthropogenic nests. Because of the difference in temperature, embryos in anthropogenic nests were predicted to have undergone nearly twice as much development as embryos in natural nests during incubation. We outline why the evolution of fast embryonic development rate cannot compensate indefinitely for the low temperature incubation regimes that become increasingly prevalent at northern range margins, thereby underlining why maternal nest site choice of relatively warm anthropogenic sites may help oviparous reptiles persist in thermally constrained environments. Future research should aim to quantify both the thermal benefits of anthropogenic nest sites, as well as associated fitness costs (e.g., increased adult mortality) to elucidate whether anthropogenic disturbance of the landscape can be an ecological trap or serve a net benefit to some reptiles in northern environments.


Chelydra serpentina Ecological trap Embryonic development Nest microhabitat Thermal performance 



We would like to thank Jacqueline D. Litzgus and Ronald J. Brooks for collaborative use of long-term study site and system; Algonquin Park/Ontario Parks for permission to conduct research; and Algonquin Wildlife Research Station for field accommodation; Nicole Brunet, Taylor Wynia, and Steven Kell for assistance in the field; Lin Schwarzkopf and one anonymous reviewer for helpful comments that improved this paper. All applicable institutional and national guidelines for the care and use of animals were followed.

Author contribution statement

PDM conceived and designed the experiment. EAF and PDM conducted fieldwork. EAF, MAG, and NR analyzed the data. EAF, PDM, MAG, and NR wrote the manuscript.


We acknowledge and thank the University of Toronto Faculty of Arts and Science Research Excursion Program, an NSERC Discovery Grant (# 2016-06469) to NR, a postdoctoral fellowship from the University of Toronto Department of Ecology and Evolutionary Biology to MAG, and Algonquin Park/Ontario Parks for funding that supported this research.

Compliance with ethical standards

Conflict of interest

All authors declare no conflict of interest.

Supplementary material

442_2019_4383_MOESM1_ESM.docx (105 kb)
Supplementary material 1 (DOCX 104 kb)


  1. Amarasekare P, Johnson C (2017) Evolution of thermal reaction norms in seasonally varying environments. Am Nat 189:E31–E45. CrossRefGoogle Scholar
  2. Andrews RM, Mathies T (2000) Natural history of reptilian development: constraints on the evolution of viviparity. Bioscience 50:227–238.;2 CrossRefGoogle Scholar
  3. Angilletta MJ Jr (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, OxfordCrossRefGoogle Scholar
  4. Ardia D, Mullen KM, Peterson BG, Ulrich J (2016) ‘DEoptim’: differential evolution in ‘R’, version 2.2-4Google Scholar
  5. Beaudry F, deMaynadier PG, Hunter ML Jr (2010) Nesting movements and the use of anthropogenic nesting sites by spotted turtles (Clemmys guttata) and Blanding’s turtles (Emydoidea blandingii). Herpetol Conserv Biol 5:1–8Google Scholar
  6. Bernardo J (1996) The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. Am Zool 36:216–236. CrossRefGoogle Scholar
  7. Bleakney S (1958a) A zoogeographic study of the amphibians and reptiles of eastern Canada. Natl Mus Can 155:1–119Google Scholar
  8. Bleakney S (1958b) Postglacial dispersal of the turtle Chrysemys picta. Herpetologica 14:101–104Google Scholar
  9. Bobyn ML, Brooks RJ (1994) Incubation conditions as potential factors limiting the northern distribution of snapping turtles, Chelydra serpentina. Can J Zool 72:28–37. CrossRefGoogle Scholar
  10. Booth DT, Burgess E, McCosker J, Lanyon JM (2004) The influence of incubation temperature on post-hatching fitness characteristics of turtles. Int Congr Ser 1275:226–233. CrossRefGoogle Scholar
  11. Bowne DR, Cosentino BJ, Anderson LJ, Bloch CP, Cooke S, Crumrine PW, Dallas J, Doran A, Dosch JJ, Druckenbrod DL, Durtsche RD, Garneau D, Genet KS, Fredericksen TS, Kish PA, Kolozsvary MB, Kuserk FT, Londquist ES, Mankiewicz C, March JG, Muir TJ, Murray KG, Santulli MN, Sicignano FJ, Smallwood PD, Urban RA, Winnett-Murray K, Zimmermann CR (2018) Effects of urbanization on the population structure of freshwater turtles across the United States. Conserv Biol. Google Scholar
  12. Brooks RJ (2007) Do reptiles in Canada have a future? An overview of the constraints on conserving Canadian snakes, turtles, and lizards. In: Seburn CNL, Bishop CA (eds) Ecology, conservation, and status of reptiles in canada. Herpetological Conservation Series Number Two. Society for the Study of Amphibians and Reptiles, Salt Lake City, pp 183–190Google Scholar
  13. Brooks RJ, Galbraith DA, Nancekivell EG, Bishop CA (1988) Developing management guidelines for snapping turtles. In: Szaro RC, Severson KE, Patton DR (eds). Symposium on management of amphibians, reptiles, and small mammals in North America (July 19–21, 1988), USDA Forest Service General Technical Report RM–166. Flagstaff, pp 174–179Google Scholar
  14. Brooks RJ, Brown GP, Galbraith DA (1991) Effects of a sudden increase in natural mortality of adults on a population of the common snapping turtle (Chelydra serpentina). Can J Zool 69:1314–1320. CrossRefGoogle Scholar
  15. Buhlmann KL, Osborn CP (2011) Use of an artificial nesting mound by wood turtles (Glyptemys insculpta): a tool for turtle conservation. Northeast Nat 18(3):315–334. CrossRefGoogle Scholar
  16. Bull JJ, Vogt RC (1979) Temperature-dependent sex determination in turtles. Science 206:1186–1188. CrossRefGoogle Scholar
  17. Congdon JD, Gibbons JW (1985) Egg components and reproductive characteristics of turtles: relationships to body size. Herpetologica 41:194–205Google Scholar
  18. Congdon JD, Dunham AE, van Loben Sels RC (1993) Delayed sexual maturity and demographics of Blanding’s turtles (Emydoidea blandingii): implications for conservation and management of long-lived organisms. Conserv Biol 7:826–833. CrossRefGoogle Scholar
  19. Congdon JD, Dunham AE, van Loben Sels RC (1994) Demographics of common snapping turtles (Chelydra serpentina): implications for conservation and management of long-lived organisms. Am Zool 34:397–408CrossRefGoogle Scholar
  20. de Solla SR, Gugelyk JA (2018) Oviposition and subsequent depredation of snapping turtle (Chelydra serpentina) nests in fresh asphalt. Can Field Nat 132(2):103–107. CrossRefGoogle Scholar
  21. Edge CB, Rollinson N, Brooks RJ, Congdon JD, Iverson JB, Janzen FJ, Litzgus JD (2017) Phenotypic plasticity of nest timing in a post-glacial landscape: how do reptiles adapt to seasonal time constraints? Ecology 98:512–524. CrossRefGoogle Scholar
  22. Ernst CH, Lovich JE (2009) Turtles of the United States and Canada, 2nd edn. Johns Hopkins University Press, BaltimoreGoogle Scholar
  23. Ewert MA (1985) Embryology of turtles. In: Gans C, Maderson PFA, Billett F (eds) Biology of the reptilia (v 14). Wiley-Interscience, New York, pp 75–267Google Scholar
  24. Ewert MA, Lang JW, Nelson CE (2005) Geographic variation in the pattern of temperature-dependent sex determination in the American snapping turtle (Chelydra serpentina). J Zool Lond 265:81–95. CrossRefGoogle Scholar
  25. Gilchrist GW (1995) Specialists and generalists in changing environments. I. Fitness landscapes of thermal sensitivity. Am Nat 146:252–270CrossRefGoogle Scholar
  26. Hale R, Swearer SE (2016) Ecological traps: current evidence and future directions. Proc R Soc B 283:20152647. CrossRefGoogle Scholar
  27. Haxton T (2000) Road mortality of snapping turtles, Chelydra serpentina, in central Ontario during their nesting period. Can Field Nat 114:106–110Google Scholar
  28. Heppel SS (1998) Application of life-history theory and population model analysis to turtle conservation. Copeia 1998:367–375. CrossRefGoogle Scholar
  29. Holman JA, Andrews KD (1994) North American quaternary cold-tolerant turtles: distributional adaptations and constraints. Boreas 23:44–52. CrossRefGoogle Scholar
  30. Hughes EJ, Brooks RJ (2006) The good mother: does nest-site selection constitute parental investment in turtles? Can J Zool 84:1545–1554. CrossRefGoogle Scholar
  31. Janzen FJ (1994) Vegetational cover predicts the sex-ratio of hatchling turtles in natural nests. Ecology 75:1593–1599. CrossRefGoogle Scholar
  32. Janzen FJ, Morjan CL (2001) Repeatability of microenvironment-specific nesting behaviour in a turtle with environmental sex determination. Anim Behav 62:73–82. CrossRefGoogle Scholar
  33. Joyal LA, McCollough M, Hunter ML Jr (2001) Landscape ecology approaches to wetland species conservation: a case study of two turtle species in southern Maine. Cons Biol 15:1755–1762. CrossRefGoogle Scholar
  34. Juliana JR, Bowden RM, Janzen FJ (2004) The impact of behavioral and physiological maternal effects on offspring sex ratio in the common snapping turtle, Chelydra serpentina. Behav Ecol Sociobiol 56:270–278. CrossRefGoogle Scholar
  35. Kearney M, Porter WP (2004) Mapping the fundamental niche: physiology, climate, and the distribution of a nocturnal lizard. Ecology 85:3119–3131. CrossRefGoogle Scholar
  36. Keevil MG, Brooks RJ, Litzgus JD (2018) Post-catastrophe patterns of abundance and survival reveal no evidence of population recovery in a long-lived animal. Ecosphere 9(9):e02396. CrossRefGoogle Scholar
  37. Kolbe JJ, Janzen FJ (2002) Impact of nest-site selection on nest success and nest temperature in natural and disturbed habitats. Ecology 83:269–281.;2 CrossRefGoogle Scholar
  38. Lapointe J (2018) Chelydra serpentina (snapping turtle) nesting range expansion. Herpetol Rev 49:316–317Google Scholar
  39. Lesbarrères D, Ashpole SL, Bishop CA, Blouin-Demers G, Brooks RJ, Echaubard P, Govindarajulu P, Green DM, Hecnar SJ, Herman T, Houlahan J, Litzgus JD, Mazerolle MJ, Paszkowski CA, Rutherford P, Schock DM, Storey KB, Lougheed SC (2014) Conservation of herpetofauna in northern landscapes: threats and challenges from a Canadian perspective. Biol Cons 170:48–55. CrossRefGoogle Scholar
  40. Loncke DJ, Obbard ME (1977) Tag success, dimensions, clutch size and nesting site fidelity for the snapping turtle, Chelydra serpentina (Reptilia, Testudines, Chelydridae) in Algonquin Park, Ontario, Canada. J Herpetol 11:243–244CrossRefGoogle Scholar
  41. Martin TL, Huey RB (2008) Why suboptimal is optimal: jensen’s inequality and ectotherm thermal preferences. Am Nat 171:E102–E118. CrossRefGoogle Scholar
  42. Mesquita DO, Costa GC, Colli GR, Costa TB, Shepard DB, Vitt LJ, Pianka ER (2016) Life-history patterns of lizards of the world. Am Nat 187:689–705. CrossRefGoogle Scholar
  43. Midwood JD, Cairns NA, Stoot LJ, Cooke SJ, Blouin-Demers G (2015) Bycatch mortality can cause extirpation in four freshwater turtle species. Aquat Cons Mar Freshw Ecosyst 25:71–80. CrossRefGoogle Scholar
  44. Mitchell TS, Warner DA, Janzen FJ (2013) Phenotypic and fitness consequences of maternal nest-site choice across multiple early life stages. Ecology 94:336–345. CrossRefGoogle Scholar
  45. Obbard ME, Brooks RJ (1980) Nesting migrations of the snapping turtle (Chelydra serpentina). Herpetologica 36:158–162Google Scholar
  46. Obbard ME, Brooks RJ (1981) Fate of overwintered clutches of the common snapping turtle (Chelydra serpentina) in Algonquin Park, Ontario. Can Field Nat 95:350–352Google Scholar
  47. Paterson JE, Steinberg BD, Litzgus JD (2013) Not just any old pile of dirt: evaluating the use of artificial nesting mounds as conservation tools for freshwater turtles. Oryx 47:607–615. CrossRefGoogle Scholar
  48. Price KV, Storn RM, Lampinen JA (2006) Differential evolution—a practical approach to global optimization. Springer, New YorkGoogle Scholar
  49. Quinn DP, Kaylor SM, Norton TM, Buhlmann KA (2015) Nesting mounds with protective boxes and an electric wire as tools to mitigate diamond-backed terrapin (Malaclemmys terrapin) nest predation. Herpetol Cons Biol 10(3):969–977Google Scholar
  50. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. R version 3.4.4 and 3.5.0Google Scholar
  51. Refsnider JM, Janzen FJ (2010) Putting eggs in one basket: ecological and evolutionary hypotheses for variation in oviposition-site choice. Annu Rev Ecol Evol Syst 41:39–57. CrossRefGoogle Scholar
  52. Richter-Boix A, Katzenberger M, Duarte H, Quintela M, Tejedo M, Laurila A (2015) Local divergence of thermal reaction norms among amphibian populations is affected by pond temperature variation. Evol 69:2210–2226. CrossRefGoogle Scholar
  53. Riley JR, Litzgus JD (2013) Evaluation of predator-exclusion cages used in turtle conservation: cost analysis and effects on nest environment and proxies of hatchling fitness. Wildl Res 40:499–511. CrossRefGoogle Scholar
  54. Riley JR, Freedberg S, Litzgus JD (2014) Incubation temperature in the wild influences hatchling phenotype of two freshwater turtle species. Evol Ecol Res 16:397–416Google Scholar
  55. Rollinson N, Hutchings JA (2013) Environmental quality predicts optimal egg size in the wild. Am Nat 182:76–90. CrossRefGoogle Scholar
  56. Rollinson N, Holt SM, Massey MD, Holt RC, Nancekivell EG, Brooks RJ (2018) A new method of estimating thermal performance of embryonic development rate yields accurate prediction of embryonic age in wild reptile nests. J Therm Biol 74:187–194. CrossRefGoogle Scholar
  57. Schoolfield RM, Sharpe PJH, Magnuson CE (1981) Non-linear regression of biological temperature-dependent rate models based on absolute reaction rate theory. J Theor Biol 88:719–731. CrossRefGoogle Scholar
  58. Telemeco RS, Gangloff EJ, Cordero GA, Mitchell TS, Bodensteiner BL, Holden KG, Mitchell SM, Polich RL, Janzen FJ (2016) Reptile embryos lack the opportunity to thermoregulate by moving within the egg. Am Nat 188:E13. CrossRefGoogle Scholar
  59. Thompson MM, Coe BH, Congdon JD, Stauffer DF, Hopkins WA (2017) Nesting ecology and habitat use of Chelydra serpentina in an area modified by agricultural and industrial activity. Herpetol Cons Biol 12:292–306Google Scholar
  60. Valenzuela N (2001) Constant, shift, and natural temperature effects on sex determination in Podocnemis expansa turtles. Ecology 82:3010–3024.;2 CrossRefGoogle Scholar
  61. Vickers MJ, Aubret F, Coulon A (2017) Using GAMM to examine inter-individual heterogeneity in thermal performance curves for Natrix natrix indicates bet hedging strategy by mothers. J Therm Biol 63:16–23. CrossRefGoogle Scholar
  62. Wilson DS (1998) Nest-site selection: microhabitat variation and its effects on the survival of turtle embryos. Ecology 79:1884–1892.;2 CrossRefGoogle Scholar
  63. Yntema CL (1976) Effects of incubation temperatures on sexual differentiation in the turtle, Chelydra serpentina. J Morph 150:453–462. CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of TorontoTorontoCanada

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