Survival of lizard eggs varies with microhabitat in the presence of an invertebrate nest predator

Abstract

The risk of nest depredation is influenced by numerous factors, including predator density, environmental conditions of the nesting landscape, and nesting behaviors of mothers. Many reptiles choose nest microhabitats that facilitate embryonic development, but little is known about how the risk of nest depredation in different habitats influences egg survival and nesting behavior. To address this knowledge gap, we quantified predator–prey relationships between square-back marsh crabs (Armases cinereum) and eggs of the brown anole lizard (Anolis sagrei). Our experiments aimed to answer the following questions: (1) are marsh crabs a predator of brown anole eggs, (2) does egg depredation differ among microhabitat types, and (3) how does crab density affect egg survival? We placed viable eggs in three different microhabitats used by nesting females (open area, palm frond, leaf litter), and manipulated the placement of the eggs as either buried or not buried. We also manipulated crab density in a field experiment. Our experiments confirmed square-back marsh crabs as egg predators, and eggs in the leaf litter or eggs buried were the least likely to be depredated. Additionally, eggs in leaf litter and under palm fronds escaped depredation longer than those in the open. Increased crab density also raised the risk of depredation for eggs placed under palm fronds or in open habitats. These results suggest that selection of nest sites by female brown anoles can influence offspring survival in the presence of marsh crabs, and the importance of nest site microhabitat choice may vary with predator density.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Data availability

The dataset generated during this study is available on the supplementary information files.

References

  1. Allen JD (2008) Size-specific predation on marine invertebrate larvae. Biol Bull 214:42–49. https://doi.org/10.2307/25066658

    Article  PubMed  Google Scholar 

  2. Andrén H (1995) Effects of landscape composition on predation rates at habitat edges. In: Hansson L, Fahrig L, Merriam G (eds) Mosaic landscapes and ecological processes. Springer, Netherlands, pp 225–255

    Google Scholar 

  3. Andrews RM (1988) Demographic correlates of variable egg survival for a tropical lizard. Oecologia 76:376–382. https://doi.org/10.1007/BF00377032

    Article  PubMed  Google Scholar 

  4. Bjorndal KA, Bolten AB, Chaloupka MY (2003) Survival probability estimates for immature green turtles Chelonia mydas in the Bahamas. Mar Ecol Prog Ser 252:273–281. https://doi.org/10.3354/meps252273

    Article  Google Scholar 

  5. Bohan DA, Bohan AC, Glen DM et al (2000) Spatial dynamics of predation by carabid beetles on slugs. J Anim Ecol 69:367–379. https://doi.org/10.1046/j.1365-2656.2000.00399.x

    Article  Google Scholar 

  6. Bro-Jorgensen J (2013) Evolution of sprint speed in African Savannah Herbivores in relation to predation. Evolution 67:3371–3376. https://doi.org/10.1111/evo.12233

    Article  PubMed  Google Scholar 

  7. Brown GE, Chivers DP (2005) Learning as an adaptive response to predation. In: Barbosa P, Castellanos I (eds) Ecology of predator-prey interactions. Oxford University Press, Oxford

    Google Scholar 

  8. Buck TL, Breed GA, Pennings SC et al (2003) Diet choice in an omnivorous salt-marsh crab: different food types, body size, and habitat complexity. J Exp Mar Biol Ecol 292:103–116. https://doi.org/10.1016/S0022-0981(03)00146-1

    Article  Google Scholar 

  9. Calsbeek R, Cox RM (2010) Experimentally assessing the relative importance of predation and competition as agents of selection. Nature 465:613–616. https://doi.org/10.1038/nature09020

    CAS  Article  PubMed  Google Scholar 

  10. Cates CD, Delaney DM, Buckelew AM et al (2014) Anolis sagrei (brown anole) egg predation. Herpetol Rev 45:491–492

    Google Scholar 

  11. Chalcraft DR, Andrews RM (1999) Predation on lizard eggs by ants: species interactions in a variable physical environment. Oecologia 119:285–292. https://doi.org/10.1007/s004420050788

    Article  PubMed  Google Scholar 

  12. Cockburn A (2006) Prevalence of different modes of parental care in birds. Proc R Soc B 273:1375–1383. https://doi.org/10.1098/rspb.2005.3458

    Article  PubMed  Google Scholar 

  13. Colombelli-Négrel D, Kleindorfer S (2009) Nest height, nest concealment, and predator type predict nest predation in superb fairy-wrens (Malurus cyaneus). Ecol Res 24:921–928. https://doi.org/10.1007/s11284-008-0569-y

    Article  Google Scholar 

  14. Crump ML (1996) Parental care among the amphibia. In: Rosenblatt JS, Snowdon CT (eds) Advances in the study of behavior. Academic Press, Cambridge, pp 109–144

    Google Scholar 

  15. Dawkins R, Krebs JR, Maynard Smith J, Holliday R (1979) Arms races between and within species. Proc R Soc B 205:489–511. https://doi.org/10.1098/rspb.1979.0081

    CAS  Article  Google Scholar 

  16. Delaney DM, Reedy AM, Mitchell TS et al (2013) Anolis sagrei (brown anole) nest-site choice. Herpetol Rev 44:314

    Google Scholar 

  17. Emmering QC, Schmidt KA (2011) Nesting songbirds assess spatial heterogeneity of predatory chipmunks by eavesdropping on their vocalizations. J Anim Ecol 80:1305–1312. https://doi.org/10.1111/j.1365-2656.2011.01869.x

    Article  PubMed  Google Scholar 

  18. Engeman RM, Martin RE, Smith HT et al (2005) Dramatic reduction in predation on marine turtle nests through improved predator monitoring and management. Oryx 39:318–326. https://doi.org/10.1017/S0030605305000876

    Article  Google Scholar 

  19. Engeman RM, Martin RE, Smith HT et al (2006) Impact on predation of sea turtle nests when predator control was removed midway through the nesting season. Wildl Res 33:187–192. https://doi.org/10.1071/WR05049

    Article  Google Scholar 

  20. Estes JA, Terborgh J, Brashares JS et al (2011) Trophic downgrading of planet Earth. Science 333:301–306. https://doi.org/10.1126/science.1205106

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Glob Ecol Biogeogr 16:265–280. https://doi.org/10.1111/j.1466-8238.2007.00287.x

    Article  Google Scholar 

  22. Fox J, Weisberg S (2019) An R Companion to Applied Regression. Third, Sage, Thousand Oaks (CA)

    Google Scholar 

  23. Gans C (1996) An overview of parental care among the reptilia. In: Rosenblatt JS, Snowdon CT (eds) Advances in the study of behavior. Academic Press, Cambridge, pp 145–157

    Google Scholar 

  24. Genovart M, Negre N, Tavecchia G et al (2010) The young, the weak and the sick: evidence of natural selection by predation. PLoS ONE 5:e9774. https://doi.org/10.1371/journal.pone.0009774

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Gill SA, Sealy SG (1996) Nest defense by yellow warblers: recognition of a brood parasite and an avian nest predator. Behaviour 133:263–282. https://doi.org/10.1163/156853996X00143

    Article  Google Scholar 

  26. Hall JM, Warner DA (2018) Thermal spikes from the urban heat island increase mortality and alter physiology of lizard embryos. J Exp Biol. https://doi.org/10.1242/jeb.181552

    Article  PubMed  Google Scholar 

  27. Hall JM, Buckelew A, Lovern M et al (2018) Seasonal shifts in reproduction depend on prey availability for an income breeder. Physiol Biochem Zool 91:1129–1147. https://doi.org/10.1086/700341

    Article  PubMed  Google Scholar 

  28. Hall JM, Mitchell TS, Thawley CJ, Stroud JT, Warner DA (2020) Adaptive seasonal shift towards investment in fewer, larger offspring: evidence from field and laboratory studies. J Anim Ecol 89:1242–1253. https://doi.org/10.1111/1365-2656.13182

    Article  PubMed  Google Scholar 

  29. Hill DA (1984) Population regulation in the mallard (Anas platyrhynchos). J Anim Ecol 53:191–202. https://doi.org/10.2307/4351

    Article  Google Scholar 

  30. Ho C-K, Pennings SC (2008) Consequences of omnivory for trophic interactions on a salt marsh shrub. Ecology 89:1714–1722. https://doi.org/10.1890/07-1069.1

    Article  PubMed  Google Scholar 

  31. Hulbert AC, Mitchell TS, Hall JM et al (2017) The effects of incubation temperature and experimental design on heart rates of lizard embryos. J Exp Zool A 327:466–476. https://doi.org/10.1002/jez.2135

    CAS  Article  Google Scholar 

  32. Husak JF (2006) Does speed help you survive? A test with Collared Lizards of different ages. Funct Ecol 20:174–179. https://doi.org/10.1111/j.1365-2435.2006.01069.x

    Article  Google Scholar 

  33. Kiskaddon E, Chernicky K, Bell S (2019) Resource use by and trophic variability of Armases cinereum (Crustacea, Brachyura) across human-impacted mangrove transition zones. PLoS ONE 14:e0212448. https://doi.org/10.1371/journal.pone.0212448

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Kuehne LM, Olden JD (2012) Prey naivety in the behavioural responses of juvenile Chinook salmon (Oncorhynchus tshawytscha) to an invasive predator. Freshwater Biol 57:1126–1137. https://doi.org/10.1111/j.1365-2427.2012.02776.x

    Article  Google Scholar 

  35. Lee J, Clayton D, Eisenstein S, Perez I (1989) The reproductive cycle of Anolis sagrei in southern Florida. Copeia. https://doi.org/10.2307/1445979

    Article  Google Scholar 

  36. Li S-R, Hao X, Wang Y et al (2018) Female lizards choose warm, moist nests that improve embryonic survivorship and offspring fitness. Funct Ecol 32:416–423. https://doi.org/10.1111/1365-2435.12995

    Article  Google Scholar 

  37. Losos JB, Schoener TW, Spiller DA (2004) Predator-induced behaviour shifts and natural selection in field-experimental lizard populations. Nature 432:505–508. https://doi.org/10.1038/nature03039

    CAS  Article  PubMed  Google Scholar 

  38. Nams VO (1997) Density-dependent predation by skunks using olfactory search images. Oecologia 110:440–448. https://doi.org/10.1007/s004420050179

    CAS  Article  PubMed  Google Scholar 

  39. O’Donoghue M, Boutin S, Krebs CJ, Hofer EJ (1997) Numerical responses of coyotes and lynx to the snowshoe hare cycle. Oikos 80:150–162. https://doi.org/10.2307/3546526

    Article  Google Scholar 

  40. O’Donoghue M, Boutin S, Krebs CJ et al (1998a) Behavioural responses of coyotes and lynx to the snowshoe hare cycle. Oikos 82:169–183. https://doi.org/10.2307/3546927

    Article  Google Scholar 

  41. O’Donoghue M, Boutin S, Krebs CJ et al (1998b) Functional responses of coyotes and lynx to the snowshoe hare cycle. Ecology 79:1193–1208. https://doi.org/10.2307/176736

    Article  Google Scholar 

  42. Packard GC, Packard MJ (1980) Evolution of the cleidoic egg among reptilian antecedents of birds. Integr Comp Biol 20:351–362. https://doi.org/10.1093/icb/20.2.351

    Article  Google Scholar 

  43. Pearson PR, Warner DA (2016) Habitat- and season-specific temperatures affect phenotypic development of hatchling lizards. Biol Lett 12:20160646. https://doi.org/10.1098/rsbl.2016.0646

    Article  PubMed  PubMed Central  Google Scholar 

  44. Pearson PR, Warner DA (2018) Early hatching enhances survival despite beneficial phenotypic effects of late-season developmental environments. Proc R Soc B 285:20180256. https://doi.org/10.1098/rspb.2018.0256

    Article  PubMed  Google Scholar 

  45. Pruett JE, Fargevieille A, Warner DA (2020) Temporal variation in maternal nest choice and its consequences on lizard embryos. Behav Ecol. https://doi.org/10.1093/beheco/araa032

    Article  Google Scholar 

  46. R Core Team (2020) R: a language and environment for statistical computing. Austria, Vienna

    Google Scholar 

  47. Reedy AM, Zaragoza D, Warner DA (2013) Maternally chosen nest sites positively affect multiple components of offspring fitness in a lizard. Behav Ecol 24:39–46. https://doi.org/10.1093/beheco/ars133

    Article  Google Scholar 

  48. 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. https://doi.org/10.1146/annurev-ecolsys-102209-144712

    Article  Google Scholar 

  49. Rosalino LM, Ferreira D, Leitão I, Santos-Reis M (2011) Selection of nest sites by wood mice Apodemus sylvaticus in a Mediterranean agro-forest landscape. Ecol Res 26:445–452. https://doi.org/10.1007/s11284-010-0797-9

    Article  Google Scholar 

  50. Schartel TE, Schauber EM (2016) Relative preference and localized food affect predator space use and consumption of incidental prey. PLoS ONE 11:e0151483. https://doi.org/10.1371/journal.pone.0151483

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. Schmidt KA (2003) Nest predation and population declines in Illinois songbirds: a case for mesopredator effects. Conserv Biol 17:1141–1150. https://doi.org/10.1046/j.1523-1739.2003.02316.x

    Article  Google Scholar 

  52. Schmidt KA, Whelan CJ (1999) The relative impacts of nest predation and brood parasitism on seasonal fecundity in songbirds. Conserv Biol 13:46–57. https://doi.org/10.1046/j.1523-1739.1999.97065.x

    Article  Google Scholar 

  53. Schnabel ZE (1938) The estimation of the total fish population of a lake. Am Math Monthly 45:348–352. https://doi.org/10.1080/00029890.1938.11990818

    Article  Google Scholar 

  54. Schoener TW, Schoener A (1980) Densities, sex ratios, and population structure in four species of Bahamian Anolis lizards. J Anim Ecol 49:19–53. https://doi.org/10.2307/4276

    Article  Google Scholar 

  55. Seip DR (1991) Predation and caribou populations. Rangifer. https://doi.org/10.7557/2.11.4.993

    Article  Google Scholar 

  56. Seiple W (1979) Distribution, habitat preferences and breeding periods in the crustaceans Sesarma cinereum and S. reticulatum (Brachyura: Decapoda: Grapsidae). Mar Biol 52:77–86. https://doi.org/10.1007/BF00386860

    Article  Google Scholar 

  57. Seiple W, Mueller B (1992) Patterns of refuge use by Sesarma cinereum (BOSC). Bull Mar Sci 50:158–164

    Google Scholar 

  58. Snyder WE, Evans EW (2006) Ecological effects of invasive arthropod generalist predators. Ann Rev Ecol Evol Syst 37:95–122. https://doi.org/10.1146/annurev.ecolsys.37.091305.110107

    Article  Google Scholar 

  59. Socci AM, Schlaepfer MA, Gavin TA (2005) The importance of soil moisture and leaf cover in a female lizard’s (Norops polylepis) evaluation of potential oviposition sites. Herpetologica 61:233–240. https://doi.org/10.1655/04-67.1

    Article  Google Scholar 

  60. Somaweera R, Brien M, Shine R (2013) The role of predation in shaping crocodilian natural istory. Herpetol Monogr 27:23–51. https://doi.org/10.1655/HERPMONOGRAPHS-D-11-00001

    Article  Google Scholar 

  61. Stoddard MC, Kupán K, Eyster HN et al (2016) Camouflage and clutch survival in plovers and terns. Sci Rep 6:1–11. https://doi.org/10.1038/srep32059

    CAS  Article  Google Scholar 

  62. Szura K, McKinney RA, Wigand C et al (2017) Burrowing and foraging activity of marsh crabs under different inundation regimes. J Exp Mar Biol Ecol 486:282–289. https://doi.org/10.1016/j.jembe.2016.10.029

    Article  Google Scholar 

  63. Teal JM (1958) Distribution of fiddler crabs in Georgia salt marshes. Ecology 39:185–193. https://doi.org/10.2307/1931862

    Article  Google Scholar 

  64. Thawley CJ, Langkilde T (2016) Invasive fire ants (Solenopsis invicta) predation of eastern fence lizard (Sceloporus undulatus) eggs. J Herpetol 50:284–288. https://doi.org/10.1670/15-017

    Article  Google Scholar 

  65. Tiatragul S, Hall JM, Pavlik NG, Warner DA (2019) Lizard nest environments differ between suburban and forest habitats. Biol J Linn Soc 126:392–403. https://doi.org/10.1093/biolinnean/bly204

    Article  Google Scholar 

  66. Tiatragul S, Hall JM, Warner DA (2020) Nestled in the city heat: urban nesting behavior enhances embryo development of an invasive lizard. J Urban Ecol. https://doi.org/10.1093/jue/juaa001

    Article  Google Scholar 

  67. Trumbo ST (2012) Patterns of parental care in invertebrates. In: Royle NJ, Smiseth PT, Kölliker M (eds) The Evolution of Parental Care. Oxford University Press, Oxford, pp 81–95

    Google Scholar 

  68. Venables WN, Ripley BD (2002) Modern Applied statistics with S., Fourth. Springer, Germany

    Google Scholar 

  69. Vucetich JA, Peterson RO, Schaefer CL (2002) The effect of prey and predator densities on wolf predation. Ecology 83:3003–3013

    Article  Google Scholar 

  70. Warkentin KM (2000) Wasp predation and wasp-induced hatching of red-eyed treefrog eggs. Anim Behav 60:503–510. https://doi.org/10.1006/anbe.2000.1508

    CAS  Article  PubMed  Google Scholar 

  71. Wilson DS (1998) Nest-site selection: microhabitat variation and its effects on the survival of turtle embryos. Ecology 79:1884–1892. https://doi.org/10.2307/176696

    Article  Google Scholar 

Download references

Acknowledgements

We thank J. Hall, J. Pruett, and S. Tiatragul for assistance in the lab and field. Thanks to the Warner and Wolak labs for comments on an earlier draft of this paper. Thanks to A. Wilson who made this Research Experience for Undergraduates Program possible. This study was supported by an NSF grant (DBI-1658694) and the Alabama Agricultural Experiment Station, and the Hatch program of the National Institute of Food and Agriculture, U.S. Department of Agriculture. This is publication #915 of the Auburn University Museum of Natural History.

Author information

Affiliations

Authors

Contributions

DW originally formulated the idea for this study, and all authors designed and performed the experiment. ADS and AF analyzed the data. The first draft of the manuscript was written by ADS and all authors contributed to subsequent versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Daniel A. Warner.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

This research followed the protocols approved by the Auburn University Animal Care and Use Committee (Protocol #: 2017–3027), and the Guana Tolomato Matanzas National Estuarine Research Reserve.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 35 kb)

Supplementary file2 (PDF 443 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

DeSana, A., Fargevieille, A. & Warner, D.A. Survival of lizard eggs varies with microhabitat in the presence of an invertebrate nest predator. Evol Ecol (2020). https://doi.org/10.1007/s10682-020-10058-w

Download citation

Keywords

  • Anolis sagrei
  • Armases cinereum
  • Egg predation
  • Nesting behavior
  • Nest-site choice