Advertisement

A multivariate approach to understanding shifts in escape strategies of urban lizards

  • Anuradha Batabyal
  • Shashank Balakrishna
  • Maria ThakerEmail author
Original Article

Abstract

Escape strategies of animals are economic decisions, expected to vary as a function of both intrinsic (e.g., performance ability) and extrinsic factors (e.g., level of threat and microhabitat). Anthropogenic disturbance, especially urbanization, changes a range of environmental factors including habitat characteristics and predation risk. As a consequence of differences in microhabitat structure and repeated exposure to anthropogenic disturbance, we hypothesize that animals in urban environments will be less risk averse than those in rural environments. Here, we examined the importance of extrinsic and intrinsic factors to understand the escape strategies of Psammophilus dorsalis across an urban-rural gradient. First, urban lizards used lower perches and chose refuges that were closer to their perches compared to rural lizards. Flight initiation distance (FID) of urban lizards in the field was shorter than that of rural lizards, but only for males. In response to a second attack, only rural males decreased their FIDs, whereas urban males showed low and invariable FIDs. Laboratory measures of sprint performance showed expected differences between the sexes, but no significant difference between urban and rural populations. Unlike the strong differences between males across habitats, escape strategies of females were similar in urban and rural areas, most likely because females generally rely on crypsis to minimize predation risk and are resistant to flee when approached. In sum, urban lizards have access to a more complex structural environment, with greater perch and refuge options, and have habituated to non-lethal anthropogenic disturbance. These extrinsic and intrinsic factors combine to result in lower risk aversion and may explain the ability to tolerate urban environments.

Significance statement

Rapid urbanization is at its peak globally, and many animals are forced to adjust to the associated environmental changes or face local extinction. Some species, however, seem to persist in urban areas, and we hypothesize that they behaviorally respond by being less risk averse. We used a multivariate approach to understand the escape strategies of the peninsula rock agama across an urban-rural gradient. Lizards in urban areas use a more complex structural environment, with greater perch and refuge options, compared to rural lizards. Urban lizards also allow closer approaches. Because of the differences in body coloration and size, escape strategies of females were less affected by urbanization as they use crypsis to minimize predation risk. All these extrinsic and intrinsic factors combine to result in lower risk aversion by urban lizards and may explain their tolerance of human altered environments.

Keywords

Urbanization Anthropogenic disturbance Flight initiation distance (FID) Habitat Perch Refuge Sprint speed Crypsis Predation risk 

Notes

Acknowledgments

We would like to thank the residents of north Bangalore for allowing us to scare lizards in their neighborhood. We would also like to thank three anonymous reviewers for comments on an earlier version of this manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Funding

The work was supported by the DBT-IISc partnership program and the Ministry of Environment, Forests and Climate Change. University Grants Commission supported the research fellowship for AB.

Ethical statement

This species is not covered under the Schedules of the Indian Wildlife (Protection) Act; therefore, collection permits were not required. All capture, handling, and experiment protocols were approved by the Institutional Animal Ethics Committee at the Indian Institute of Science (CAF/Ethics/394/2014).

Supplementary material

265_2017_2307_MOESM1_ESM.docx (384 kb)
ESM 1 (DOCX 383 kb)
265_2017_2307_MOESM2_ESM.xlsx (24 kb)
ESM 2 (XLSX 23 kb)

References

  1. Balakrishna S, Batabyal A, Thaker M (2016) Dining in the city: dietary shifts in Indian rock agamas across an urban–rural landscape. J Herpetol 50:423–428CrossRefGoogle Scholar
  2. Batabyal A, Gosavi SM, Gramapurohit NP (2014) Determining sensitive stages for learning to detect predators in larval bronzed frogs: importance of alarm cues in learning. J Biosci 39:701–710CrossRefPubMedGoogle Scholar
  3. Bateman PW, Fleming PA (2014a) Does human pedestrian behaviour influence risk assessment in a successful mammal urban adapter? J Zool 294:93–98CrossRefGoogle Scholar
  4. Bateman PW, Fleming PA (2014b) Living on the edge: Effects of body size, group density and microhabitat selection on escape behaviour of southern leopard frogs Lithobates sphenocephalus. Curr Zool 60(6):712–718Google Scholar
  5. Brown GE, Chivers DP (2005) Learning as an adaptive response to predation. In: Barbosa R, Castellanos I (eds) Ecology of predator-prey interactions. Oxford University Press, Oxford, pp 34–54Google Scholar
  6. Calsbeek R, Irschick DJ (2007) The quick and the dead: correlational selection on morphology, performance, and habitat use in island lizards. Evolution 61:2493–2503CrossRefPubMedGoogle Scholar
  7. Chivers DP, Mirza RS, Bryer PJ, Kiesecker JM (2001) Threat-sensitive predator avoidance by slimy sculpins: understanding the importance of visual versus chemical information. Can J Zool 79:867–873CrossRefGoogle Scholar
  8. Cooper WE Jr, Blumstein DT (eds) (2015) Escaping from predators: an integrative view of escape decisions. Cambridge University Press, CambridgeGoogle Scholar
  9. Cooper WE, Frederick WG (2007) Optimal flight initiation distance. J Theor Biol 244:59–67CrossRefPubMedGoogle Scholar
  10. Cooper WE, Whiting MJ (2007) Universal optimization of flight initiation distance and habitat-driven variation in escape tactics in a Namibian lizard assemblage. Ethology 113:661–672CrossRefGoogle Scholar
  11. DeStefano S, DeGraaf RM (2003) Exploring the ecology of suburban wildlife. Front Ecol Environ 1:95–101CrossRefGoogle Scholar
  12. Ditchkoff SS, Saalfeld ST, Gibson CJ (2006) Animal behavior in urban ecosystems: modifications due to human-induced stress. Urban Ecosyst 9:5–12CrossRefGoogle Scholar
  13. Ellenberg U, Mattern T, Seddon PJ (2009) Habituation potential of yellow-eyed penguins depends on sex, character and previous experience with humans. Anim Behav 77:289–296CrossRefGoogle Scholar
  14. Engelhardt SC, Weladji RB (2011) Effects of levels of human exposure on flight initiation distance and distance to refuge in foraging eastern gray squirrels (Sciurus carolinensis). Can J Zool 89:823–830CrossRefGoogle Scholar
  15. Frid A, Dill L (2002) Human-caused disturbance stimuli as a form of predation risk. Conserv Ecol 6:11CrossRefGoogle Scholar
  16. Garland T Jr, Losos JB (1994) Ecological morphology of locomotor performance in squamate reptiles. In: Wainwright PC, Reilly S (eds) Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago, pp 240–302Google Scholar
  17. Guay PJ, Lorenz RDA, Robinson RW, Symonds MRE, Weston MA (2013) Distance from water, sex and approach direction influence flight distances among habituated black swans. Ethology 119:552–558CrossRefGoogle Scholar
  18. Helfman GS (1989) Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav Ecol Sociobiol 24:47–58CrossRefGoogle Scholar
  19. Herrel A, Measey GJ, Vanhooydonck B, Tolley KA (2011) Functional consequences of morphological differentiation between populations of the Cape dwarf chameleon (Bradypodion pumilum). Biol J Linn Soc 104:692–700CrossRefGoogle Scholar
  20. Irschick DJ, Meyers JJ, Husak JF, Le Galliard JF (2008) How does selection operate on whole-organism functional performance capacities? A review and synthesis. Evol Ecol Res 10:177–196Google Scholar
  21. Krams I (2001) Perch selection by singing chaffinches: a better view of surroundings and the risk of predation. Behav Ecol 12:295–300CrossRefGoogle Scholar
  22. Labra A, Leonard R (1999) Intraspecific variation in antipredator responses of three species of lizards (Liolaemus): possible effects of human presence. J Herpetol 33:441–448CrossRefGoogle Scholar
  23. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  24. Losos JB (1990) The evolution of form and function: morphology and locomotor performance in West Indian Anolis lizards. Evolution 44:1189–1203CrossRefGoogle Scholar
  25. Marcellini DL, Jenssen TA (1991) Avoidance learning by the curly-tailed lizard, Leiocephalus schreibersi: implications for anti-predator behavior. J Herpetol 25:238–241CrossRefGoogle Scholar
  26. Martin J, López P (1995) Influence of habitat structure on the escape tactics of the lizard Psammodromus algirus. Can J Zool 73:129–132CrossRefGoogle Scholar
  27. Marzluff J, Shulenberger E, Endlicher W, Bradley G, Ryan C, ZumBrunnen C, Simon U (eds) (2008) Urban ecology: an international perspective on the interaction between humans and nature. Springer, New YorkGoogle Scholar
  28. McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst 11:161–176CrossRefGoogle Scholar
  29. Prosser C, Hudson S, Thompson MB (2006) Effects of urbanization on behavior, performance, and morphology of the garden skink, Lampropholis guichenoti. J Herpetol 40:151–159CrossRefGoogle Scholar
  30. Qi Y, Noble DWA, Wu Y, Whiting MJ (2014) Sex- and performance-based escape behaviour in an Asian agamid lizard, Phrynocephalus vlangalii. Behav Ecol Sociobiol 68:2035–2042CrossRefGoogle Scholar
  31. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org/ Google Scholar
  32. Radder RS, Saidapur SK, Shine R, Shanbhag BA (2006) The language of lizards: interpreting the function of visual displays of the Indian rock lizard, Psammophilus dorsalis (Agamidae). J Ethol 24:275–283CrossRefGoogle Scholar
  33. Rodriguez-Prieto I, Martin J, Fernandez-Juricic E (2011) Individual variation in behavioural plasticity: direct and indirect effects of boldness, exploration and sociability on habituation to predators in lizards. Proc R Soc Lond B 278:266–273CrossRefGoogle Scholar
  34. Runyan AM, Blumstein DT (2004) Do individual differences influence flight initiation distance? J Wildlife Manage 68:1124–1129CrossRefGoogle Scholar
  35. Samia DSM, Blumstein DT, Stankowich T, Cooper WE (2016) Fifty years of chasing lizards: new insights advance optimal escape theory. Biol Rev 91:349–366CrossRefPubMedGoogle Scholar
  36. Schlaepfer MA, Runge MC, Sherman PW (2002) Ecological and evolutionary traps. Trends Ecol Evol 17:474–480CrossRefGoogle Scholar
  37. Schooley RL, Sharpe PB, Van Horne B (1996) Can shrub cover increase predation risk for a desert rodent? Can J Zool 74:157–163CrossRefGoogle Scholar
  38. Schwarzkopf L, Shine R (1992) Costs of reproduction in lizards: escape tactics and susceptibility to predation. Behav Ecol Sociobiol 31:17–25CrossRefGoogle Scholar
  39. Shochat E, Warren PS, Faeth SH, McIntyre NE, Hope D (2006) From patterns to emerging processes in mechanistic urban ecology. Trends Ecol Evol 21:186–191CrossRefPubMedGoogle Scholar
  40. Stankowich T, Blumstein DT (2005) Fear in animals: a meta-analysis and review of risk assessment. Proc R Soc Lond B 272:2627–2634CrossRefGoogle Scholar
  41. Stiller RB, McBrayer LD (2013) The ontogeny of escape behavior, locomotor performance, and the hind limb in Sceloporus woodi. Zoology 116:175–181CrossRefPubMedGoogle Scholar
  42. Thaker M, Vanak AT, Lima SL, Hews DK (2010) Stress and aversive learning in a wild vertebrate: the role of corticosterone in mediating escape from a novel stressor. Am Nat 175:50–60CrossRefPubMedGoogle Scholar
  43. Van Damme R, Entin P, Vanhooydonck B, Herrel A (2008) Causes of sexual dimorphism in performance traits: a comparative approach. Evol Ecol Res 10:229–250Google Scholar
  44. Webb NV, Blumstein DT (2005) Variation in human disturbance differentially affects predation risk assessment in western gulls. Condor 107:178–181CrossRefGoogle Scholar
  45. Ydenberg RC, Dill LM (1986) The economics of fleeing from predators. Adv Study Behav 16:229–249Google Scholar
  46. Young CH, Jarvis PJ (2001) Assessing the structural heterogeneity of urban areas: an example from the Black Country (UK). Urban Ecosyst 5:49–69CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Centre for Ecological SciencesIndian Institute of ScienceBangaloreIndia
  2. 2.Department of ZoologySt. Josephs CollegeBangaloreIndia
  3. 3.Vrije Universiteit BrusselBrusselsBelgium

Personalised recommendations