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

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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.

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References

  • Balakrishna S, Batabyal A, Thaker M (2016) Dining in the city: dietary shifts in Indian rock agamas across an urban–rural landscape. J Herpetol 50:423–428

    Article  Google Scholar 

  • 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 39:701–710

    Article  PubMed  Google Scholar 

  • Bateman PW, Fleming PA (2014a) Does human pedestrian behaviour influence risk assessment in a successful mammal urban adapter? J Zool 294:93–98

    Article  Google Scholar 

  • 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):712–718

  • 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 34–54

    Google Scholar 

  • Calsbeek R, Irschick DJ (2007) The quick and the dead: correlational selection on morphology, performance, and habitat use in island lizards. Evolution 61:2493–2503

    Article  PubMed  Google Scholar 

  • 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 79:867–873

    Article  Google Scholar 

  • Cooper WE Jr, Blumstein DT (eds) (2015) Escaping from predators: an integrative view of escape decisions. Cambridge University Press, Cambridge

    Google Scholar 

  • Cooper WE, Frederick WG (2007) Optimal flight initiation distance. J Theor Biol 244:59–67

    Article  PubMed  Google Scholar 

  • Cooper WE, Whiting MJ (2007) Universal optimization of flight initiation distance and habitat-driven variation in escape tactics in a Namibian lizard assemblage. Ethology 113:661–672

    Article  Google Scholar 

  • DeStefano S, DeGraaf RM (2003) Exploring the ecology of suburban wildlife. Front Ecol Environ 1:95–101

    Article  Google Scholar 

  • Ditchkoff SS, Saalfeld ST, Gibson CJ (2006) Animal behavior in urban ecosystems: modifications due to human-induced stress. Urban Ecosyst 9:5–12

    Article  Google Scholar 

  • Ellenberg U, Mattern T, Seddon PJ (2009) Habituation potential of yellow-eyed penguins depends on sex, character and previous experience with humans. Anim Behav 77:289–296

    Article  Google Scholar 

  • 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 89:823–830

    Article  Google Scholar 

  • Frid A, Dill L (2002) Human-caused disturbance stimuli as a form of predation risk. Conserv Ecol 6:11

    Article  Google Scholar 

  • 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 240–302

    Google Scholar 

  • 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 119:552–558

    Article  Google Scholar 

  • Helfman GS (1989) Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav Ecol Sociobiol 24:47–58

    Article  Google Scholar 

  • 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 104:692–700

    Article  Google Scholar 

  • 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 10:177–196

    Google Scholar 

  • Krams I (2001) Perch selection by singing chaffinches: a better view of surroundings and the risk of predation. Behav Ecol 12:295–300

    Article  Google Scholar 

  • Labra A, Leonard R (1999) Intraspecific variation in antipredator responses of three species of lizards (Liolaemus): possible effects of human presence. J Herpetol 33:441–448

    Article  Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  • Losos JB (1990) The evolution of form and function: morphology and locomotor performance in West Indian Anolis lizards. Evolution 44:1189–1203

    Article  Google Scholar 

  • Marcellini DL, Jenssen TA (1991) Avoidance learning by the curly-tailed lizard, Leiocephalus schreibersi: implications for anti-predator behavior. J Herpetol 25:238–241

    Article  Google Scholar 

  • Martin J, López P (1995) Influence of habitat structure on the escape tactics of the lizard Psammodromus algirus. Can J Zool 73:129–132

    Article  Google Scholar 

  • 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 York

    Google Scholar 

  • McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst 11:161–176

    Article  Google Scholar 

  • Prosser C, Hudson S, Thompson MB (2006) Effects of urbanization on behavior, performance, and morphology of the garden skink, Lampropholis guichenoti. J Herpetol 40:151–159

    Article  Google Scholar 

  • 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 68:2035–2042

    Article  Google Scholar 

  • 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 

  • 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 24:275–283

    Article  Google Scholar 

  • 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 278:266–273

    Article  Google Scholar 

  • Runyan AM, Blumstein DT (2004) Do individual differences influence flight initiation distance? J Wildlife Manage 68:1124–1129

    Article  Google Scholar 

  • Samia DSM, Blumstein DT, Stankowich T, Cooper WE (2016) Fifty years of chasing lizards: new insights advance optimal escape theory. Biol Rev 91:349–366

    Article  PubMed  Google Scholar 

  • Schlaepfer MA, Runge MC, Sherman PW (2002) Ecological and evolutionary traps. Trends Ecol Evol 17:474–480

    Article  Google Scholar 

  • Schooley RL, Sharpe PB, Van Horne B (1996) Can shrub cover increase predation risk for a desert rodent? Can J Zool 74:157–163

    Article  Google Scholar 

  • Schwarzkopf L, Shine R (1992) Costs of reproduction in lizards: escape tactics and susceptibility to predation. Behav Ecol Sociobiol 31:17–25

    Article  Google Scholar 

  • Shochat E, Warren PS, Faeth SH, McIntyre NE, Hope D (2006) From patterns to emerging processes in mechanistic urban ecology. Trends Ecol Evol 21:186–191

    Article  PubMed  Google Scholar 

  • Stankowich T, Blumstein DT (2005) Fear in animals: a meta-analysis and review of risk assessment. Proc R Soc Lond B 272:2627–2634

    Article  Google Scholar 

  • Stiller RB, McBrayer LD (2013) The ontogeny of escape behavior, locomotor performance, and the hind limb in Sceloporus woodi. Zoology 116:175–181

    Article  PubMed  Google Scholar 

  • 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 175:50–60

    Article  PubMed  Google Scholar 

  • Van Damme R, Entin P, Vanhooydonck B, Herrel A (2008) Causes of sexual dimorphism in performance traits: a comparative approach. Evol Ecol Res 10:229–250

    Google Scholar 

  • Webb NV, Blumstein DT (2005) Variation in human disturbance differentially affects predation risk assessment in western gulls. Condor 107:178–181

    Article  Google Scholar 

  • Ydenberg RC, Dill LM (1986) The economics of fleeing from predators. Adv Study Behav 16:229–249

  • Young CH, Jarvis PJ (2001) Assessing the structural heterogeneity of urban areas: an example from the Black Country (UK). Urban Ecosyst 5:49–69

    Article  Google Scholar 

Download references

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.

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Correspondence to Maria Thaker.

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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).

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Communicated by S. J. Downes

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Batabyal, A., Balakrishna, S. & Thaker, M. A multivariate approach to understanding shifts in escape strategies of urban lizards. Behav Ecol Sociobiol 71, 83 (2017). https://doi.org/10.1007/s00265-017-2307-3

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