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Intrinsic factors are relatively more important than habitat features in modulating risk perception in a tropical lizard

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Abstract

Anti-predator responses in animals are dynamic and depend on multiple factors. However, most of our understanding about animal escape responses comes from studies which examine only a small set of factors at a time and are done over a short period of animal life spans. This limits our understanding of the dynamic nature of animal escape behaviour and the relative importance of individual factors in determining their escape behaviour. We used a repeated-measures study design to assess the anti-predator response of a wild population of a sexually dimorphic tropical lizard, Psammophilus dorsalis. We followed marked individuals throughout their breeding lifespan, repeatedly assayed their escape response and measured representative intrinsic and extrinsic factors that could modulate their escape response. Our findings suggest that intrinsic factors, such as sex and body size, influenced escape response relatively more than extrinsic factors did, such as distance to refuge and perch height. Although individual variables influenced escape behaviour, in a direction mostly consistent with predictions from optimal escape theory, the interaction between factors led to novel insights into how animals dynamically evaluate multiple and changing costs throughout their lifetime to evade predation.

Significance statement

Fleeing from a potential predator is crucial to animals and depends on different factors, as there are various costs to escaping. Although several studies in the past have evaluated the role of various factors in determining escape response, the relative importance of factors and how it changes across the lifetime of individuals are not clear. By assessing individuals repeatedly over a substantial part of their lifespan, we could gain insight into how escape response changes as associated factors, intrinsic or extrinsic, change for an individual over time. This approach provided us a more robust and accurate representation of the dynamic nature of escape decisions. We also demonstrate that when multiple factors are considered simultaneously, their relative importance in determining timing of escape can considerably differ from theoretical predictions.

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References

  • Bartoń K (2016) MuMIn: Multi-model inference. R package version 1.15.6, https://cran.rproject.org/package=MuMIn

  • Batabyal A, Balakrishna S, Thaker M (2017) A multivariate approach to understanding shifts in escape strategies of urban lizards. Behav Ecol Sociobiol 71:83

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Belk MC, Tuckfield RC (2010) Changing costs of reproduction: age-based differences in reproductive allocation and escape performance in a livebearing fish. Oikos 119:163–169

    Article  Google Scholar 

  • Bennett AF (1980) The thermal dependence of lizard behaviour. Anim Behav 28:752–762

    Article  Google Scholar 

  • Blumstein DT (2016) Habituation and sensitization: new thoughts about old ideas. Anim Behav 120:255–262

    Article  Google Scholar 

  • Blumstein DT, Press A (2003) Flight-initiation distance in birds is dependent on intruder starting distance. J Wildlife Manage 67:852–857

    Article  Google Scholar 

  • Blumstein DT, Samia DS, Cooper WE (2016) Escape behavior: dynamic decisions and a growing consensus. Curr Opin Behav Sci 12:24–29

    Article  Google Scholar 

  • Brodie ED III (1989) Behavioral modification as a means of reducing the cost of reproduction. Am Nat 134:225–238

  • Bulova SJ (1994) Ecological correlates of population and individual variation in antipredator behavior of two species of desert lizards. Copeia 1994:980–992

  • Butler M, Schoener T, Losos J (2000) The relationship between sexual size dimorphism and habitat use in Greater Antillean Anolis lizards. Evolution 54:259–272

    CAS  PubMed  Google Scholar 

  • Cabido C, Galan P, Lopez P, Martin J (2009) Conspicuousness-dependent antipredatory behavior may counteract coloration differences in Iberian rock lizards. Behav Ecol 20:362–370

    Article  Google Scholar 

  • Calsbeek R (2008) An ecological twist on the morphology-performance-fitness axis. Evol Ecol Res 10:197–212

    Google Scholar 

  • Card NA, Little TD (2016) Applied meta-analysis for social science research. Guilford Press, New York

    Google Scholar 

  • Carter AJ, Heinsohn R, Goldizen AW, Biro PA (2012) Boldness, trappability and sampling bias in wild lizards. Anim Behav 83:1051–1058

    Article  Google Scholar 

  • Clark CW (1994) Antipredator behavior and the asset-protection principle. Behav Ecol 5:159–170

    Article  Google Scholar 

  • Cooper WE (1999) Tradeoffs between courtship, fighting, and antipredatory behavior by a lizard, Eumeces laticeps. Behav Ecol Sociobiol 47:54–59

    Article  Google Scholar 

  • Cooper WE (2010) Escape tactics and effects of perch height and habituation on flight initiation distance in two Jamaican anoles (Squamata: Polychrotidae). Rev Biol Trop 58:1199–1209

    PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Cooper WE, Pérez-Mellado V (2011) Escape by the Balearic lizard (Podarcis lilfordi) is affected by elevation of an approaching predator, but not by some other potential predation risk factors. Acta Herpetol 6:247–259

    Google Scholar 

  • Cooper WE, Vitt L, Hedges R, Huey R (1990) Locomotor impairment and defense in gravid lizards (Eumeces laticeps): behavioral shift in activity may offset costs of reproduction in an active forager. Behav Ecol Sociobiol 27:153–157

    Article  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 

  • Cooper WE, Wilson DS (2007) Sex and social costs of escaping in the striped plateau lizard Sceloporus virgatus. Behav Ecol 18:764–768

    Article  Google Scholar 

  • Core Team R (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org/

    Google Scholar 

  • Creel S, Christianson D, Liley S, Winnie JA (2007) Predation risk affects reproductive physiology and demography of elk. Science 315:960

    Article  CAS  PubMed  Google Scholar 

  • Cury de Barros F, Eduardo de Carvalho J, Abe AS, Kohlsdorf T (2010) Fight versus flight: the interaction of temperature and body size determines antipredator behaviour in tegu lizards. Anim Behav 79:83–88

    Article  Google Scholar 

  • Deodhar S, Isvaran K (2017) Breeding phenology of Psammophilus dorsalis: patterns in time, space, and morphology. Curr Sci India

  • Dill M (1989) The influence of distance to refuge on flight initiation distance in the gray squirrel (Sciurus carolinensisi). Can J Zool 67:233–235

    Article  Google Scholar 

  • Fisher M, Muth A (1989) A technique for permanently marking lizards. Herpetol Rev 20:45–46

    Google Scholar 

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

    Article  Google Scholar 

  • Garrido M, Pérez-Mellado V, Cooper WE (2015) Complex relationships amongst parasite load and escape behaviour in an insular lizard. Ethology 121:116–124

    Article  Google Scholar 

  • Godin J-GJ, McDonough HE (2003) Predator preference for brightly colored males in the guppy: a viability cost for a sexually selected trait. Behav Ecol 14:194–200

    Article  Google Scholar 

  • Halliday TR, Verrell PA (1988) Body size and age in amphibians and reptiles. J Herpetol 22:253

    Article  Google Scholar 

  • Hernandez-Jimenez A, Rios-Cardenas O (2012) Natural versus sexual selection: predation risk in relation to body size and sexual ornaments in the green swordtail. Anim Behav 84:1051–1059

    Article  Google Scholar 

  • Hertz PE, Huey RB, Nevo E (1982) Fight versus flight: body temperature influences defensive responses of lizards. Anim Behav 30:676–679

    Article  Google Scholar 

  • Husak JF (2006a) Does survival depend on how fast you can run or how fast you do run? Funct Ecol 20:1080–1086

    Article  Google Scholar 

  • Husak JF (2006b) Do female collared lizards change field use of maximal sprint speed capacity when gravid? Oecologia 150:339–343

    Article  PubMed  Google Scholar 

  • Irschick DJ, Carlisle E, Elstrott J, Ramos M, Buckley C, Vanhooydonck B, Meyers J, Herrel A (2005) A comparison of habitat use, morphology, clinging performance and escape behaviour among two divergent green anole lizard (Anolis carolinensis) populations. Biol J Linn Soc 85:223–234

    Article  Google Scholar 

  • King R (2000) Analyzing the relationship between clutch size and female body size in reptiles. J Herpetol 34:148–150

    Article  Google Scholar 

  • Lafaille M, Bimbard G, Greenfield MD (2010) Risk trading in mating behavior: forgoing anti-predator responses reduces the likelihood of missing terminal mating opportunities. Behav Ecol Sociobiol 64:1485–1494

    Article  Google Scholar 

  • Lailvaux SP (2007) Interactive effects of sex and temperature on locomotion in reptiles. Integr Comp Biol 47:189–199

    Article  PubMed  Google Scholar 

  • Lailvaux SP, Alexander GJ, Whiting MJ (2003) Sex-based differences and similarities in locomotor performance, thermal preferences, and escape behaviour in the lizard Platysaurus intermedius wilhelmi. Physiol Biochem Zool 76:511–521

    Article  PubMed  Google Scholar 

  • Lima SL (1998) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Adv Study Behav 27:215–290

    Article  Google Scholar 

  • Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659

    Article  Google Scholar 

  • Lind J, Cresswell W (2005) Determining the fitness consequences of antipredation behavior. Behav Ecol 16:945–956

    Article  Google Scholar 

  • Lowry H, Lill A, Wong BBM (2013) Behavioural responses of wildlife to urban environments. Biol Rev 88:537–549

    Article  PubMed  Google Scholar 

  • Luttbeg B, Sih A (2010) Risk, resources and state-dependent adaptive behavioural syndromes. Philos T Roy Soc B 365:3977–3990

    Article  Google Scholar 

  • Mahapatro NN, Begum KA, Behera HN, Patnaik BK (1989) Age-determination in the lizard, Psammophilus dorsalis (Gray 1831). J Anim Morphol Physiol 36:3–80

    Google Scholar 

  • Martín J, Luque-Larena JJ, López P (2009) When to run from an ambush predator: balancing crypsis benefits with costs of fleeing in lizards. Anim Behav 78:1011–1018

    Article  Google Scholar 

  • Miles DB, Sinervo B, Frankino AWA (2000) Reproductive burden, locomotor performance and the cost of reproduction in free ranging lizards. Evolution 54:1386–1395

    Article  CAS  PubMed  Google Scholar 

  • Møller AP, Liang W (2013) Tropical birds take small risks. Behav Ecol 24:267–272

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Olsson M, Shine R (1996) Does reproductive success increase with age or with size in species with indeterminate growth? A case study using sand lizards (Lacerta agilis). Oecologia 105:175

    Article  PubMed  Google Scholar 

  • Olsson M, Shine R, Bak-Olsson E (2000) Locomotor impairment of gravid lizards: is the burden physical or physiological? J Evol Biol 13:263–268

    Article  Google Scholar 

  • Ory NC, van Son TC, Thiel M (2015) Mating rock shrimp hedge their bets: old males take greater risk, but only after careful assessment of the investment scenario. Behav Ecol Sociobiol 69:1975–1984

    Article  Google Scholar 

  • Delarue EMP, Kerr SE, Lee TR (2015) Habitat complexity, environmental change, and personality: a tropical perspective. Behav Process 120:101–110

  • Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891

    Article  Google Scholar 

  • Pérez-Cembranos A, Pérez-Mellado V, Cooper WE (2013) Predation risk and opportunity cost of fleeing while foraging on plants influence escape decisions of an insular lizard. Ethology 119:522–530

    Article  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York

    Book  Google Scholar 

  • Polcák D, Gvozdík L (2014) Should I stay or should I go? The influence of temperature and sex on predator-induced responses in newts. Anim Behav 89:79–84

    Article  Google Scholar 

  • Qi Y, Noble DW, 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 

  • Radder RS, Saidapur SK (2005) Population density, microhabitat use and activity pattern of the Indian rock lizard, Psammophilus dorsalis (Agamidae). Curr Sci India 89:560–566

    Google Scholar 

  • Radder RS, Saidapur SK, Shanbhag BA (2006) Big boys on top: effects of body size, sex, and reproductive state on perching behaviour in the tropical rock dragon, Psammophilus dorsalis. Anim Biol 56:311–321

    Article  Google Scholar 

  • Rand AS (1964) Inverse relationship between temperature and shyness in the lizard Anolis Lineatopus. Ecology 45:863–864

    Article  Google Scholar 

  • Rangaswami S, Sridhar S (1993) Birds of Rishi Valley and renewal of their habitats. Rishi Valley Education Centre, Krishnamurti Foundation India, Andhra Pradesh

    Google Scholar 

  • Roff DA (2002) Life history evolution. Sinauer Associates, Massachusetts

    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 

  • Samia DSM, Møller AP, Blumstein DT, Stankowich T, Cooper WE (2015) Sex differences in lizard escape decisions vary with latitude, but not sexual dimorphism. Proc R Soc B 282:20150050

    Article  PubMed  PubMed Central  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 

  • Shine R (2003) Locomotor speeds of gravid lizards: placing “costs of reproduction” within an ecological context. Funct Ecol 17:526–533

    Article  Google Scholar 

  • Shine R, Olsson MM, Lemaster MP, Moore IT, Mason RT (2000) Effects of sex, body size, temperature, and location on the antipredator tactics of free-ranging gartersnakes (Thamnophis sirtalis, Colubridae). Behav Ecol 11:239–245

    Article  Google Scholar 

  • Sinervo B, Licht P (1991) Proximate constraints on the evolution of egg size, number, and total clutch mass in lizards. Science 252:1300–1302

    Article  CAS  PubMed  Google Scholar 

  • Smith MA (1935) The Fauna of British India, including Ceylon and Burma, Vol. I. Taylor and Francis, London

    Google Scholar 

  • Sreekar R, Quader S (2013) Influence of gaze and directness of approach on the escape responses of the Indian rock lizard, Psammophilus dorsalis (Gray, 1831). J Biosci 38:829–833

    Article  CAS  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 

  • Stankowich T, Coss RG (2007) Effects of risk assessment, predator behavior, and habitat on escape behavior in Columbian black-tailed deer. Behav Ecol 18:358–367

    Article  Google Scholar 

  • Stuart-Fox DM, Moussalli A, Marshall NJ, Owens IPF (2003) Conspicuous males suffer higher predation risk: visual modelling and experimental evidence from lizards. Anim Behav 66:541–550

    Article  Google Scholar 

  • Vanhooydonck B, Herrel A, Irschick DJ (2007) Determinants of sexual differences in escape behavior in lizards of the genus Anolis: a comparative approach. Integr Comp Biol 47:200–210

    Article  PubMed  Google Scholar 

  • Whiting MJ, Lailvaux SP, Reaney LT, Wymann M (2003) To run or hide? Age-dependent escape behaviour in the common flat lizard (Platysaurus intermedius wilhelmi). J Zool 260:123–128

    Article  Google Scholar 

  • Wilson ADM, Godin J-GJ (2010) Boldness and intermittent locomotion in the bluegill sunfish, Lepomis macrochirus. Behav Ecol 21:57–62

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Zani PA, Jones TD, Neuhaus RA, Milgrom JE (2009) Effect of refuge distance on escape behavior of side-blotched lizards (Uta stansburiana). Can J Zool 87:407–414

    Article  Google Scholar 

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Acknowledgements

This manuscript results from part of thesis work that was submitted in partial fulfilment for a BS-MS Degree at IISER Pune. We thank P. Somnath for his impeccable field assistance; Pratik Gupte and Ambika for assistance in tagging lizards early in the summer; Rishi Valley School and NCF for providing field logistics; Maria Thaker and Raghav Rajan for their advice regarding methods and presentation; peers at CES and IISER Pune for their encouragement and support throughout the course of this project; and E.D. Brodie III, R.M. Cox, all members of the Brodie-Cox lab, S. Zeeshan Ali, the handling editor and two anonymous reviewers, whose comments greatly helped improve earlier versions of this manuscript.

Funding information

We thank the varied funding agencies that provided financial assistance throughout the project. This project was made possible by funding and scholarship provided through Scholarship for Higher Education (SHE-INSPIRE) to RB and Funding for Improvement of Science and technology (FIST) grant to CES provided by the Department of Science and Technology (DST) and DBT-IISc Partnership Programme.

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Correspondence to Rachana Bhave.

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The authors declare that they have no conflict of interest.

Ethical note

This species is not covered under the Schedules of the Indian Wildlife Protection Act; thus, specific permits from government were not required. All experimental protocols on field including the capture and handling of animals were approved by the Institutional Animal Ethics Committee constituted by the Indian Institute of Science (CAF/Ethics/390/2014).

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Data and R code generated and analysed during this study are available from the corresponding author upon request.

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Communicated by T. Madsen

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Bhave, R., Deodhar, S. & Isvaran, K. Intrinsic factors are relatively more important than habitat features in modulating risk perception in a tropical lizard. Behav Ecol Sociobiol 71, 146 (2017). https://doi.org/10.1007/s00265-017-2372-7

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