Skip to main content

Sex- and performance-based escape behaviour in an Asian agamid lizard, Phrynocephalus vlangalii

Abstract

In lizards, males are predicted to sprint faster and run for longer than females by virtue of higher testosterone levels and differences in morphology. Consequently, escape behaviour is also predicted to be associated with sex and locomotor performance, yet these links have rarely been explored. Here, we tested whether escape behaviour is associated with locomotor performance in the toad-headed agama, Phrynocephalus vlangalii, and whether it is sex-dependent. This species is also characterized by elaborate tail displays, which we examined as a potential pursuit-deterrent signal. Tail waves were performed by a very small proportion (2/58, 3 %) of individuals during predatory trials, suggesting that tail signalling functions exclusively in a social context. To understand the relationships between sex, escape behaviour and performance, we first measured escape behaviour (flight initiation distance, flight distance—measured differently compared to previous studies of lizard escape behaviour, and refuge use) in the field before measuring maximal sprint speed and endurance on the same individuals in the laboratory. Flight initiation distance did not differ between the sexes and was unrelated to performance capacity (maximal endurance and sprint speed) but was positively related to body size with larger individuals fleeing earlier. Males fled farther than females, but flight distance was also unrelated to either endurance or sprint speed. Interestingly, faster females were less likely to enter a refuge than slower females, whereas sprint speed and the probability of taking refuge were unrelated for males. Our results suggest that when males and females are not obviously sexually dimorphic, they are more likely to overlap in escape tactics.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Blumstein DT, Pelletier D (2005) Yellow-bellied marmot hiding time is sensitive to variation in costs. Can J Zool 83:363–367

    Article  Google Scholar 

  • Broom M, Ruxton GD (2005) You can run—or you can hide: optimal strategies for cryptic prey against pursuit predators. Behav Ecol 16:534–540

    Article  Google Scholar 

  • Clobert J, Oppliger A, Sorci G, Ernande B, Swallow JG, Garland T (2000) Trade-offs in phenotypic traits: endurance at birth, growth, survival, predation and susceptibility to parasitism in a lizard, Lacerta vivipara. Funct Ecol 14:675–684

    Article  Google Scholar 

  • Cooper WE (2000) Effect of temperature on escape behaviour by an ectothermic vertebrate, the keeled earless lizard (Holbrookia propinqua). Behaviour 137:1299–1315

    Article  Google Scholar 

  • Cooper WE (2001) Multiple roles of tail display by the curly-tailed lizard Leiocephalus carinatus: pursuit deterrent and deflective roles of a social signal. Ethology 107:1137–1149

    Article  Google Scholar 

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

    PubMed  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 

  • Dial BE (1986) Tail display in two species of iguanid lizards: a test of the 'predator signal' hypothesis. Am Nat 127:101–111

    Article  Google Scholar 

  • Font E, Carazo P, Pérez i de Lanuza G, Kramer M (2012) Predator-elicited foot shakes in wall lizards (Podarcis muralis): evidence for a pursuit-deterrent function. J Comp Psychol 126:87–96

    PubMed  Article  Google Scholar 

  • Goodman BA, Miles DB, Schwarzkopf L (2008) Life on the rocks: habitat use drives morphological and performance evolution in lizards. Ecology 89:3462–3471

    PubMed  Article  Google Scholar 

  • Husak JF, Fox SF (2008) Sexual selection on locomotor performance. Evol Ecol Res 10:213–228

    Google Scholar 

  • Irschick DJ, Meyers JJ, Husak JF, Le Galliard J-F (2008) How does selection operate on whole-organism functional performance capacities? A review and synthesis. Evol Ecol Res 10:177–196

    Google Scholar 

  • Klukowski M, Jenkinson NM, Nelson CE (1998) Effects of testosterone on locomotor performance and growth in field-active northern fence lizards, Sceloporus undulatus hyacinthinus. Physiol Zool 71:506–514

    CAS  PubMed  Google Scholar 

  • Kullberg C, Houston DC, Metcalfe NB (2002) Impaired flight ability—a cost of reproduction in female blue tits. Behav Ecol 13:575–579

    Article  Google Scholar 

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

    PubMed  Article  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

    PubMed  Article  Google Scholar 

  • Le Galliard JF, Ferriere R (2008) Evolution of maximal endurance capacity: natural and sexual selection across age classes in a lizard. Evol Ecol Res 10:157–176

    Google Scholar 

  • Leal M (1999) Honest signalling during prey-predator interactions in the lizard Anolis cristatellus. Anim Behav 58:521–526

    PubMed  Article  Google Scholar 

  • Losos JB, Creer DA, Schulte JA (2002) Cautionary comments on the measurement of maximum locomotor capabilities. J Zool 258:57–61

    Article  Google Scholar 

  • Martin J, Lopez P (2000) Costs of refuge use affect escape decisions of Iberian rock lizards Lacerta monticola. Ethology 106:483–492

    Article  Google Scholar 

  • Martin J, Lopez P (2003) Ontogenetic variation in antipredator behavior of Iberian rock lizards (Lacerta monticola): effects of body-size-dependent thermal-exchange rates and costs of refuge use. Can J Zool 81:1131–1137

    Article  Google Scholar 

  • Martin J, Lopez P (2010) Thermal constraints of refuge use by Schreiber’s green lizards, Lacerta schreiberi. Behaviour 147:275–284

    Article  Google Scholar 

  • Martin J, Luque-Larena JJ, Lopez 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 

  • Miller BM, McDonnell LH, Sanders DJ, Lewtas KLM, Turgeon K, Kramer DL (2011) Locomotor compensation in the sea: body size affects escape gait in parrotfish. Anim Behav 82:1109–1116

    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 

  • Noble DWA, Fanson KV, Whiting MJ (2014) Sex, androgens and whole organism performance in an Australian lizard. Biol J Linn Soc 111:834–849

    Article  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 

  • Qi Y, Noble DWA, Fu JZ, Whiting MJ (2012) Spatial and social organization in a burrow-dwelling lizard (Phrynocephalus vlangalii) from China. PLoS ONE 7:e41130

    CAS  PubMed Central  PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

  • R-Core-Team (2013) R: a language and environment for statistical computing

  • Sagonas K, Meiri S, Valakos ED, Pafilis P (2013) The effect of body size on the thermoregulation of lizards on hot, dry Mediterranean islands. J Therm Biol 38:92–97

    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 

  • 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 

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

    PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

Download references

Acknowledgments

We thank Li Hua and Cuoke for helping with field data collection. This work was supported by the National Natural Science Foundation of China (31201723) and the Chinese Academy of Sciences (Y2C3041).

Ethical standards

Handling and processing of lizards followed approved protocols from the Chengdu Institute of Biology of the Chinese Academy of Sciences and the Animal Behavior Society (ABS)/Association for the Study of Animal Behaviour (ASAB) Guidelines for the treatment of animals in behavioural research and teaching. The Chengdu Institute of Biology approved this project, and permission for fieldwork was provided by the Forestry Department of the Sichuan Provincial Government and the Management Office of the Zoige Nature Reserve.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martin J. Whiting.

Additional information

Communicated by T. Madsen

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Qi, Y., Noble, D.W.A., Wu, Y. et al. Sex- and performance-based escape behaviour in an Asian agamid lizard, Phrynocephalus vlangalii . Behav Ecol Sociobiol 68, 2035–2042 (2014). https://doi.org/10.1007/s00265-014-1809-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-014-1809-5

Keywords

  • Escape behaviour
  • Locomotor performance
  • Sprint speed
  • Endurance
  • Reptile