Acta Herpetologica 16(1): 53-57, 2021 ISSN 1827-9635 (print) © Firenze University Press ISSN 1827-9643 (online) www.fupress.com/ah DOI: 10.36253/a_h-9843 Flight initiation distance of Urosaurus ornatus from the Sierra de Samalayuca, Mexico Julio A. Lemos-Espinal1,*, Geoffrey R. Smith2 1 Laboratorio de Ecología-UBIPRO, FES Iztacala UNAM, Avenida los Barrios 1, Los Reyes Iztacala, Tlalnepantla,edo. de México, 54090, México 2 Department of Biology, Denison University, Granville, Ohio 43023 USA * Corresponding author. E-mail: lemos@unam.mx Submitted on: 2020, 6th October; revised on: 2021, 10th January; accepted on: 2020, 12th January Editor: Simon Baeckens Abstract. In lizards, flight initiation distance (FID), the distance between a prey individual and a predator when escape begins, can be affected by numerous intrinsic and extrinsic factors, including sex, temperature, and level of conspicuousness. Here we report on a study of FID in a population of Ornate Tree Lizards, Urosaurus ornatus, from the Sierra de Samalyuca, Chihuahua, Mexico which are cryptic due to their dorsal coloration blending into their back- ground. Urosaurus ornatus in our study population allowed close approaches (mean FID = 65 cm). Mean FID did not differ between males and females. We also found no effect of body, air, or substrate temperature on FID. The short FID we observed may be related to the cryptic nature of U. ornatus. Keywords. Approach distance, anti-predator response, cryptic, lizard, sex, temperature. For many prey individuals one of the most important decisions that must be made when confronted with an approaching predator is when to begin their antipreda- tor response, which for many prey is flight (Ydenberg and Dill, 1986). Theoretically, this decision should reflect a balance between fleeing too early and losing fitness due to lost opportunities (e.g., foraging, thermoregulation, mat- ing) and fleeing too late and being caught by the predator (Ydenberg and Dill, 1986; Cooper and Frederick, 2007). The distance from the predator to the prey when the prey begins to flee is the flight initiation distance (FID) and is a readily measured aspect of a prey’s behavior (Ydenberg and Dill, 1986; Cooper and Frederick, 2007). For lizards, FID can be affected by numerous intrin- sic and extrinsic factors, including body and environ- mental temperature (e.g., Smith and Lemos-Espinal, 2005; Cooper et al., 2009; Braun et al., 2010; Cooper, 2011a); perch, habitat, or microhabitat characteristics (Cooper, 2003b; Cooper et al., 2009; Morris and Lattan- zio, 2020), and sex (Vanhooydonck et al., 2007; Majláth and Majláthova, 2009; Salido and Vicente, 2019). How- ever, these factors do not always affect FID in lizards (e.g., temperature: Martin and López, 2000; Amo et al., 2005; Smith and Lemos-Espinal, 2005; Cooper, 2006; sex: Cooper, 2003a, 2011b; Cooper and Pérez-Mellado, 2011; Kopena et al., 2015). For example, because lizards are ectotherms, temperature, whether body or environmen- tal, can influence their locomotor performance, includ- ing sprint speed (van Damme and Vanhooydonck, 2001; Herrel et al., 2007). Thus, when temperature does affect lizard FID, the FID typically decreases with body or environmental temperature since lizards at higher tem- peratures can usually run faster and therefore can allow a predator to approach closer and still escape compared to lizards at lower temperatures (e.g., Cooper, 2006, 2011b; Cooper et al., 2009; Braun et al., 2010). Another aspect of a lizard that could affect its FID is the level of crypsis. In general, organisms with effective 54 J.A. Lemos-Espinal, G.R. Smith crypsis should remain still and allow close approaches (Cooper et al., 2008). Compared to other aspects of liz- ards that might affect FID, the effects of conspicuous- ness are relatively understudied. However, previous work related to the conspicuousness of lizards and FID has generally found that more cryptic or more concealed liz- ards allow closer approaches than less cryptic or less con- cealed lizards (Cooper, 2006; Vanhooydonck et al., 2007; Cooper et al., 2009; Cooper and Sherbrooke, 2010). Here we report on a field study of FID in a popula- tion of Ornate Tree Lizards, Urosaurus ornatus, from the Sierra de Samalyuca, Chihuahua, Mexico. Urosau- rus ornatus are distributed from Utah and Colorado to northern Mexico (Wiens, 1993; Haenel, 2007) and their populations often primarily use trees as perches (Bal- tosser and Best, 1990; Smith, 1996b; James et al., 2003) but some populations are more terrestrial, using rocks as perches (Herrel et al., 2001; Haenel, 2018; Taylor et al., 2018), including the population we studied (see also Gadsden et al., 2021). Urosaurus ornatus tend to be rel- atively small lizards (mean SVL = 50 cm; Smith, 1996b) that are sit-and-wait foragers (Cooper et al., 2001). We examined whether body temperature and sex affect flight initiation distance. In addition, U. ornatus can adjust their dorsal coloration and reflectance to match their background (Zucker, 1989; Hamilton et al., 2008), mak- ing them cryptic. Given their ability to blend into their background (see Fig. 1), we expected that U. ornatus would allow closer approaches compared to other species (i.e., have a relatively short FID). We also predicted that temperatures, both body and environmental, would have little effect on FID since they may rely more on being still and remaining cryptic rather than relying on locomotor performance which can be affected by temperature (e.g., Gilbert and Miles, 2016, 2017). We studied the FID of U. ornatus on 10 and 11 November 1998 in a population at the Ojo de Enmedio, Sierra de Samalyuca, Chihuahua, Mexico ((31°22’48.2”N, 106°35´2.7”W, 1344 m elevation). Ojo de Enmedio is a small ranch located approximately 10 km northwest of the town of Samalayuca (municipality of Juárez, Chi- huahua), in the foothills of the extreme northwest of the Sierra de Samalayuca. The vegetation is typical xerophyte scrub of the Chihuahuan Desert. When we spotted a stationary and undisturbed liz- ard, one of us (JLE) slowly and directly approached it at a constant speed. The same person always made the approach to promote a more consistent appearance and approach among lizards. We measured FID as the dis- tance between the location where the approaching “pred- ator” was when the lizard first fled and where the lizard was first observed (to nearest cm using a meter tape). Since we walked through the study area and did not return to a specific site it is highly unlikely we repeated measuring FID on any individual. We captured all lizards and recorded their sex. We also measured body tempera- ture (Tb), air temperature (Ta: 1 cm above surface at loca- tion lizard first observed), and substrate temperature (Ts: on surface at location lizard first observed) to the nearest 0.1 C using a quick-reading cloacal thermometer. All liz- ards were captured within 1 minute of determining FID. All lizards were in full sun when first observed. We compared FID between males and females using an analysis of variance on log-transformed FIDs. We used linear regressions to analyze the relationships between FID and Tb, Ta, and Ts. We used JMP Pro 14 (SAS Insti- tute, Cary, North Carolina, USA) to conduct all statistical analyses and used an a-value of 0.05 to determine statisti- cal significance. Means are given ± 1 S.E. Overall mean FID was 64.7 ± 6.7 cm (n = 50). Mean FID did not differ between males (68.9 ± 8.4 cm; n = 32) and females (57.4 ± 11.2 cm; n = 18; F1,48 = 0.18, P = 0.67). Flight initiation distance was not affected by Tb (n = 50, r2 = 0.057, P = 0.10), Ta (n = 50, r2 = 0.02, P = 0.34), or Ts (n = 50, r2 = 0.03, P = 0.22). Urosaurus ornatus in our study population allowed close approaches by the human simulated predator (i.e., mean FID = 65 cm). Indeed, in Samalayuca, it is possi- ble to capture U. ornatus directly with one’s hands rather than needing to use a lasso (J.A. Lemos-Espinal, pers. observ.). Urosaurus ornatus in Arizona also allow similar- ly close approaches, with a mean FID in males of 90 cm and 64 cm in females (Morris and Lattanzio, 2020). The Fig. 1. Photograph of a Urosaurus ornatus on a rock substrate dem- onstrating its cryptic dorsal coloration. Photograph was taken from a population at San José de las Piedras, municipality of Ocampo, Coahuila but the U. ornatus from our study site are very similar. Photograph by J.A. Lemos-Espinal. 55Flight initiation distance of U. ornatus short FID we observed, and as has been observed in oth- er U. ornatus, may be related to the cryptic nature of U. ornatus (Zucker, 1989; Hamilton et al., 2008). The mean FID of Urosaurus bicarinatus, a congener but not sister species of U. ornatus that occurs further south in Mexico (Wiens, 1993; Reeder and Wiens, 1996) and uses aca- cia trees as perches (Lemos-Espinal et al., 1997), in the Cañón del Zopilote in Guerrero was 200 cm (Smith and Lemos-Espinal, 2005), which is almost 3x greater than the FID we observed. However, in our experience, U. bicarinatus in the Cañón del Zopilote occurs mainly on trees, and although still cryptic, are more readily seen by humans than the U. ornatus in the Sierra del Samalayuca (J.A. Lemos-Espinal, pers. observ.). Other phrynosomatid lizards from the southwestern United States and Mexico have greater FIDs (e.g., Sceloporus virgatus, 160-310 cm, Smith, 1996a; Cooper and Avalos, 2010; S. anahuacus, 260 cm, Smith and Lemos-Espinal, 2005; S. gadoviae, 283 cm, Smith and Lemos-Espinal, 2005; S. jarrovii, 150- 290 cm, Cooper and Avalos, 2010; S. mucronatus, 605 cm, Smith and Lemos-Espinal, 2005, Uta stansburiana, 210 cm, Keehn and Feldman, 2018). Our results are also consistent with other studied lizards that are cryptic. For example, when in situations in which they are more cryp- tic, Phrynosoma modestum allowed closer approaches than when they were less cryptic, especially at lower tem- peratures (Cooper and Sherbrooke, 2010), and cryptic species of Anolis allow a human to approach closer than other less cryptic species (Cooper, 2006; Vanhooydonck et al., 2007). We found no effect of body, air, or substrate tem- perature on FID, perhaps because of the relatively low overall FID we observed. It may be that the FID of cryp- tic species is less affected by body and environmental temperatures than other species since predator avoid- ance is not predicated on locomotor performance. This is also consistent with the fact that air and substrate temperature did not affect FID in U. bicarinatus (Smith and Lemos-Espinal, 2005). However, the FID of U. orna- tus in Arizona decreased with increased body and perch temperature (Morris and Lattanzio, 2020), suggesting the situation may be more complex. Indeed, whereas temperature did not affect FID, U. bicarinatus that were captured were using perches with lower Tas than those that escaped (Smith and Lemos-Espinal, 2005), indicat- ing that the ability to escape, if not their predilection to flee, may still be related to temperature in these lizards. The lack of effect of temperature on FID has also been observed in non-cryptic lizards (e.g., Martin and López, 2000; Amo et al., 2005; Smith and Lemos-Espinal, 2005; Cooper, 2006). However, in other species of lizards, FID typically decreases with increased body or environmen- tal temperatures (e.g., Cooper, 2006, 2011a; Cooper et al., 2009; Braun et al., 2010), and FID in Hobrookia propin- qua increases with substrate temperature (Cooper, 2000). The variation in the effects of temperature on FID in liz- ards needs more study to understand why there is a rela- tionship in some species but not in others. The lack of a difference in approach distance between male and female U. ornatus in our population contrasts with results from another population of U. ornatus where male U. ornatus had greater FID than females (Morris and Lattanzio, 2020). However, our result is consistent with results from U. bicarinatus (Smith and Lemos-Espi- nal, 2005). In a review of the literature, Cooper (2011b) found that in general most species of lizards show no sexual dimorphism in FID. However, females in some lizards allow closer approaches than males (Majláth and Majláthová, 2009; Vanhooydonck et al., 2017; Salido and Vicente, 2019). Why some populations and species show sexual dimorphism in FID and others do not is not clear and warrants more direct investigation. In conclusion, the cryptic nature of U. ornatus in our population may lead to a short FID since staying still is probably better than fleeing. This supposition is sup- ported by the lack of an effect of temperature, both body and environmental, and sex on FID in this population. However, directly assessing the effect of crypsis on FID is needed to confirm this conclusion. ACKNOWLEDGMENTS We thank two anonymous reviewers for helpful com- ments on the manuscript. Support for this study was provided by Dirección General de Asuntos del Personal Académico – Programa de Apoyo a Proyectos de Inves- tigación e Innovación Tecnológica (DGAPA – PAPIIT), through Project IN202021. This research conformed with all regulations in place in Mexico at the time the research was conducted. REFERENCES Amo, L., López P., Martin, J. (2005): Flexibility in anti- predatory behavior allows wall lizards to cope with multiple types of predators. Ann. Zool. Fenn. 42: 109- 121. Baltosser, W.H., Best, T.L. (1990): Seasonal occurrence and habitat utilization by lizards in southwestern New Mexico. Southwest. Nat. 35: 377-384. Braun, C.A., Baird, T.A., LeBeau, J.K. (2010): Influence of substrate temperature and directness of approach on 56 J.A. Lemos-Espinal, G.R. Smith the escape response of juvenile Collared Lizards. Her- petologica 66: 418-424. Cooper, W.E. Jr. (2000): Effect of temperature on escape behaviour by an ectothermic vertebrate, the Keeled Earless Lizard (Holbrookia propinqua). Behaviour 137: 1299-1315. Cooper, W.E. Jr. (2003a): Sexual dimorphism in distance from cover but not escape behavior by the Keeled Earless Lizard Holbrookia propinqua. J. Herpetol. 37: 374-378. Cooper, W.E. Jr. (2003b): Risk factors affecting escape behavior by the desert iguana, Dipsosaurus dorsalis: speed and directness of predator approach, degree of cover, direction of turning by a predator, and temper- ature. Can. J. Zool. 81: 979-984. Cooper, W.E. Jr. (2006): Risk factors affecting escape behavior by Puerto Rican Anolis lizards. Can. J. Zool. 84: 495-504. Cooper, W.E. Jr. (2011a): Influence of some potential pre- dation risk factors and interaction between predation risk and cost of fleeing on escape by the lizard Sce- loporus virgatus. Ethology 117: 620-629. Cooper, W.E. Jr. (2011b): Age, sex and escape behaviour in the Striped Plateau Lizard (Sceloporus virgatus) and the Mountain Spiny Lizard (S. jarrovi), with a review of age and sex effects on escape by lizards. Behaviour 148: 1215-1238. Cooper, W.E. Jr., Avalos, A. (2010): Escape decisions by the syntopic congeners Sceloporus jarrovii and S. vir- gatus: comparative effects of perch height and of predator approach speed, persistence, and direction of turning. J. Herpetol. 44: 425-430. Cooper, W.E. Jr., Caldwell, J.P., Vitt, L.J. (2008): Effective crypsis and its maintenance by immobility in Crau- gastor frogs. Copeia 2008: 527-532. Cooper, W.E. Jr., Frederick, W.G. (2007): Optimal flight initiation distance. J. Theor. Biol. 244: 59-67. Cooper, W.E. Jr., Hawlena, D., Pérez-Mellado, V. (2009): Effects of predation risk factors on escape behavior by Balearic lizards (Podarcis lilfordi) in relation to opti- mal escape theory. Amphibia-Reptilia 30: 99-110. Cooper, W.E. Jr., Pérez-Mellado, V. (2011): Escape by the Balearic lizard (Podarcis lilfordi) is affected by eleva- tion of an approaching predator, but not by some other potential predation risk factors. Acta Herpetol. 6: 247-259. Cooper, W.E. Jr., Sherbrooke, W.C. (2010): Crypsis influ- ences escape decisions in the round-tailed horned liz- ard (Phrynosoma modestum). Can. J. Zool. 88 1003- 1010. Cooper, W.E. Jr., Vitt, L.J., Caldwell, J.P., Fox, S.F. (2001): Foraging modes of some American lizards: Relation- ships among measurement variables and discreteness of modes. Herpetologica 57: 65-76. Gadsden, H., Lara-Reséndiz, R.A., Minjarrez-Flores, N.F., Gatica-Colima, A., Smith, G.R. (2021): Thermoregula- tion in a saxicolous population of the lizard Urosaurus ornatus from the northern Chihuahuan Desert, Mexi- co. Amphibia-Reptilia. 42: 153-166 Gilbert, A.L., Miles, D.B. (2016): Food, temperature and endurance: effects of food deprivation on the thermal sensitivity of physiological performance. Funct. Ecol. 30: 1790-1799. Gilbert, A.L., Miles, D.B. (2017): Natural selection on thermal preference, critical thermal maximum and locomotor performance. Proc. R. Soc. 284B: 20170536. Haenel, G.J. (2007): Phylogeography of the tree lizard, Urosaurus ornatus: responses of populations to past climate change. Mol. Ecol. 16: 4321-4334. Haenel, G.J. (2018): Local adaptation of tree lizards to canyon dwelling. Evol. Ecol. 32: 315-334. Hamilton, P.S., Gaalema, D.E., Sullivan, B.K. (2008): Short-term changes in dorsal reflectance for back- ground matching in Ornate Tree Lizards (Urosaurus ornatus). Amphibia-Reptilia 29: 473-477. Herrel, A., James, R.S., van Damme, R. (2007): Fight wer- sus flight: physiological basis for temperature-depend- ent behavioral shifts in lizards. J. Exp. Biol. 210: 1762- 1767. Herrel, A., Meyers, J.J., Vanhooydonck, B. (2001): Cor- relations between habitat use and body shape in a phrynosomatid lizard (Urosaurus ornatus): a popula- tion-level analysis. Biol. J. Linn. Soc. 74: 305-314. James, S.E., M’Closkey, R.T. (2002): Patterns of microhab- itat use in a sympatric lizard assemblage. Can. J. Zool. 80: 2226-2234. Keehn, J.E., Feldman, C.R. (2018): Predator attack rates and anti-predator behavior of side-blotched lizards (Uta stansburiana) at southern California wind farms, USA. Herpetol. Conserv. Biol. 13: 194-204. Kopena, R., Herczeg, G., López, P., Martin, J. (2015): Escape strategy of Schreiber’s green lizards (Lacerta schreiberi) is determined by environment but not sea- son or sex. Behaviour 152: 1527-1542. Lemos-Espinal, J.A., Smith, G.R., Ballinger, R.E. (1997): Temperature relationships of the tropical tree lizard (Urosaurus bicarinatus) from the Cañón del Zopilote, Guerrero, México. Herpetol. J. 7: 26-27. Majláth, I., Majláthová, V. (2009): Escape behavior of the green lizard (Lacerta viridis) in the Slovak Karst. Acta Ethol. 12: 99-103. Martin, J., López, P. (2000): Fleeing to unsafe refuges: effects of conspicuousness and refuge safety on the 57Flight initiation distance of U. ornatus escape decisions of the lizard Psammodromus algirus. Can. J. Zool. 78: 265-270. Morris, C.L., Lattanzio, M.S. (2020): Intraspecific varia- tion in tree lizard escape behaviour in relation to hab- itat and temperature. Behaviour 157: 185-204. Reeder, T.W., Wiens, J.J. (1996): Evolution of the lizard family Phrynosomatidae as inferred from diverse types of data. Herpetol. Monogr. 10: 43-84. Salido, C.A., Vicente, N.S. (2019): Sex and refuge distance influence escape decision in a Liolaemus lizard when it is approached by a terrestrial predator. Behaviour 156: 909-925. Smith, G.R. (1996a): Correlates of approach distance in the striped plateau lizard (Sceloporus virgatus). Herpe- tol. J. 6: 56-58. Smith, G.R. (1996b): Habitat use and its effect on body size distribution of the tree lizard, Urosaurus ornatus. J. Herpetol. 30: 528-530. Smith, G.R., Lemos-Espinal, J.A. (2005): Comparative escape behavior of four species of Mexican phrynoso- matid lizards. Herpetologica 61: 225-232. Taylor, J.N., Ternes, W.M., Lattanzio, M.S. (2018): Natural selection favors local specialization in a widespread habitat generalist. Evolution 72: 2090-2099. Van Damme, R., Vanhooydonck, B. (2001): Origins of interspecific variation in lizard sprint capacity. Funct. Ecol. 15: 186-202. Vanhooydonck, B., Herrel, A., Irschick, D.J. 2007. Deter- minants of sexual differences in escape behavior in lizards of the genus Anolis: a comparative approach. Int. Comp. Biol. 47: 200-210. Wiens, J.J. (1993): Phylogenetic systematics of the tree liz- ards (genus Urosaurus). Herpetologica 49: 399-420. Ydenberg, R.C., Dill, L.M. (1986): The economics of flee- ing for predators. Adv. Stud. Behav. 16: 229-249. Zucker, N. (1989): Dorsal darkening and territoriality in a wild population of the Tree Lizard, Urosaurus ornatus. J. Herpetol. 23: 389-398.