Abstract
Males and females often differ in use of antipredator behaviors, particularly when antipredator behavior comes at the cost of missed mating opportunities or territory defense. When using thermally suboptimal refugia, ectotherms are especially vulnerable to these costs, as their performance is linked to body temperature. To flee from predators, semi-aquatic Anolis lizards dive underwater for long periods and rebreathe from a bubble of air. We hypothesized that using aquatic refugia would result in body heat loss, that dive duration is influenced by sex, and that oxygen consumption when diving would help explain sex differences. We tested these hypotheses by measuring dive length and body temperatures in A. aquaticus, and by recording oxygen consumption and final oxygen partial pressure during controlled dives in several semi-aquatic Anolis species. Not only was there a significant thermal cost to diving, but A. aquaticus males and females appeared to tolerate different levels of this cost: males re-emerged from water more quickly and at higher body temperatures than did females. Body temperature decreased according to an exponential decay function, dropping up to 6 °C in 5 min. Oxygen consumption rates in semi-aquatic anoles were primarily explained by the expected allometric scaling relationship with mass and, therefore, are unlikely to lead to sex differences in physiological limits to dive times. Instead, shorter male dives may help them maintain physiological performance, mating opportunities or territory defense. Antipredator diving behavior is physiologically costly but undoubtedly beneficial to both sexes, highlighting the need for further study of sex-based antipredator optimization.
Significance statement
To avoid predators, semi-aquatic Anolis lizards can dive underwater and remain there for an extended time by rebreathing a bubble of air over their heads. In this study, we reveal that diving to escape predators also comes with a cost: submersion in water reduces lizard body temperatures. Reduced body temperature can impair a lizard’s ability to move quickly and defend mates or territories, suggesting that there may be divergent diving behaviors in males and females. Our findings confirm that males do indeed spend less time underwater than females. We measured oxygen consumption during dives, and our data suggest that sex differences in diving behavior are unrelated to oxygen use. This study sheds light on the sex-specific balance of antipredator behaviors and the maintenance of optimal body temperatures, and more broadly contributes insight into adaptive responses to environmental challenges.
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Data availability
All data are freely available from the Binghamton ORB repository, https://orb.binghamton.edu/bio_fac/27
References
Angilletta MJJ, Niewiarowski PH, Navas CA (2002) The evolution of thermal physiology in endotherms. J Therm Biol 27:249–268. https://doi.org/10.2741/e148
Avery RA, Bedford JD, Newcombe CP (1982) The role of thermoregulation in lizard biology: predatory efficiency in a temperate diurnal basker. Behav Ecol Sociobiol 11:261–267
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using {lme4}. J Stat Softw 67:1–48
Blanchard RJ, Agullana R, McGee L, Weiss S, Blanchard DC (1992) Sex differences in the incidence and sonographic characteristics of antipredator ultrasonic cries in the laboratory rat (Rattus norvegicus). J Comp Psychol 106:270–277. https://doi.org/10.1037/0735-7036.106.3.270
Bennett AF (1988) Structural and functional determinates of metabolic rate. Am Zool 28:699–708. https://doi.org/10.1093/icb/28.2.699
Boccia CK, Swierk L, Ayala-Varela FP et al (2021) Repeated evolution of underwater rebreathing in diving Anolis lizards. Curr Biol 31:2947-2954.e4. https://doi.org/10.1016/j.cub.2021.04.040
Boyer JFF, Swierk L (2017) Rapid body color brightening is associated with exposure to a stressor in an Anolis lizard. Can J Zool 95:213–219. https://doi.org/10.1139/cjz-2016-0200
Brunel-Pons O, Alem S, Greenfield MD (2011) The complex auditory scene at leks: Balancing antipredator behaviour and competitive signalling in an acoustic moth. Anim Behav 81:231–239. https://doi.org/10.1016/j.anbehav.2010.10.010
Carrascal LM, López P, Martín J, Salvador A (1992) Basking and antipredator behaviour in a high altitude lizard: Implications of heat-exchange rate. Ethology 92:143–154. https://doi.org/10.1111/j.1439-0310.1992.tb00955.x
Cooper WE (1999) Tradeoffs between courtship, fighting, and antipredatory behavior by a lizard, Eumeces laticeps. Behav Ecol Sociobiol 47(1–2):54–59. https://doi.org/10.1007/s002650050649
Cooper WE Jr (2011) Age, sex and escape behaviour in the Striped Plateau Lizard (Sceloporus virgatus) and the Mountain Spiny Lizard (S. jarrovii), with a review of age and sex effects on escape by lizards. Behaviour 148:1215–1238. https://doi.org/10.1163/000579511X598334
Cooper WE Jr, Wilson DS (2007) Sex and social costs of escaping in the striped plateau lizard Sceloporus virgatus. Behav Ecol 18:764–768. https://doi.org/10.1093/beheco/arm041
Curlis JD, Macklem DC, Davis R, Cox CL (2016) Sex-specific antipredator response to auditory cues in the black spiny-tailed iguana. J Zool 299:68–74. https://doi.org/10.1111/jzo.12326
Daniels CB, Heatwole H, Oakes N (1987) Heating and cooling rates in air and during diving of the Australian water skink, Sphenomorphus quoyii. Comp Biochem Physiol A 87:487–492. https://doi.org/10.1016/0300-9629(87)90155-1
DeWitt CB (1967) Precision of thermoregulation and its relation to environmental factors in the desert iguana, Dipsosaurus dorsalis. Physiol Zool 40:49–66
Dorcas ME, Hopkins WA, Roe JH (2004) Effects of body mass and temperature on standard metabolic rate in the Eastern Diamondback Rattlesnake (Crotalus adamanteus). Copeia 2004:145–151
Giesbrecht GG, Lockhart TL, Bristow GK, Steinman AM (2005) Thermal effects of dorsal head immersion in cold water of nonshivering humans. J Appl Physiol 99:1958–1964
Grigg GC, Alchin J (1976) The role of the cardiovascular system in thermoregulation of Crocodylus johnstoni. Physiol Zool 49:24–36
Hayward A, Pajuelo M, Haase CG, Anderson DM, Gillooly JF (2016) Common metabolic constraints on dive duration in endothermic and ectothermic vertebrates. PeerJ 4(e2569). https://doi.org/10.7717/peerj.2569
Herczeg G, Herrero A, Saarikivi J, Gonda A, Jäntti M, Merilä J (2008) Experimental support for the cost-benefit model of lizard thermoregulation: the effects of predation risk and food supply. Oecologia 155:1–10. https://doi.org/10.1007/s00442-007-0886-9
Huey RB (1982) Temperature, physiology, and the ecology of reptiles. In: Gans C, Pough F (eds) Biology of the Reptilia, vol. 12, Physiology C. Academic Press, London, pp 25–91
Huey RB (1983) Natural variation in body temperature and physiological performance in a lizard (Anolis cristatellus). In: Rhodin AGJ, Miyata K (eds) Advances in Herpetology and Evolutionary Biology: Essays in Honor of Ernest E. Williams. Museum of Comparative Zoology, Cambridge, pp 484–490
John-Alder HB, Barnhart MC, Bennett AF (1989) Thermal sensitivity of swimming performance and muscle contraction in northern and southern populations of tree frogs (Hyla crucifer). J Exp Biol 142:357–372. https://doi.org/10.1242/jeb.142.1.357
Johnson CE (1925) Kingfisher and Cooper’s Hawk. Auk 42:585–586
Johnson JC, Sih A (2007) Fear, food, sex and parental care: a syndrome of boldness in the fishing spider, Dolomedes triton. Anim Behav 74:1131–1138. https://doi.org/10.1016/j.anbehav.2007.02.006
Johnston RF (1957) Adaptation of salt marsh mammals to high tides. J Mammal 38:529–531
Lailvaux SP (2007) Interactive effects of sex and temperature on locomotion in reptiles. Integr Comp Biol 47:189–199. https://doi.org/10.1093/icb/icm011
Lailvaux SP, Irschick DJ (2007) Effects of temperature and sex on jump performance and biomechanics in the lizard Anolis carolinensis. Funct Ecol 21:534–543. https://doi.org/10.1111/j.1365-2435.2007.01263.x
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. https://doi.org/10.1086/376423
Lea AJ, Blumstein DT (2011) Age and sex influence marmot antipredator behavior during periods of heightened risk. Behav Ecol Sociobiol 65:1525–1533. https://doi.org/10.1007/s00265-011-1162-x
Leal M (1999) Honest signalling during prey–predator interactions in the lizard Anolis cristatellus. Anim Behav 58:521–526
Lelièvre H, Rivalan P, Delmas V, Ballouard JM, Bonnet X, Blouin-Demers G, Lourdais O (2013) The thermoregulatory strategy of two sympatric colubrid snakes affects their demography. Popul Ecol 55:585–593. https://doi.org/10.1007/s10144-013-0388-z
Lenth RV (2022) emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.7.4–1. https://CRAN.R-project.org/package=emmeans
Márquez CMM, Márquez LD (2009) Reproductive biology in the wild and in captivity of Anolis aquaticus (Sauria: Polychrotidae) in Costa Rica. Bol Téc Ser Zool 8:50–73
Márquez C, Manuel Mora J, Bolaños F, Rea S (2005) Field population biology of Anolis aquaticus, Sauria: Polychridae in Costa Rica. Ecol Appl 4:59–69. https://doi.org/10.21704/rea.v4i1-2.299
Martín J, López P (1999) An experimental test of the costs of antipredatory refuge use in the wall lizard, Podarcis muralis. Oikos 84:499–505
Martín J, López P, Cooper WE Jr (2003) Loss of mating opportunities influences refuge use in the Iberian rock lizard, Lacerta monticola. Behav Ecol Sociobiol 54:505–510. https://doi.org/10.1007/s00265-003-0659-3
Mateo JM (2007) Ecological and hormonal correlates of antipredator behavior in adult Belding’s ground squirrels (Spermophilus beldingi). Behav Ecol Sociobiol 62:37–49. https://doi.org/10.1007/s00265-007-0436-9
McConnachie S (2014) The effects of temperature on oxygen consumption in the lizard Pseudocordylus melanotus from Suikerbosrand Nature Reserve. Afr J Herpetol 63:57–69. https://doi.org/10.1080/21564574.2014.892901
Milinski M, Heller R (1978) Influence of a predator on the optimal foraging behavior of sticklebacks (Gasterosteus aculeatus L.). Nature 275:642–644
Nagy KA (2005) Field metabolic rate and body size. J Exp Biol 9:1621–1625. https://doi.org/10.1242/jeb.01553
Pinheiro J, Bates D, DebRoy S, Sarkar D (2021) nlme: linear and nonlinear mixed effects models. R package version 3.1-152. https://CRAN.R-project.org/package=nlme
Polis GA, Barnes JD, Seely MK, Henschel JR, Margit M (1998) Predation as a major cost of reproduction in Namib Desert tenebrionid beetles. Ecology 79(7):2560–2566
Polo V, López P, Martín J (2005) Balancing the thermal costs and benefits of refuge use to cope with persistent attacks from predators: A model and an experiment with an alpine lizard. Evol Ecol Res 7:23–35
Power J, SimõesRé A, Barwood M, Tikuisis P, Tipton M (2015) Reduction in predicted survival times in cold water due to wind and waves. Appl Ergon 49:18–24
Putman BJ, Azure KR, Swierk L (2018) Dewlap size in male water anoles associates with consistent inter-individual variation in boldness. Curr Zool 65:189–195. https://doi.org/10.1093/cz/zoy041
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Radzio TA, O’Connor MP (2017) Behavior and temperature modulate a thermoregulation-predation risk trade-off in juvenile gopher tortoises. Ethology 123:957–965. https://doi.org/10.1111/eth.12695
Samia DSM, Blumstein DT, Stankowich T, Cooper WE Jr (2016) Fifty years of chasing lizards: new insights advance optimal escape theory. Biol Rev 91:349–366. https://doi.org/10.1111/brv.12173
Sannolo M, Ponti R, Carretero MA (2019) Waitin’ on a sunny day: factors affecting lizard body temperature while hiding from predators. J Therm Biol 84:146–153
Savage JM (2002) Norops aquaticus. In: The amphibians and reptiles of Costa Rica: a herpetofauna between two continents, between two seas. The University of Chicago Press, Chicago, p 458
Savage VM, Gillooly JF, Woodruff WH, West GB, Allen AP, Enquist BJ, Brown JH (2004) The predominance of quarter-power scaling in biology. Funct Ecol 18:257–282. https://doi.org/10.1111/j.0269-8463.2004.00856.x
Segall M, Tolley KA, Vanhooydonck B, Measey GJ, Herrel A (2013) Impact of temperature on performance in two species of South African dwarf chameleon, Bradypodion pumilum and B. occidentale. J Exp Biol 216:3828–3836. https://doi.org/10.1242/jeb.092353
Sih A (1980) Optimal behavior: Can foragers balance two conflicting demands? Science 210:1041–1043
Stevenson RD (1985) Body size and limits to the daily range of body temperature in terrestrial ectotherms. Am Nat 125:102–117
Swierk L (2019) Anolis aquaticus (= Norops aquaticus) (Water Anole). Underwater breathing. Herpetol Rev 50:134–135
Swierk L, Graham SP, Langkilde T (2014) The stress of scramble: sex differences in behavior and physiological stress response in a time-constrained mating system. Behav Ecol Sociobiol 68:1761–1768. https://doi.org/10.1007/s00265-014-1784-x
Swierk L, Boyer JFF, Chang J, Petelo M, Drobniak SM (2021) Intrasexual variability of a conspicuous social signal influences attack rate of lizard models in an experimental test. Evol Ecol 35:131–146. https://doi.org/10.1007/s10682-020-10085-7
Talavera JB, Carriere A, Swierk L, Putman BJ (2021) Tail autotomy is associated with boldness in male but not female water anoles. Behav Ecol Sociobiol 75:44. https://doi.org/10.1007/s00265-021-02982-w
Tanis BP, Bott B, Gaston BJ (2018) Sex-based differences in anti-predator response of crickets to chemical cues of a mammalian predator. PeerJ 6:e4923. https://doi.org/10.7717/peerj.4923
Therneau TM (2020) coxme: Mixed Effects Cox Models. R package version 2.2–16. https://CRAN.R-project.org/package=coxme
Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual Selection and the Descent of Man, 1871-1971. Aldine Publishing Company, London, pp 136–179. https://doi.org/10.1097/00129334-200103000-00012
Ultsch GR (1989) Ecology and physiology of hibernation and overwintering among freshwater fishes, turtles and snakes. Biol Rev 64:435–515. https://doi.org/10.1111/j.1469-185x.1989.tb00683.x
van Berkum FH (1986) Evolutionary patterns of the thermal sensitivity of sprint speed in Anolis lizards. Evolution 40:594–604. https://doi.org/10.1111/j.1558-5646.1986.tb00510.x
Vleck D, Bartholomew GA (1979) The relation of oxygen consumption to body size and to heating and cooling in the Galapagos Marine Iguana, Amblyrhynchus cristatus. J Comp Physiol B 132:285–288. https://doi.org/10.1007/BF00799040
Warton DI, Duursma RA, Falster DS, Taskinen S (2012) smatr 3 – an R package for estimation and inference about allometric lines. Methods Ecol Evol 3:257–259. https://doi.org/10.1111/j.2041-210X.2011.00153.x
Weatherhead PJ, Robertson IC (1992) Thermal constraints on swimming performance and escape response of northern water snakes (Nerodia sipedon). Can J Zool 70:94–98. https://doi.org/10.1139/z92-014
Webb JK, Whiting MJ (2005) Why don’t small snakes bask? Juvenile broad-headed snakes trade thermal benefits for safety. Oikos 110:515–522. https://doi.org/10.1111/j.0030-1299.2005.13722.x
Wuthrich KL, Nagel A, Swierk L (2022) Rapid body color change provides lizards with facultative crypsis in the eyes of their avian predators. Am Nat 199:277–290. https://doi.org/10.1086/717678
Xu W, Zhang J, Du S, Dai Q, Zhang W, Luo M, Zhao B (2014) Sex differences in alarm response and predation risk in the fresh water snail Pomacea canaliculata. J Mollus Stud 80:117–122. https://doi.org/10.1093/mollus/eyt054
Ydenberg RC, Dill LM (1986) The economics of fleeing from predators. Adv Stud Behav 16:229–249. https://doi.org/10.1016/S0065-3454(08)60192-8
Yeager LA, Stoner EW, Peters JR, Layman CA (2016) A terrestrial-aquatic food web subsidy is potentially mediated by multiple predator effects on an arboreal crab. J Exp Mar Biol Ecol 475:73–79. https://doi.org/10.1016/j.jembe.2015.10.017
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14. https://doi.org/10.1111/j.2041-210X.2009.00001.x
Acknowledgements
We thank R. Quirós Flores, S. Walter, and the Organization for Tropical Studies for logistical support and two anonymous reviewers for their helpful suggestions.
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This work was supported by an NSERC Discovery Grant (RGPIN-2015-04334) to D.L. Mahler; a NSERC CGS M Grant, and a National Geographic Young Explorer Grant (WW-104ER-17) and Sigma Xi Grant in Aid of Research to CKB; and an Animal Behavior Society Grant, and ASIH Gaige Fund Award, and a Chicago Herpetological Society Grant to AMM.
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This study was approved by animal ethics committees at Binghamton University (IACUC protocols #817-19 and #874-22) and University of Toronto (LACC protocol #20011469). Research permits were obtained from the Ministry of the Environment and Energy, Costa Rica (SINAC-CUS-PI-R-049-2017, R-SINAC-PNI-ACLAP-022-2019, SINAC-ACC-PI-R-064-2019, R-SINAC-PNI-ACLAP-022-2021, and R-SINAC-PNI-ACLAP-003-2022) and Autorización de Recolección en Parques Nacionales Naturales, Colombia (permit #009 de 2017). Mexican fieldwork was conducted on private property with the permission of the Universidad Nacional Autónoma de México.
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Martin, A.M., Boccia, C.K. & Swierk, L. Diving behavior in semi-aquatic Anolis lizards results in heat loss with sex-specific cooling tolerance. Behav Ecol Sociobiol 78, 33 (2024). https://doi.org/10.1007/s00265-024-03448-5
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DOI: https://doi.org/10.1007/s00265-024-03448-5