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Routine handling does not lead to chronic stress in captive green anole (Anolis carolinensis)

Published online by Cambridge University Press:  01 January 2023

G Borgmans*
Affiliation:
Department of Biology, University of Antwerp, Universiteitsplein 1, 2610 Antwerp, Belgium Centre for Research and Conservation, Royal Zoological Society of Antwerp, Antwerp, Belgium
R Palme
Affiliation:
Unit of Physiology, Pathophysiology and Experimental Endocrinology, Department of Biomedical Sciences, University of Veterinary Medicine, Veterinärplatz 1, 1210 Vienna, Austria
A Sannen
Affiliation:
Ethology & Animal Welfare, Agro- & Biotechnology, HUB-ODISEE University College, Hospitaalstraat 21, 9100 Sint-Niklaas, Belgium
H Vervaecke
Affiliation:
Ethology & Animal Welfare, Agro- & Biotechnology, HUB-ODISEE University College, Hospitaalstraat 21, 9100 Sint-Niklaas, Belgium
R Van Damme
Affiliation:
Department of Biology, University of Antwerp, Universiteitsplein 1, 2610 Antwerp, Belgium
*
* Contact for correspondence: glenn.borgmans@uantwerpen.be
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Abstract

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Routine handling has been shown to affect stress levels in a variety of animal species. This could result in a general decrease in welfare and may confound the results of scientific experiments or observations on captive study animals. In reptiles, there seems to be variation in the effects of handling on stress levels. Furthermore, most studies on reptiles only look at the effect of handling in the short term. In this study we quantified the physiological and behavioural impact of being held, twice daily, for 1 min at a time over a three-week period on the green anole (Anolis carolinensis). Measurements were collected at the end of the three-week repeated handling period. Our results showed no effect of repeated handling on body mass, tail-base width, heterophil to lymphocyte ratios (H/L ratios), behaviour and faecal corticosterone metabolite (FCM) levels for both males and females in the experimental treatments (‘handled’, ‘unhandled’). Our study animals did score very highly for several stress-indicating variables in the three weeks preceding the experiments — suggesting that they had experienced considerable stress during capture, transport and temporary housing in the pet store.

Type
Research Article
Copyright
© 2021 Universities Federation for Animal Welfare

References

Avery, R 1974 Storage lipids in the lizard Lacerta vivipara: a quan-titative study. Journal of Zoology 173: 419425. https://doi.org/10.1111/j.1469-7998.1974.tb04124.xCrossRefGoogle Scholar
Balcombe, JP, Barnard, ND and Sandusky, C 2004 Laboratory routines cause animal stress. Journal of the American Association for Laboratory Animal Science 43(6): 42-51Google Scholar
Bauwens, D 1985 Demografische kenmerken en aantalsdynamiek in een populatie van de levendbarende hagedis (Lacerta vivipara). Unpublished doctoral dissertation, Universitaire Instelling Antwerp, Antwerp, Belgium. [Title translation: Demographical characteristics and population dynamics in a population of vivipa-rous lizards (Lacerta vivipara)]Google Scholar
Blumstein, D, Evans, C and Daniel, J 2006 JWatcher 1.0. http://www.jwatcher.ucla.eduGoogle Scholar
Borgmans, G, Palme, R, Sannen, A, Vervaecke, H and Van Damme, R 2018 The effect of environmental provisioning on stress levels in captive green anole (Anolis carolinensis). Animal Welfare 27: 3546. https://doi.org/10.7120/09627286.27.1.035CrossRefGoogle Scholar
Borgmans, G, Palme, R, Sannen, A, Vervaecke, H and Van Damme, R 2019 The effect of cage size on stress levels in captive green anole (Anolis carolinensis). Animal Welfare 28: 455464. https://doi.org/10.7120/09627286.28.4.455CrossRefGoogle Scholar
Cabanac, A and Cabanac, M 2000 Heart rate response to gen-tle handling of frog and lizard. Behavioural Processes 52(2): 8995. https://doi.org/10.1016/S0376-6357(00)00108-XCrossRefGoogle ScholarPubMed
Case, BC, Lewbart, GA and Doerr, PD 2005 The physiologi-cal and behavioural impacts of and preference for an enriched environment in the eastern box turtle (Terrapene carolina carolina). Applied Animal Behaviour Science 92(4): 353365. https://doi.org/10.1016/j.applanim.2004.11.011CrossRefGoogle Scholar
Cash, WB, Holberton, RL and Knight, SS 1997 Corticosterone secretion in response to capture and handling in free-living red-eared slider turtles. General and Comparative Endocrinology, 108: 427433. https://doi.org/10.1006/gcen.1997.6999CrossRefGoogle ScholarPubMed
Chen, X, Niu, C and Pu, L 2007 Effects of stocking density on growth and non-specific immune responses in juvenile soft-shelled turtle (Pelodiscus sinensis). Aquaculture Research 38: 13801386. https://doi.org/10.1111/j.1365-2109.2007.01813.xCrossRefGoogle Scholar
Cree, A, Amey, AP and Whittier, JM 2000 Lack of consistent hormonal responses to capture during the breeding season of the bearded dragon (Pogona barbata). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 126: 275285. https://doi.org/10.1016/S1095-6433(00)00210-5CrossRefGoogle ScholarPubMed
Cree, A, Tyrrell, CL, Preest, MR, Thorburn, D and Guillette, LJ 2003 Protecting embryos from stress: corticosterone effects and the corticosterone response to capture and confinement during pregnancy in a live-bearing lizard (Hoplodactylus maculatus). General and Comparative Endocrinology 134: 316329. https://doi.org/10.1016/S0016-6480(03)00282-XCrossRefGoogle Scholar
Cuthill, IC, Bennett, ATD, Partridge, JC and Maier, EJ 1999 Plumage reflectance and the objective assessment of avian sexual dichromatism. American Naturalist 153: 183200. https://doi.org/10.1086/303160CrossRefGoogle ScholarPubMed
Davis, AK and Maerz, JC 2008 Sex-related differences in hema-tological stress indices of breeding paedomorphic mole salaman-ders. Journal of Herpetology 42: 197201. https://doi.org/10.1670/06-277R2.1CrossRefGoogle Scholar
Donoghue, S, Vidal, J and Kronfeld, D 1998 Growth and mor-phometrics of green iguanas (Iguana iguana) fed four levels of dietary protein. The Journal of Nutrition 128: 25872589. https://doi.org/10.1093/jn/128.12.2587SCrossRefGoogle Scholar
Edson, PH and Gallup, GG 1972 Tonic immobility as a fear response in lizards Anolis carolinensis. Psychonomic Science 26: 2728. https://doi.org/10.3758/BF03337874CrossRefGoogle Scholar
Endler, JA 1990 On the measurement and classification of colour in studies of animal colour patterns. Biological Journal of the Linnean Society 41: 315352. https://doi.org/10.1111/j.1095-8312.1990.tb00839.xCrossRefGoogle Scholar
Farbridge, K and Leatherland, J 1992 Plasma growth hormone levels in fed and fasted rainbow trout (Oncorhynchus mykiss) are decreased following handling stress. Fish Physiology and Biochemistry 10: 6773. https://doi.org/10.1007/BF00004655CrossRefGoogle ScholarPubMed
Foo, J and Lam, T 1993 Serum cortisol response to handling stress and the effect of cortisol implantation on testosterone level in the tilapia, Oreochromis mossambicus. Aquaculture 115: 145158. https://doi.org/10.1016/0044-8486(93)90365-6CrossRefGoogle Scholar
Garner, JP 2005 Stereotypies and other abnormal repetitive behaviors: potential impact on validity, reliability, and replicability of scientific outcomes. ILAR Journal 46: 106117. https://doi.org/10.1093/ilar.46.2.106CrossRefGoogle ScholarPubMed
Gilman, CA and Irschick, DJ 2013 Foils of flexion: the effects of perch compliance on lizard locomotion and perch choice in the wild. Functional Ecology 27: 374381. https://doi.org/10.1111/1365-2435.12063CrossRefGoogle Scholar
Girling, JE and Cree, A 1995 Plasma corticosterone levels are not significantly related to reproductive stage in female common geck-ons (Hoplodactylus maculatus). General and Comparative Endocrinology 100: 273281. https://doi.org/10.1006/gcen.1995.1158CrossRefGoogle Scholar
Gregory, LF and Schmid, JR 2001 Stress responses and sexing of wild Kemp's ridley sea turtles (Lepidochelys kempii) in the north-eastern Gulf of Mexico. General and Comparative Endocrinology 124: 6674. https://doi.org/10.1006/gcen.2001.7683CrossRefGoogle Scholar
Griggio, M, Serra, L, Licheri, D, Campomori, C and Pilastro, A 2009 Moult speed affects structural feather ornaments in the blue tit. Journal of Evolutionary Biology 22: 782792. https://doi.org/10.1111/j.1420-9101.2009.01700.xCrossRefGoogle ScholarPubMed
Hennig, CW and Dunlap, WP 1978 Tonic immobility in Anolis carolinensis: Effects of time and conditions of captivity. Behavioral Biology 23: 7586. https://doi.org/10.1016/S0091-6773(78)91180-XCrossRefGoogle Scholar
Hoffmayer, ER and Parsons, GR 2001 The physiological response to capture and handling stress in the Atlantic sharpnose shark, Rhizoprionodon terraenovae. Fish Physiology and Biochemistry 25: 277285CrossRefGoogle Scholar
Kalliokoski, O, Timm, JA, Ibsen, IB, Hau, J, Frederiksen, A-MB and Bertelsen, MF 2012 Fecal glucocorticoid response to environmental stressors in green iguanas (Iguana iguana). General and Comparative Endocrinology 177: 9397. https://doi.org/10.1016/j.ygcen.2012.02.017CrossRefGoogle ScholarPubMed
Kreger, MD and Mench, JA 1993 Physiological and behavioral effects of handling and restraint in the ball python (Python regius) and the blue-tongued skink (Tiliqua scincoides). Applied Animal Behaviour Science 38: 323336. https://doi.org/10.1016/0168-1591(93)90030-SCrossRefGoogle Scholar
Lailvaux, S and Irschick, D 2007 Effects of temperature and sex on jump performance and biomechanics in the lizard Anolis caroli-nensis. Functional Ecology 21: 534543. https://doi.org/10.1111/j.1365-2435.2007.01263.xCrossRefGoogle Scholar
Lance, VA and Elsey, RM 1999 Plasma catecholamines and plas-ma corticosterone following restraint stress in juvenile alligators. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 283: 559565. https://doi.org/10.1002/(SICI)1097-010X(19990501)283:6<559::AID-JEZ7>3.0.CO;2-43.0.CO;2-4>CrossRefGoogle Scholar
Lance, VA and Lauren, D 1984 Circadian variation in plasma cor-ticosterone in the American alligator, Alligator mississippiensis, and the effects of ACTH injections. General and Comparative Endocrinology 54:17. https://doi.org/10.1016/0016-6480(84)90192-8CrossRefGoogle Scholar
Langkilde, T and Shine, R 2006 How much stress do researchers inflict on their study animals? A case study using a scincid lizard, Eulamprus heatwolei. Journal of Experimental Biology 209: 10351043. https://doi.org/10.1242/jeb.02112CrossRefGoogle ScholarPubMed
Licht, P 1968 Response of the thermal preferendum and heat resistance to thermal acclimation under different photoperiods in the lizard Anolis carolinensis. American Midland Naturalist 79: 149158. https://doi.org/10.2307/2423160CrossRefGoogle Scholar
MacLean, GS, Lee, AK and Wilson, KJ 1973 A simple method of obtaining blood from lizards. Copeia 1973: 338339. https://doi.org/10.2307/1442973CrossRefGoogle Scholar
Mathies, T, Felix, TA and Lance, VA 2001 Effects of trapping and subsequent short-term confinement stress on plasma corti-costerone in the brown treesnake (Boiga irregularis) on Guam. General and Comparative Endocrinology 124: 106114. https://doi.org/10.1006/gcen.2001.7694CrossRefGoogle Scholar
Merchant, M, Fleury, L, Rutherford, R and Paulissen, M 2008 Effects of bacterial lipopolysaccharide on thermoregulation in green anole lizards (Anolis carolinensis). Veterinary Immunology and Immunopathology 125: 176181. https://doi.org/10.1016/j.vetimm.2008.04.014CrossRefGoogle ScholarPubMed
Montgomerie, R 2006 Analyzing colors. In: Hill, GE and McGraw, KJ (eds) Bird Coloration pp 90147 Harvard University Press: Cambridge, MA, USACrossRefGoogle Scholar
Montuelle, SJ, Daghfous, G and Bels, VL 2008 Effect of locomo-tor approach on feeding kinematics in the green anole (Anolis caroli-nensis). Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 309: 563567. https://doi.org/10.1002/jez.484CrossRefGoogle Scholar
Moore, IT, Lemaster, MP and Mason, RT 2000 Behavioural and hormonal responses to capture stress in the male red-sided garter snake, Thamnophis sirtalis parietalis. Animal Behaviour 59:529534. https://doi.org/10.1006/anbe.1999.1344CrossRefGoogle ScholarPubMed
Moore, MC, Thompson, CW and Marler, CA 1991 Reciprocal changes in corticosterone and testosterone levels following acute and chronic handling stress in the tree lizard, Urosaurus ornatus. General and Comparative Endocrinology 81: 217226. https://doi.org/10.1016/0016-6480(91)90006-RCrossRefGoogle ScholarPubMed
Morgan, KN and Tromborg, CT 2007 Sources of stress in cap-tivity. Applied Animal Behaviour Science 102: 262302. https://doi.org/10.1016/j.applanim.2006.05.032CrossRefGoogle Scholar
Morici, LA, Elsey, RM and Lance, VA 1997 Effects of long-term corticosterone implants on growth and immune function in juve-nile alligators, Alligator mississippiensis. The Journal of Experimental Zoology 279: 156162. https://doi.org/10.1002/(SICI)1097-010X(19971001)279:2<156::AID-JEZ6>3.0.CO;2-N3.0.CO;2-N>CrossRefGoogle ScholarPubMed
Möstl, E and Palme, R 2002 Hormones as indicators of stress. Domestic Animal Endocrinology 23: 6774. https://doi.org/10.1016/S0739-7240(02)00146-7CrossRefGoogle ScholarPubMed
Palme, R 2019 Non-invasive measurement of glucocorticoids: advances and problems. Physiology and Behaviour 199: 229243. https://doi.org/10.1016/j.physbeh.2018.11.021CrossRefGoogle ScholarPubMed
Palme, R, Rettenbacher, S, Touma, C, El-Bahr, S and Möstl, E 2005 Stress hormones in mammals and birds: comparative aspects regarding metabolism, excretion, and noninvasive meas-urement in fecal samples. Annals of the New York Academy of Sciences 1040: 162171. https://doi.org/10.1196/annals.1327.021CrossRefGoogle Scholar
Palme, R, Touma, C, Arias, N, Dominchin, M and Lepschy, M 2013 Steroid extraction: get the best out of faecal samples. Wiener Tierarztliche Monatsschrift 100: 238246Google Scholar
Ramsay, JM, Feist, GW, Varga, ZM, Westerfield, M, Kent, ML and Schreck, CB 2009 Whole-body cortisol response of zebrafish to acute net handling stress. Aquaculture 297: 157162. https://doi.org/10.1016/j.aquaculture.2009.08.035CrossRefGoogle ScholarPubMed
Rittenhouse, CD, Millspaugh, JJ, Washburn, BE and Hubbard, MW 2005 Effects of radiotransmitters on fecal glucocorticoid metabolite levels of three-toed box turtles in captivity. Wildlife Society Bulletin 33(2): 706713. https://doi.org/10.2193/0091-7648(2005)33[706:EOROFG]2.0.CO;2CrossRefGoogle Scholar
Romero, LM and Wikelski, M 2002 Exposure to tourism reduces stress-induced corticosterone levels in Galápagos marine iguanas. Biological Conservation 108: 371374. http://dx.doi.org/10.1016/S0006-3207(02)00128-3CrossRefGoogle Scholar
Saad, AH and El Ridi, R 1988 Endogenous corticosteroids mediate seasonal cyclic changes in immunity of lizards. Immunobiology 177: 390403. https://doi.org/10.1016/S0171-2985(88)80007-XCrossRefGoogle ScholarPubMed
Schuett, GW, Taylor, EN, van Kirk, EA and Murdoch, WJ 2004 Handling stress and plasma corticosterone levels in captive male western diamond-backed rattlesnakes (Crotalus atrox). Herpetological Review 35: 229232Google Scholar
Stellar, JE and White, DJ 2010 Social influences on female choice in green anole lizards (Anolis carolinensis). Behavioral Processes 83: 282286. https://doi.org/10.1016/j.beproc.2010.01.005CrossRefGoogle ScholarPubMed
Summers, CH and Greenberg, N 1994 Somatic correlates of adrenergic activity during aggression in the lizard, Anolis carolinen-sis. Hormones and Behavior 28: 2940. https://doi.org/10.1006/hbeh.1994.1003CrossRefGoogle Scholar
Touma, C, Sachser, N, Möstl, E and Palme, R 2003 Effects of sex and time of day on metabolism and excretion of corticos-terone in urine and feces of mice. General and Comparative Endocrinology 130: 267278. https://doi.org/10.1016/S0016-6480(02)00620-2CrossRefGoogle ScholarPubMed
Tyrrell, C and Cree, A 1998 Relationships between corticos-terone concentration and season, time of day and confinement in a wild reptile (tuatara, Sphenodon punctatus). General and Comparative Endocrinology 110: 97108. https://doi.org/10.1006/gcen.1997.7051CrossRefGoogle Scholar
Vervust, B, Lailvaux, SP, Grbac, I and Van Damme, R 2008 Do morphological condition indices predict locomotor perform-ance in the lizard Podarcis sicula? Acta Oecologica 34: 244251. https://doi.org/10.1016/j.actao.2008.05.012CrossRefGoogle Scholar
Walberg, J 2001 White blood cell counting techniques in birds. Seminars in Avian and Exotic Pet Medicine 10: 7276. https://doi.org/10.1053/saep.2001.22051CrossRefGoogle Scholar
Waters, RP, Emerson, AJ, Watt, MJ, Forster, GL, Swallow, JG and Summers, CH 2005 Stress induces rapid changes in cen-tral catecholaminergic activity in Anolis carolinensis: restraint and forced physical activity. Brain Research Bulletin 67(3): 210218. https://doi.org/10.1016/j.brainresbull.2005.06.029CrossRefGoogle Scholar
Woodley, SK and Moore, MC 2002 Plasma corticosterone response to an acute stressor varies according to reproductive condition in female tree lizards (Urosaurus ornatus). General and Comparative Endocrinology 128(2): 143148. https://doi.org/10.1016/S0016-6480(02)00068-0CrossRefGoogle Scholar
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