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The effect of environmental provisioning on stress levels in captive green anole (Anolis carolinensis)

Published online by Cambridge University Press:  03 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 and requests for reprints author: [email protected]
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Abstract

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In response to an increased awareness concerning the welfare of captive animals, several studies have investigated the effect of provisions on stress levels in model species, such as small mammals, birds and fish. In contrast, reptiles have received less attention. Although many reptilian species are becoming increasingly popular in the pet trade and are frequently used as model species in various branches of biology and a number of studies have explored how they react to stress in different contexts (eg social, predatory), little is known about how they react to stress induced by housing conditions or experimental treatments. In this study, we quantified the effect of provision of perches and leaves as refuges (provisioned) on the behaviour, morphology and physiology of the green anole (Anolis carolinensis). Our results showed that increased or decreased structural complexity of the cage had no effect on body mass, tail-base width, heterophil to lymphocyte ratios (H/L ratios), brightness, body colour, behaviour and faecal corticosterone metabolite (FCM) levels for both males and females in the experimental treatments (provisioned or deprived situation). 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
© 2018 Universities Federation for Animal Welfare

References

Ackermann, L 1997 The Biology, Husbandry and Healthcare of Reptiles, Volume 1 pp 291293. TFH Publications Inc: USAGoogle Scholar
Almli, LM and Burghardt, GM 2006 Environmental enrichment alters the behavioral profile of ratsnakes (Elaphe). Journal of Applied Animal Welfare Science 9: 85109. https://doi.org/10.1207/s15327604jaws0902_1CrossRefGoogle ScholarPubMed
Asher, L, Davies, GTO, Bertenshaw, CE, Cox, MAA and Bateson, M 2009 The effects of cage volume and cage shape on the condition and behaviour of captive European starlings (Sturnus vulgaris). Applied Animal Behaviour Science 116: 286294. https://doi.org/10.1016/j.applanim.2008.10.008CrossRefGoogle Scholar
Baeckens, S, Huyghe, K, Palme, R and Van Damme, R 2017 Chemical communication in the lacertid lizard Podarcis muralis: the functional significance of testosterone. Acta Zoologica (Stockholm)98: 94-103. https://doi.org/10.1111/azo.12160CrossRefGoogle Scholar
Blumstein, D, Evans, C and Daniel, J 2006 JWatcher 1.0. http://www.jwatcher.ucla.eduGoogle Scholar
Carlton, FC 1903 The color changes in the skin of the so-called Florida Chameleon, Anolis Carolinensis. Proceedings of the American Academy of Arts and Sciences 39(10): 259276. https://doi.org/10.2307/20021878CrossRefGoogle Scholar
Carstens, E and Moberg, GP 2000 Recognizing pain and dis-tress in laboratory animals. ILAR Journal 41: 6271. https://doi.org/10.1093/ilar.41.2.62CrossRefGoogle ScholarPubMed
Case, BC, Lewbart, GA and Doerr, PD 2005 The physiologi-cal and behavioral impacts of and preference for an enriched envi-ronment in the eastern box turtle (Terrapene carolina carolina). Applied Animal Behavior Science 92: 353365. https://doi.org/10.1016/j.applanim.2004.11.011CrossRefGoogle Scholar
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
Cooper, JJ, Odberg, F and Nicol, CJ 1996 Limitations on the effectiveness of environmental improvement in reducing stereo-typic behavior in bank voles (Clethrionomys glareolus). Applied Animal Behavior Science 48: 237248. https://doi.org/10.1016/0168-1591(95)01020-3CrossRefGoogle 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
Dawkins, MS, Cook, PA, Whittingham, MJ, Mansell, KA and Harper, AE 2003 What makes free-range broiler chickens range? In situ measurement of habitat preference. Animal Behaviour 66:151160. https://doi.org/10.1006/anbe.2003.2172CrossRefGoogle Scholar
De Jong, IC, Prelle, IT, van de Burgwal, JA, Lambooij, E, Korte, SM, Blokhuis, JJ and Koolhaas, JM 2000 Effects of envi-ronmental enrichment on behavioral responses to novelty, learning, and the circadian rhythm in cortisol in growing pigs. Physiology & Behavior 68: 571578. https://doi.org/10.1016/S0031-9384(99)00212-7CrossRefGoogle Scholar
Denardo, D 2006 Stress in captive reptiles. In: Mader, DR (ed) Reptile Medicine and Surgery pp 119123. Saunders Elsevier: Missouri, USA. https://doi.org/10.1016/B0-72-169327-X/50013-4CrossRefGoogle 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
Garner, JP 2005 Stereotypies and other abnormal repetitive behaviors: Potential impact on validity, reliability, and replicability of scientific outcomes. ILAR Journal: 46: 106-117. https://doi.org/10.1093/ilar.46.2.106CrossRefGoogle Scholar
Gilman, C 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
Greenberg, N 2003 Sociality, stress, and the corpus striatum of the green anolis lizard. Physiology & behavior 79(3): 429440. https://doi.org/10.1016/S0031-9384(03)00162-8CrossRefGoogle ScholarPubMed
Greenberg, N, Chen, T and Crews, D 1984 Social status, gonadal state, and the adrenal stress response in the lizard, Anolis carolinensis. Hormones and Behavior 18: 111. https://doi.org/10.1016/0018-506X(84)90045-XCrossRefGoogle ScholarPubMed
Greenberg, N and Crews, D 1990 Endocrine and behavioral responses to aggression and social dominance in the green anole lizard, Anolis carolinensis. General and Comparative Endocrinology 77(2): 246255. https://doi.org/10.1016/0016-6480(90)90309-ACrossRefGoogle ScholarPubMed
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 1977 Effects of simulated predation on tonic immobili-ty in Anolis carolinensis: The role of eye contact. Bulletin of the Psychonomic Society 9(4): 239242. https://doi.org/10.3758/BF03336987CrossRefGoogle Scholar
Hennig, CW, Dunlap, WP and Gallup, GG 1976 The effect of distance between predator and prey and the opportunity to escape on tonic immobility in ‘Anolis carolinensis. The Psychological Record 26: 313. https://doi.org/10.1007/BF03394393CrossRefGoogle Scholar
Henning, 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
Kalliokoski, O, Timm, JA, Ibsen, IB, Hau, J, Frederiksen, AMB and Bertelsen, MF 2012 Fecal glucocorticoid response to environmental stressors in green iguanas (Iguana iguana). General and Comparative Endocrinology 177(1): 9397. https://doi.org/10.1016/j.ygcen.2012.02.017CrossRefGoogle ScholarPubMed
Lailvaux, SP and Irschick, DJ 2007 Effects of temperature and sex on jump performance and biomechanics in the lizard Anolis carolinensis. 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 plasma corticosterone following restraint stress in juvenile alligators. Journal of Experimental Zoology283: 559-565. https://doi.org/10.1002/(SICI)1097-010X(19990501)283:6<559::AID-JEZ7>3.0.CO;2-4CrossRef3.0.CO;2-4>Google 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. The American Midland Naturalist 79(1): 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 2: 338339. https://doi.org/10.2307/1442973CrossRefGoogle Scholar
Mar Sanchez, M, Aguado, F, Sanchez-Toscano, F and Saphier, D 1998 Neuroendocrine and immunocytochemical demonstrations of decreased hypothalamo-pituitary-adrenal axis responsiveness to restraint stress after long-term social isolation. Endocrinology 139:579587. https://doi.org/10.1210/endo.139.2.5720CrossRefGoogle 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
Meylan, S, Dufty, AM and Clobert, J 2003 The effect of trans-dermal corticosterone application on plasma corticosterone lev-els in pregnant Lacerta vivipara. Comparative Biochemistry and Physiology A 134: 497503. https://doi.org/10.1016/S1095-6433(02)00343-4CrossRefGoogle Scholar
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 loco-motor approach on feeding kinematics in the green anole (Anolis carolinensis). Journal of Experimental Zoology 309A: 563-567. https://doi.org/10.1002/jez.484CrossRefGoogle Scholar
Morgan, KN and Tromborg, CT 2007 Sources of stress in cap-tivity. Applied Animal Behavior 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. 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
Näslund, J, Rosengren, M, Del Villar, D, Gansel, L, Norrgård, JR, Persson, L, Winkowski, JJ and Kvingedal, E 2013 Hatchery tank enrichment affects cortisol levels and shel-ter-seeking in Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 70(4): 585590. https://doi.org/10.1139/cjfas-2012-0302CrossRefGoogle Scholar
Newberry, RC and Shackleton, DM 1997 Use of visual cover by domestic fowl: a Venetian blind effect? Animal Behavior 54: 387395. https://doi.org/10.1006/anbe.1996.0421CrossRefGoogle ScholarPubMed
Palme, R, Rettenbacher, S, Touma, C, El-Bahr, SM and Möstl, E 2005 Stress hormones in mammals and birds: Comparative aspects regarding metabolism, excretion and nonin-vasive measurement in fecal samples. Trends in Comparative Endocrinology and Neurobiology. 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, MF and Lepschy, M 2013 Steroid extraction: Get the best out of faecal samples. Wiener Tierarztliche Monatsschrift - Veterinary Medicine Austria 100: 238246Google Scholar
Pfister, HP 1979 The glucocorticosterone response to novelty as a psychological stressor. Physiology & Behavior 23: 649652. https://doi.org/10.1016/0031-9384(79)90154-9CrossRefGoogle ScholarPubMed
Phillips, CJC, Jiang, Z, Hatto, AJ, Tribe, A, Bouar, MlE, Guerlin, M and Murray, PJ 2011 Environmental enrichment for captive Eastern blue-tongue lizards (Tiliqua scincoides). Animal Welfare 20: 377384CrossRefGoogle Scholar
Rittenhouse, CD, Millspaugh, JJ, Washburn, BE and Hubbard, MW 2005 Effects of radiotransmitters on fecal gluco-corticoid metabolite levels of three-toed box turtles in captivity. Wildlife Society Bulletin 33: 706713. https://doi.org/10.2193/0091-7648(2005)33[706:EOROFG]2.0.CO;2CrossRefGoogle Scholar
Rosier, RL and Langkilde, T 2011a Does environmental enrich-ment really matter? A case study using the eastern fence lizard, Sceloporus undulates. Applied Animal Behavior Science 131: 7176. https://doi.org/10.1016/j.applanim.2011.01.008CrossRefGoogle Scholar
Rosier, RL and Langkilde, T 2011b In response to the letter to the editor regarding the article: Does environmental enrichment really matter? A case study using the eastern fence lizard, Sceloporus undulates. Applied Animal Behavior Science 135: 171172. https://doi.org/10.1016/j.applanim.2011.08.011CrossRefGoogle Scholar
Saad, AH and Elridi, R 1988 Endogenous corticosteroids medi-ate seasonal cyclic changes in immunity of lizards. Immunobiology 177: 390403. https://doi.org/10.1016/S0171-2985(88)80007-XCrossRefGoogle 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
Taylor, JD and Hadley, ME 1970 Chromatophores and color change in the lizard, Anolis carolinensis. Cell and Tissue Research 104(2): 282294. https://doi.org/10.1007/BF00309737Google ScholarPubMed
Therrien, CL, Gaster, L, Cunningham-Smith, P and Manire, CA 2007 Experimental evaluation of environmental enrichment of sea turtles. Zoo Biology 26: 407416. https://doi.org/10.1002/zoo.20145CrossRefGoogle Scholar
Touma, C and Palme, R 2005 Measuring fecal glucocorticoid metabolites in mammals and birds: The importance of validation. Annals of the New York Academy of Sciences 1046: 5474. https://doi.org/10.1196/annals.1343.006CrossRefGoogle ScholarPubMed
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
Townsend, P 1997 Use of in-cage shelters by laboratory rats. Animal Welfare 6: 95103Google Scholar
Vroonen, J, Vervust, B, Fulgione, D, Maselli, V and Van Damme, R 2012 Physiological color change in the Moorish gecko, Tarentola mauritanica (Squamata: Gekkonidae): effects of background, light, and temperature. Biological Journal of the Linnean Society 107: 182191. https://doi.org/10.1111/j.1095-8312.2012.01915.xCrossRefGoogle 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: 210218. https://doi.org/10.1016/j.brainresbull.2005.06.029CrossRefGoogle Scholar
Weinberg, J and Wong, R 1986 Adrenocortical responsiveness to novelty in the hamster. Physiology & Behavior 37: 669672. https://doi.org/10.1016/0031-9384(86)90170-8CrossRefGoogle ScholarPubMed
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