[en] The interest in the welfare of zoo animals, from both the public and the scientific community, has long been biased towards mammals. However, growing evidence of the complex behavioural repertoires of less charismatic animals, such as reptiles, reveals the necessity to better comply with their welfare needs in captivity. Here, we present the effects of an enclosure change towards a more natural habitat in captive Galapagos tortoises (Chelonoidis spp.) held at ZSL London Zoo. Using behavioural observations, we found that the tortoises habituated to their new enclosure in six days. This represents the first quantification of habituation latency to a new enclosure in a reptile model to our knowledge—which is important information to adapt policies governing animal moves. The tortoises expressed time budgets more similar to those of wild individuals after their transition to the new enclosure. Interestingly, the hierarchy between the individuals was inverted and more stable after this change in environment. The tortoises interacted less often, which led to a decrease in the frequency of agonistic encounters. We also found that higher ambient sound volume was associated with increased likelihood of interactions turning into fights. Taken together, our results demonstrate the potential of appropriate enclosure design to improve reptile welfare.
Disciplines :
Zoology
Author, co-author :
Fieschi-Méric, Léa ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS)
Ellis, Charlotte
Servini, Francesca
Tapley, Benjamin
Michaels, Christopher J.
Language :
English
Title :
An Improvement in Enclosure Design Can Positively Impact Welfare, Reduce Aggressiveness and Stabilise Hierarchy in Captive Galapagos Giant Tortoises
Caccone A. Gibbs J.P. Ketmaier V. Suatoni E. Powell J.R. Origin and evolutionary relationships of giant Galapagos tortoises Proc. Natl. Acad. Sci. USA 1999 96 13223 13228 10.1073/pnas.96.23.13223 10557302
Caccone A. Gentile G. Gibbs J.P. Fritts T.H. Snell H.L. Betts J. Powell J.R. Phylogeography and History of Giant Galapagos Tortoises Evolution 2002 56 2052 2066 10.1111/j.0014-3820.2002.tb00131.x 12449492
Ciofi C. Milinkovitch M. Gibbs J.J. Caccone A.A. Powell J.J. Microsatellite analysis of genetic divergence among populations of giant Galápagos tortoises Mol. Ecol. 2002 11 2265 2283 10.1046/j.1365-294X.2002.01617.x 12406238
Caccone A. Evolution and phylogenetics Galapagos Giant Tortoises Gibbs J.P. Cayot L.J. Aguilera W.T. Academic Press Cambridge, MA, USA 2021 117 138 10.1016/B978-0-12-817554-5.00019-8
Kehlmaier C. Albury N.A. Steadman D.W. Graciá E. Franz R. Fritz U. Ancient mitogenomics elucidates diversity of extinct West Indian tortoises Sci. Rep. 2021 11 3224 10.1038/s41598-021-82299-w
IUCN The IUCN Red List of Threatened Species 2021 Available online: https://www.iucnredlist.org/es (accessed on 30 May 2022)
Cayot L.J. The history of Galapagos tortoise conservation Galapagos Giant Tortoises Gibbs J.P. Cayot L.J. Aguilera W.T. Academic Press Cambridge, MA, USA 2021 333 353 10.1016/B978-0-12-817554-5.00008-3
Toral-Granda M.V. Causton C.E. Jäger H. Trueman M. Izurieta J.C. Araujo E. Cruz M. Zander K. Izurieta A. Garnett S.T. Alien species pathways to the Galapagos Islands, Ecuador PLoS ONE 2017 12 e0184379 10.1371/journal.pone.0184379
Frazier J. The Galapagos: Island home of giant tortoises Galapagos Giant Tortoises Gibbs J.P. Cayot L.J. Aguilera W.T. Academic Press Cambridge, MA, USA 2021 3 21 10.1016/B978-0-12-817554-5.00004-6
Galapagos Conservancy 2021 Outrage at Massacre of Giant Tortoises in Galápagos. Published 13 October 2021 Available online: https://www.galapagos.org/newsroom/outrage-at-massacre-of-giant-tortoises-in-galapagos/ (accessed on 30 May 2022)
Charney N.D. Galapagos tortoises in a changing climate Galapagos Giant Tortoises Gibbs J.P. Cayot L.J. Aguilera W.T. Academic Press Cambridge, MA, USA 2021 317 330 10.1016/b978-0-12-817554-5.00017-4
Cayot L.J. The Restoration of Giant Tortoise and Land Iguana Populations in Galapagos Galapagos Res. 2008 65 39 43 Available online: http://hdl.handle.net/1834/36138 (accessed on 30 May 2022)
Jensen E.L. Tapia W. Caccone A. Russello M.A. Genetics of a head-start program to guide conservation of an endangered Galápagos tortoise (Chelonoidis ephippium) Conserv. Genet. 2015 16 823 832 10.1007/s10592-015-0703-7
Russello M.A. Hyseni C. Gibbs J.P. Cruz S. Marquez C. Tapia W. Velensky P. Powell J.R. Caccone A. Lineage identification of Galápagos tortoises in captivity worldwide Anim. Conserv. 2007 10 304 311 10.1111/j.1469-1795.2007.00113.x
Furrer S. Hatt J. Snell H. Marquez C. Honegger R. Rübel A. Comparative study on the growth of juvenile Galapagos giant tortoises (Geochelone nigra) at the Charles Darwin Research Station (Galapagos Islands, Ecuador) and Zoo Zurich (Zurich, Switzerland) Zoo Biol. 2004 23 177 183 10.1002/zoo.10130
Shaw C.E. Breeding the Galapagos Tortoise—Success Story Oryx 1967 9 119 126 10.1017/S0030605300006141
Warwick C. Reptilian ethology in captivity: Observations of some problems and an evaluation of their aetiology Appl. Anim. Behav. Sci. 1990 26 1 13 10.1016/0168-1591(90)90082-O
Freeland L. Ellis C. Michaels C.J. Documenting Aggression, Dominance and the Impacts of Visitor Interaction on Galápagos Tortoises (Chelonoidis nigra) in a Zoo Setting Animals 2020 10 699 10.3390/ani10040699 32316413
Schafer S.F. Krekorian C.O. Agonistic Behavior of the Galapagos Tortoise, Geochelone elephantopus, with Emphasis on Its Relationship to Saddle-Backed Shell Shape Herpetologica 1983 39 448 456
Townsend C.H. The Galapagos tortoises in their relation to the Whaling Industry—A study of old logbooks Zool. Sci. Contrib. N. Y. Zool. Soc. 1925 4 55 135 10.5962/p.203768
Cooper W.E. Dimopoulos I. Pafilis P. Sex, Age, and Population Density Affect Aggressive Behaviors in Island Lizards Promoting Cannibalism Ethology 2015 121 260 269 10.1111/eth.12335
Schuett G.W. Fighting dynamics of male copperheads, Agkistrodon contortrix (Serpentes, Viperidae): Stress-induced inhibition of sexual behavior in losers Zoo Biol. 1996 15 209 221 10.1002/(SICI)1098-2361(1996)15:3<209::AID-ZOO2>3.0.CO;2-F
McMillan D.M. Irschick D.J. Experimental Test of Predation and Competition Pressures on the Green Anole (Anolis carolinensis) in Varying Structural Habitats S. Am. J. Herpetol. 2010 44 272 278 10.1670/08-196.1
Silvestre A.M. How to Assess Stress in Reptiles J. Exot. Pet Med. 2014 23 240 243 10.1053/j.jepm.2014.06.004
Warwick C. Arena P. Lindley S. Jessop M. Steedman C. Assessing reptile welfare using behavioural criteria In Practice 2013 35 123 131 10.1136/inp.f1197
Sherwen S.L. Hemsworth P.H. The Visitor Effect on Zoo Animals: Implications and Opportunities for Zoo Animal Welfare Animals 2019 9 366 10.3390/ani9060366
Ward S.J. Sherwen S. Clark F.E. Advances in Applied Zoo Animal Welfare Science J. Appl. Anim. Welf. Sci. 2018 21 (Suppl. S1) 23 33 10.1080/10888705.2018.1513842 30325227
Hoehfurtner T. Wilkinson A. Nagabaskaran G. Burman O.H.P. Does the provision of environmental enrichment affect the behaviour and welfare of captive snakes? Appl. Anim. Behav. Sci. 2021 239 105324 10.1016/j.applanim.2021.105324
Mellen J. Macphee M.S. Philosophy of environmental enrichment: Past, present, and future Zoo Biol. 2001 20 211 226 10.1002/zoo.1021
Berger A. Activity patterns, chronobiology and the assessment of stress and welfare in zoo and wild animals Int. Zoo Yearb. 2011 45 80 90 10.1111/j.1748-1090.2010.00121.x
Cayot L.J. Ecology of Giant Tortoises (Geochelone elephantopus) in the Galapagos Islands Ph.D. Dissertation Syracuse University Syracuse, NY, USA 1987
Blake S. Tapia P.I. Safi K. Ellis-Soto D. Diet, Behavior, and Activity Patterns Galapagos Giant Tortoises Gibbs J.P. Cayot L.J. Aguilera W.T. Academic Press Cambridge, MA, USA 2021 207 239 10.1016/B978-0-12-817554-5.00025-3
R Core Team R: A Language and Environment for Statistical Computing R Foundation for Statistical Computing Vienna, Austria 2022 Available online: https://www.R-project.org/ (accessed on 29 June 2021)
Wickham H. ggplot2: Elegant Graphics for Data Analysis R Package version 3.3.6 Springer-Verlag New York, NY, USA 2016 978-3-319-24277-4 Available online: https://ggplot2.tidyverse.org (accessed on 30 May 2022)
Kassambara A. ggpubr: ‘ggplot2’ Based Publication Ready Plots R Package Version 0.2.5 R Foundation for Statistical Computing Vienna, Austria 2019 Available online: https://CRAN.R-project.org/package=ggpubr (accessed on 30 May 2022)
Killick R. Haynes K. Eckley I.A. Changepoint: An R Package for Changepoint Analysis R Package Version 2.2.3 R Foundation for Statistical Computing Vienna, Austria 2022 Available online: https://CRAN.R-project.org/package=changepoint (accessed on 30 May 2022)
Neumann C. Kulik L. EloRating: Animal Dominance Hierarchies by Elo Rating R Package Version 0.46.11 R Foundation for Statistical Computing Vienna, Austria 2020 Available online: https://CRAN.R-project.org/package=EloRating (accessed on 30 May 2022)
Bolker B.M. Linear and Generalized Linear Mixed Models Ecological Statistics: Contemporary Theory and Application Fox G.A. Negrete-Yankelevich S. Sosa V.J. Oxford University Press New York, NY, USA 2015 309 333 10.1093/acprof:oso/9780199672547.003.0014
Eagan T. Evaluation of Enrichment for Reptiles in Zoos J. Appl. Anim. Welf. Sci. 2019 22 69 77 10.1080/10888705.2018.1490182 30052062
Riley L.M. Rose P.E. Concepts, applications, uses and evaluation of environmental enrichment: Perceptions of zoo professionals J. Zoo Aquar. Res. 2020 8 18 28 10.19227/JZAR.V8I1.384
Bloomsmith M.A. Brent L.Y. Schapiro S.J. Guidelines for developing and managing an environmental enrichment program for nonhuman primates Lab. Anim. Sci. 1991 41 372 377
Young R.J. Environmental Enrichment for Captive Animals John Wiley & Sons Hoboken, NJ, USA 2013
Wells A. Terio K.A. Ziccardi M.H. Munson L. The Stress Response to Environmental Change in Captive Cheetahs (Acinonyx jubatus) J. Zoo Wildl. Med. 2004 35 8 14 10.1638/02-084
Ferreira V.H.B. Fonseca E.D.P. Das Chagas A.C.C.S. Pinheiro L.G.M. de Sousa M.B.C. da Silva H.P.A. Galvão-Coelho N.L. Ferreira R.G. Personality traits modulate stress responses after enclosure change of captive capuchin monkeys (Sapajus libidinosus) Appl. Anim. Behav. Sci. 2020 232 105111 10.1016/j.applanim.2020.105111
Little K.A. Sommer V. Change of enclosure in langur monkeys: Implications for the evaluation of environmental enrichment Zoo Biol. 2002 21 549 559 10.1002/zoo.10058
Wolfensohn S. Shotton J. Bowley H. Davies S. Thompson S. Justice W.S.M. Assessment of Welfare in Zoo Animals: Towards Optimum Quality of Life Animals 2018 8 110 10.3390/ani8070110 29973560
Dawkins M.S. Time budgets in Red Junglefowl as a baseline for the assessment of welfare in domestic fowl Appl. Anim. Behav. Sci. 1989 24 77 80 10.1016/0168-1591(89)90126-3
Veasey J. Waran N. Young R. On Comparing the Behaviour of Zoo Housed Animals with Wild Conspecifics as a Welfare Indicator, Using the Giraffe (Giraffa camelopardalis) as a Model Anim. Welf. 1996 5 139 153
Rose P. Roper A. Banks S. Giorgio C. Timms M. Vaughan P. Hatch S. Halpin S. Thomas J. O’Brien M. Evaluation of the time-activity budgets of captive ducks (Anatidae) compared to wild counterparts Appl. Anim. Behav. Sci. 2022 251 105626 10.1016/j.applanim.2022.105626
Johnson B. Langton J. Behaviour change in Amur tigers Panthera tigris altaica after an enclosure move J. Zoo Aquar. Res. 2021 9 186 192 10.19227/JZAR.V9I3.520
Ryan J.C. Litchfield C.A. Impact of an enclosure rotation on the activity budgets of two zoo-housed giant pandas (Ailuropoda melanoleuca): An observational case study Eat Sleep Work 2020 1 26 38 10.21913/JDRSSesw.v1i1.1200
Tibbetts E.A. Pardo-Sanchez J. Weise C. The establishment and maintenance of dominance hierarchies Philos. Trans. R. Soc. B Biol. Sci. 2022 377 20200450 10.1098/rstb.2020.0450
Evans L.T. Evans L.T. Quaranta J.V. A study of the social behavior of a captive herd of giant tortoises Zoologica 1951 36 171 181 10.5962/p.203482
Alberts A.C. Dominance hierarchies in male lizards: Implications for zoo management programs Zoo Biol. 1994 13 479 490 10.1002/zoo.1430130510
Gutnick T. Weissenbacher A. Kuba M.J. The underestimated giants: Operant conditioning, visual discrimination and long-term memory in giant tortoises Anim. Cogn. 2020 23 159 167 10.1007/s10071-019-01326-6
Mafli A. Wakamatsu K. Roulin A. Melanin-based coloration predicts aggressiveness and boldness in captive eastern Hermann’s tortoises Anim. Behav. 2011 81 859 863 10.1016/j.anbehav.2011.01.025
Radzio T.A. Cox J.A. Spotila J.R. O’Connor M.P. Aggression, Combat, and Apparent Burrow Competition in Hatchling and Juvenile Gopher Tortoises (Gopherus polyphemus) Chelonian Conserv. Biol. 2016 15 231 237 10.2744/CCB-1181.1
Waters R.M. Bowers B.B. Burghardt G.M. Personality and Individuality in Reptile Behavior Personality in Nonhuman Animals Vonk J. Weiss A. Kuczaj S.A. Springer International Publishing Berlin/Heidelberg, Germany 2017 153 184 10.1007/978-3-319-59300-5
Carlson B.E. Tetzlaff S.J. Long-term behavioral repeatability in wild adult and captive juvenile turtles (Terrapene carolina): Implications for personality development Ethology 2020 126 668 678 10.1111/eth.13024
Jacobs J.A. Coe J.B. Widowski T.M. Pearl D.L. Niel L. Defining and Clarifying the Terms Canine Possessive Aggression and Resource Guarding: A Study of Expert Opinion Front. Vet. Sci. 2018 5 115 10.3389/fvets.2018.00115
Quadros S. Goulart V.D.L.R. Passos L. Vecci M.A. Young R.J. Zoo visitor effect on mammal behaviour: Does noise matter? Appl. Anim. Behav. Sci. 2014 156 78 84 10.1016/j.applanim.2014.04.002
Jackson C.G. Awbrey F.T. Mating Bellows of the Galapagos Tortoise, Geochelone elephantopus Herpetologica 1978 34 134 136
Carter K.C. Keane I.A.T. Clifforde L.M. Rowden L.J. Fieschi-Méric L. Michaels C.J. The Effect of Visitors on Zoo Reptile Behaviour during the COVID-19 Pandemic J. Zoöl. Bot. Gard. 2021 2 664 676 10.3390/jzbg2040048