An Improvement in Enclosure Design Can Positively Impact Welfare, Reduce Aggressiveness and Stabilise Hierarchy in Captive Galapagos Giant Tortoises
Open accessAbstract
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.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Increases in exhibit complexity and size have been shown to positively impact behavioral patterns in diverse taxa.
“However, increases in exhibit complexity and size have been shown to positively impact behavioral patterns in diverse taxa.”
From The Benefits of Increased Space and Habitat Complexity for the Welfare of Zoo-Housed King Penguins (Aptenodytes patagonicus) (2023) · cites this paper as [8]
The Introduction (page unavailable) says environmental enrichment and available space contribute to well-being across a wide range of animal taxa. The Discussion (page unavailable) reports improved welfare and reduced aggression after tortoises moved to a more resource-rich enclosure. The paper therefore supports the general benefit of larger, enriched exhibits, but its evidence for improved behavioral patterns is specific to tortoises, not diverse taxa. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
ggplot2: Elegant Graphics for Data Analysis
Ginestet, C. E. (2011) · Journal of the Royal Statistical Society Series A (Statistics in Society) · doi:10.1111/j.1467-985x.2010.00676_9.x · Cited by 14,484 · see citing works
Wickham, H. (2016) · Use R! · doi:10.1007/978-3-319-24277-4_9 · Cited by 12,675 · see citing works
ggpubr: 'ggplot2' Based Publication Ready Plots
Kassambara, A. (2016) · doi:10.32614/cran.package.ggpubr · Cited by 1,752 · see citing works
Philosophy of environmental enrichment: Past, present, and future
Mellen, J. D., & Sevenich, M. (2001) · Zoo Biology · doi:10.1002/zoo.1021 · Cited by 367 · see citing works
Linear and generalized linear mixed models
Bolker, B. M. (2015) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199672547.003.0014 · Cited by 358 · see citing works
The visitor effect on zoo animals: implications and opportunities for zoo animal welfare
Sherwen, S. L., & Hemsworth, P. H. (2019) · Animals · doi:10.3390/ani9060366 · Cited by 267 · see citing works
Time budgets in Red Junglefowl as a baseline for the assessment of welfare in domestic fowl
Dawkins, M. S. (1989) · Applied Animal Behaviour Science · doi:10.1016/0168-1591(89)90126-3 · Cited by 263 · see citing works
The establishment and maintenance of dominance hierarchies
Tibbetts, E., Pardo-Sanchez, J., & Weise, C. (2022) · Philosophical Transactions of the Royal Society of London. Biological Sciences · doi:10.1098/rstb.2020.0450 · Cited by 216 · see citing works
Assessment of welfare in zoo animals: towards optimum quality of life
Wolfensohn, S., Shotton, J., Bowley, H., Davies, S., Thompson, S., & Justice, W. S. M. (2018) · Animals · doi:10.3390/ani8070110 · Cited by 197 · see citing works
(2015) · doi:10.1093/acprof:oso/9780199672547.001.0001 · Cited by 190 · see citing works
PHYLOGEOGRAPHY AND HISTORY OF GIANT GALAPAGOS TORTOISES
Caccone, A., Gentile, G., Gibbs, J. P., Fritts, T. H., Snell, H. L., Betts, J., & Powell, J. R. (2002) · Evolution · doi:10.1111/j.0014-3820.2002.tb00131.x · Cited by 165 · see citing works
Origin and evolutionary relationships of giant Galápagos tortoises
Caccone, A., Gibbs, J. P., Ketmaier, V., Suatoni, E., & Powell, J. R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.23.13223 · Cited by 164 · see citing works
Assessing reptile welfare using behavioural criteria
Warwick, C., Arena, P. C., Lindley, S., Jessop, M., & Steedman, C. (2013) · In Practice · doi:10.1136/inp.f1197 · Cited by 159 · see citing works
Guidelines for developing and managing an environmental enrichment program for nonhuman primates.
Bloomsmith, M. A., Brent, L., & Schapiro, S. J. (1991) · PubMed · Cited by 146 · see citing works
Zoo visitor effect on mammal behaviour: does noise matter?
Quadros, S., Goulart, V. D. L., Passos, L., Vecci, M. A. M., & Young, R. J. (2014) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2014.04.002 · Cited by 135 · see citing works
Alien species pathways to the Galapagos Islands, Ecuador
Toral-Granda, M. V., Causton, C., Jäger, H., Trueman, M., Izurieta, J., Araujo, E., Cruz, M., Zander, K., Izurieta, A., & Garnett, S. (2017) · PLoS ONE · doi:10.1371/journal.pone.0184379 · Cited by 134 · see citing works
Veasey, J. S., Waran, N. K., & Young, R. J. (1996) · Animal Welfare · doi:10.1017/s0962728600018571 · Cited by 103 · see citing works
Microsatellite analysis of genetic divergence among populations of giant Galápagos tortoises
Ciofi, C., Milinkovitch, M. C., Gibbs, J. P., Caccone, A., & Powell, J. R. (2002) · Molecular Ecology · doi:10.1046/j.1365-294x.2002.01617.x · Cited by 98 · see citing works
Melanin-based coloration predicts aggressiveness and boldness in captive eastern Hermann’s tortoises
Mafli, A., Wakamatsu, K., & Roulin, A. (2011) · Animal Behaviour · doi:10.1016/j.anbehav.2011.01.025 · Cited by 98 · see citing works
Environmental Enrichment for Captive Animals
Lindley, A. (2004) · The Veterinary Journal · doi:10.1016/j.tvjl.2004.03.006 · Cited by 90 · see citing works
Personality in Nonhuman Animals
(2017) · Springer eBooks · doi:10.1007/978-3-319-59300-5 · Cited by 90 · see citing works
Reptilian ethology in captivity: Observations of some problems and an evaluation of their aetiology
Warwick, C. (1990) · Applied Animal Behaviour Science · doi:10.1016/0168-1591(90)90082-o · Cited by 87 · see citing works
How to Assess Stress in Reptiles
Silvestre, A. M. (2014) · Journal of Exotic Pet Medicine · doi:10.1053/j.jepm.2014.06.004 · Cited by 82 · see citing works
Advances in Applied Zoo Animal Welfare Science
Ward, S. J., Sherwen, S., & Clark, F. E. (2018) · Journal of Applied Animal Welfare Science · doi:10.1080/10888705.2018.1513842 · Cited by 78 · see citing works
Sex, Age, and Population Density Affect Aggressive Behaviors in Island Lizards Promoting Cannibalism
Cooper, W. E., Dimopoulos, I., & Pafilis, P. (2014) · Ethology · doi:10.1111/eth.12335 · Cited by 72 · see citing works
EloRating: Animal Dominance Hierarchies by Elo Rating
Neumann, C., & Kulik, L. (2014) · doi:10.32614/cran.package.elorating · Cited by 69 · see citing works
THE STRESS RESPONSE TO ENVIRONMENTAL CHANGE IN CAPTIVE CHEETAHS (ACINONYX JUBATUS)
Wells, A., Terio, K. A., Ziccardi, M. H., & Munson, L. (2004) · Journal of Zoo and Wildlife Medicine · doi:10.1638/02-084 · Cited by 60 · see citing works
The Galapagos tortoises in their relation to the whaling industry--A study of old logbooks
Townsend, C. H. (1925) · Zoologica scientific contributions of the New York Zoological Society · doi:10.5962/p.203768 · Cited by 59 · see citing works
Change of enclosure in langur monkeys: implications for the evaluation of environmental enrichment
Little, K. A., & Sommer, V. (2002) · Zoo Biology · doi:10.1002/zoo.10058 · Cited by 58 · see citing works
Does the provision of environmental enrichment affect the behaviour and welfare of captive snakes?
Hoehfurtner, T., Wilkinson, A., Nagabaskaran, G., & Burman, O. H. P. (2021) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2021.105324 · Cited by 53 · see citing works
Activity patterns, chronobiology and the assessment of stress and welfare in zoo and wild animals
Berger, A. (2010) · International Zoo Yearbook · doi:10.1111/j.1748-1090.2010.00121.x · Cited by 44 · see citing works
The restoration of giant tortoise and land iguana populations in Galapagos
Cayot, L. J. (2008) · AquaDocs (United Nations Educational, Scientific and Cultural Organization) · Cited by 43 · see citing works
Carlson, B. E., & Tetzlaff, S. J. (2020) · Ethology · doi:10.1111/eth.13024 · Cited by 39 · see citing works
Lineage identification of Galápagos tortoises in captivity worldwide
Russello, M. A., Hyseni, C., Gibbs, J. P., Cruz, S., Márquez, C., Tapia, W., Velenský, P., Powell, J. R., & Caccone, A. (2007) · Animal Conservation · doi:10.1111/j.1469-1795.2007.00113.x · Cited by 32 · see citing works
Gutnick, T., Weissenbacher, A., & Kuba, M. J. (2019) · Animal Cognition · doi:10.1007/s10071-019-01326-6 · Cited by 31 · see citing works
McMillan, D. M., & Irschick, D. J. (2010) · Journal of Herpetology · doi:10.1670/08-196.1 · Cited by 30 · see citing works
Dominance hierarchies in male lizards: Implications for zoo management programs
Alberts, A. C. (1994) · Zoo Biology · doi:10.1002/zoo.1430130510 · Cited by 28 · see citing works
Ancient mitogenomics elucidates diversity of extinct West Indian tortoises
Kehlmaier, C., Albury, N. A., Steadman, D. W., Graciá, E., Franz, R., & Fritz, U. (2021) · Scientific Reports · doi:10.1038/s41598-021-82299-w · Cited by 26 · see citing works
Evaluation of the time-activity budgets of captive ducks (Anatidae) compared to wild counterparts
Rose, P., Roper, A., Banks, S., Giorgio, C., Timms, M., Vaughan, P., Hatch, S., Halpin, S. M., Thomas, J., & O'Brien, M. (2022) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2022.105626 · Cited by 23 · see citing works
Evaluation of Enrichment for Reptiles in Zoos
Eagan, T. (2018) · Journal of Applied Animal Welfare Science · doi:10.1080/10888705.2018.1490182 · Cited by 23 · see citing works
Riley, L. M., & Rose, P. E. (2020) · The Journal of zoo and aquarium research · doi:10.19227/jzar.v8i1.384 · Cited by 21 · see citing works
The Effect of Visitors on Zoo Reptile Behaviour during the COVID-19 Pandemic
Carter, K. C., Keane, I. A. T., Clifforde, L. M., Rowden, L. J., Fieschi‐Méric, L., & Michaels, C. J. (2021) · Journal of Zoological and Botanical Gardens · doi:10.3390/jzbg2040048 · Cited by 21 · see citing works
Self-citationSchafer, S. F., & Krekorian, C. O. (1983) · Cited by 20 · see citing works
Jensen, E. L., Tapia, W., Caccone, A., & Russello, M. A. (2015) · Conservation Genetics · doi:10.1007/s10592-015-0703-7 · Cited by 19 · see citing works
Furrer, S. C., Hatt, J., Snell, H. L., Márquez, C., Honegger, R. E., & Rübel, A. (2004) · Zoo Biology · doi:10.1002/zoo.10130 · Cited by 19 · see citing works
Freeland, L. V., Ellis, C., & Michaels, C. J. (2020) · Animals · doi:10.3390/ani10040699 · Cited by 18 · see citing works
Self-citationThe Galapagos: Island home of giant tortoises
Frazier, J. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-817554-5.00004-6 · Cited by 17 · see citing works
A study of the social behavior of a captive herd of giant tortoises
Evans, L. T., & Quaranta, J. V. (1951) · Zoologica scientific contributions of the New York Zoological Society · doi:10.5962/p.203482 · Cited by 12 · see citing works
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., Coelho, N. L. G., & Ferreira, R. G. (2020) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2020.105111 · Cited by 11 · see citing works
Jacobs, J., Coe, J. B., Widowski, T. M., Pearl, D. L., & Niel, L. (2018) · Frontiers in Veterinary Science · doi:10.3389/fvets.2018.00115 · Cited by 11 · see citing works
Radzio, T. A., Cox, J. A., Spotila, J. R., & O’Connor, M. P. (2016) · Chelonian Conservation and Biology · doi:10.2744/ccb-1181.1 · Cited by 11 · see citing works
Diet, behavior, and activity patterns
Blake, S., Tapia, P. I., Safi, K., & Ellis‐Soto, D. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-817554-5.00025-3 · Cited by 10 · see citing works
Breeding the Galapagos Tortoise—Success Story
Shaw, C. E. (1967) · Oryx · doi:10.1017/s0030605300006141 · Cited by 10 · see citing works
Caccone, A. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-817554-5.00019-8 · Cited by 7 · see citing works
The history of Galapagos tortoise conservation
Cayot, L. J. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-817554-5.00008-3 · Cited by 5 · see citing works
Ryan, J. C., & Litchfield, C. A. (2016) · Eat Sleep Work · doi:10.21913/jdrssesw.v1i1.1200 · Cited by 4 · see citing works
Galapagos tortoises in a changing climate
Charney, N. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-817554-5.00017-4 · Cited by 4 · see citing works
Behaviour change in Amur tigers Panthera tigris altaica after an enclosure move
Johnson, B., & Langton, J. (2021) · The Journal of zoo and aquarium research · doi:10.19227/jzar.v9i3.520
Ferguson, G. W., Jones, J. R., Gehrmann, W. H., Hammack, S. H., Talent, L. G., Hudson, R. D., Dierenfeld, E. S., Fitzpatrick, M. P., Frye, F. L., Holick, M. F., et al. (1996) · Zoo Biology · doi:10.1002/(sici)1098-2361(1996)15:3
Flagged first, then by citations
2 of the 61 references couldn’t be matched to a known paper.
Research works printed but not linked: 2
- Cayot, L.J. Ecology of Giant Tortoises (Geochelone elephantopus) in the Galapagos Islands. Ph.D. Dissertation, Syracuse University, Syracuse, NY, USA, 1987.
- Jackson, C.G.; Awbrey, F.T. Mating Bellows of the Galapagos Tortoise, Geochelone elephantopus. Herpetologica 1978, 34, 134-136.
Cited by
Sorted by citations
de Azevedo, C. S., Cipreste, C. F., Pizzutto, C. S., & Young, R. J. (2023) · Animals · doi:10.3390/ani13081277 · Cited by 82 · see citing works
Fuller, G., Jones, M., Gartland, K. N., Zalewski, S., Heintz, M. R., & Allard, S. (2023) · Animals · doi:10.3390/ani13142312 · Cited by 8 · see citing works
Effects of Enclosure Complexity and Design on Behaviour and Physiology in Captive Animals
Smith, A. C., Rose, P. E., & Mettke‐Hofmann, C. (2024) · Animals · doi:10.3390/ani14142028 · Cited by 7 · see citing works
Hanson, S. L., Whittaker, A. L., Cooper‐Rogers, B., Burghardt, G. M., & Fernandez, E. J. (2025) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2025.106831 · Cited by 6 · see citing works
Influence of enclosure design on the behaviour and welfare of Pogona vitticeps
Denommé, M., Bakker, N. L., & Tattersall, G. J. (2025) · PLoS ONE · doi:10.1371/journal.pone.0322682 · Cited by 4 · see citing works
Stalter, L., Dorleus, T., Milone, N., Sincage, J., Skurski, M. L., & Leeds, A. (2024) · PLoS ONE · doi:10.1371/journal.pone.0314501 · Cited by 2 · see citing works
Social dynamics and behavior of zoo-housed red-footed tortoises at different housing densities
O’Brien, S. L., Diaz, A., & Cronin, K. A. (2025) · Behavioural Processes · doi:10.1016/j.beproc.2025.105242 · Cited by 1 · see citing works
Geijtenbeek, J. W., van den Berg, L. M., & Roth, T. S. (2026) · Animal Welfare · doi:10.1017/awf.2026.10086 · Cited by 1 · see citing works
Tortoise Behaviour and Learning
Williams, J. (2024) · CABI eBooks · doi:10.1079/9781800623736.0008
Social Interactions in Tortoises
Williams, J. (2024) · CABI eBooks · doi:10.1079/9781800623736.0010
Animal welfare implications of management strategies for invasive freshwater turtles
Moser, L. A., Smith, B. R., Matthys, S., Kenup, C. F., Spongano, I., Cavatoni, S., Zotto, M. D., Ferrari, N., Ferri, V., Hoby, S., et al. (2026) · NeoBiota · doi:10.3897/neobiota.109.204683
- Authors
- Fieschi-Méric, L., Ellis, C., Servini, F., Tapley, B., & Michaels, C. J.
- Affiliations
- Zoological Society of London, London NW1 4RY, UK
- Zoological Society of London (GB)
- Venue
- Journal of Zoological and Botanical Gardens
- Publisher
- MDPI AG
- Published
- 2022-09-28
- Volume
- 3
- Issue
- 4
- Pages
- 499-512
- ISSN
- 2673-5636 (ISSN-L)
- OpenAlex
- W4297476904
- Cited by
- 11
- References
- 61
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 4 · 2023: 2
- FWCI
- 2.49
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Journal of Zoological and Botanical Gardens (publishedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Open Repository and Bibliography (University of Liège) (submittedVersion, other-oa)
- Funders
- ReNewZoo PhD program
- Topics
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Physical Sciences › Environmental Science › Global and Planetary Change › Amphibian and Reptile Biology
- Keywords
- Galápagos tortoise, Chelonoidis, reptile welfare, enclosure design, captive reptiles, time budget, social hierarchy, agonistic behavior, aggression, environmental sounds, zoo animal welfare
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
