Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-17T19:29:43.680Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of developmental history on the behavioural responses of European starlings (Sturnus vulgaris) to laboratory husbandry

Published online by Cambridge University Press:  01 January 2023

K Jayne ,
G Feenders  and
M Bateson
K Jayne*
Affiliation:
Centre for Research in Animal Behaviour, Washington Singer Laboratories, University of Exeter EX4 4QG, UK
G Feenders
Affiliation:
Centre for Behaviour and Evolution, Institute of Neuroscience, Newcastle University, Newcastle-upon-Tyne, UK
M Bateson
Affiliation:
Centre for Behaviour and Evolution, Institute of Neuroscience, Newcastle University, Newcastle-upon-Tyne, UK
*
* Contact for correspondence and requests for reprints: kjayne@alumni.exeter.ac.uk
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

This study examined the impact of rearing environment on the behavioural responses of wild European starlings (Sturnus vulgaris) to standard laboratory husbandry procedures. We compared birds that had been caught from the wild as independent juveniles with birds taken from the nest and hand-reared in the laboratory from approximately ten days post-hatch. Although hand-rearing can increase habituation to humans and hence reduce fearfulness in laboratory birds, in other species maternal deprivation is also associated with increased stress-sensitivity in later life. Thus, the welfare benefits of hand-rearing are unclear. We investigated the interaction between rearing environment (12 hand-reared versus 12 wild-caught birds) and current laboratory housing conditions (enriched versus non-enriched cages and top-level cages versus bottom-level cages) on measures of behaviour before, during and after husbandry. Both wild-caught and hand-reared birds reacted to focal husbandry by moving to the periphery of their cages, indicative of high escape motivation during a stressful procedure. Wild-caught birds were overall less active than hand-reared birds. We found no difference in the response of the wild-caught and hand-reared birds to focal husbandry, but hand-reared birds were faster to resume normal behaviour following husbandry than wild-caught birds when housed in the top cages. We interpret our results as showing evidence for chronic depressive apathy (lower overall activity) coupled with greater fear (longer latencies to resume normal behaviour following husbandry) in the wild-caught birds in some environments. Our data support the conclusion that hand-rearing is associated with some welfare benefits for birds involved in laboratory research.

Keywords

animal welfarecage positionenrichmentEuropean starlinglaboratory husbandryrearing environment
Type
Research Article
Information
Animal Welfare , Volume 22 , Issue 1: Including selected abstracts from the WSPA/Defra Whale Welfare and Ethics Workshop, March 2011 , February 2013 , pp. 67 - 78
Copyright
© 2013 Universities Federation for Animal Welfare

References

Asher, L 2007 The welfare of captive European starlings (Sturnus vulgaris). PhD Thesis, Newcastle University, UKGoogle Scholar
Asher, L, Davies, GTO, Bertenshaw, CE, Cox, MAA and Bateson, M 2009a The effects of cage volume and cage shape on the condition and behaviour of captive European starlings (Sturnus vulgaris). Applied Animal Behaviour Science 116: 286-294. http://dx.doi.org/10.1016/j.applanim.2008.10.008CrossRefGoogle Scholar
Asher, L, Kirkden, RD and Bateson, M 2009b An empirical investigation of two assumptions of motivation testing in captive starlings (Sturnus vulgaris): do animals have an energy budget to ‘spend’? and does cost reduce demand? Applied Animal Behaviour Science 118: 152–160. http://dx.doi.org/10.1016/j.applanim.2009.02.029CrossRefGoogle Scholar
Balcombe, J, Barnard, N and Sandusky, C 2004 Laboratory routines cause animal stress. American Association for Laboratory Animal Science 43: 42–51Google ScholarPubMed
Bateson, M and Feenders, G 2010 The use of passerine bird species in laboratory research: implications of basic biology for husbandry and welfare. ILAR Journal 51: 394–408CrossRefGoogle ScholarPubMed
Bateson, M and Matheson, SM 2007 Performance on a categorisation task suggests that removal of environmental enrichment induces ‘pessimism’ in captive European starlings (Sturnus vulgaris). Animal Welfare 16: 33–36Google Scholar
Bowlby, J 1951 Maternal Care and Mental Health. World Health Organisation: Geneva, SwitzerlandGoogle ScholarPubMed
Brilot, BO, Asher, L and Bateson, M 2009a Water bathing alters the speed-accuracy trade-off of escape flights in European starlings. Animal Behaviour 78: 801–807. http://dx.doi.org/10.1016/j.an behav.2009.07.022CrossRefGoogle Scholar
Brilot, BO, Asher, L and Bateson, M 2010 Stereotyping starlings are more ‘pessimistic’. Animal Cognition 13: 721–731. http://dx.doi.org/10.1007/s10071-010-0323-zCrossRefGoogle Scholar
Brilot, BO, Asher, L, Feenders, G and Bateson, M 2009b Quantification of abnormal repetitive behaviour in captive European starlings (Sturnus vulgaris). Behavioural Processes 82: 256–264. http://dx.doi.org/10.1016/j.beproc.2009.07.003CrossRefGoogle Scholar
Brilot, BO and Bateson, M 2012 Water bathing alters threat perception in starlings. Biology Letters 8: 379–381. http://dx.doi.org/10.1098/rsbl.2011.1200CrossRefGoogle ScholarPubMed
Burn, CC, Peters, A and Mason, GJ 2006 Acute effects of cage cleaning at different frequencies on laboratory rat behaviour and welfare. Animal Welfare 15: 161–171Google Scholar
Cabanac, M and Aizawa, S 2000 Fever and tachycardia in a bird (Gallus domesticus) after simple handling. Physiology & Behaviour 69: 541–545. http://dx.doi.org/10.1016/S0031-9384(00)00227-4CrossRefGoogle Scholar
Carere, C and van Oers, K 2004 Shy and bold great tits (Parus major): body temperature and breath rate in response to handling stress. Physiology & Behaviour 82: 905–912CrossRefGoogle ScholarPubMed
Chase, WK, Marinus, LM and Novak, MA 2000 A behavioural comparison of male rhesus macaques (Macaca mulatta) in four different housing conditions. American Journal of Primatology 51: 51Google Scholar
Collins, SA, Archer, JA and Barnard, CJ 2008 Welfare and mate choice in zebra finches: effect of handling regime and presence of cover. Animal Welfare 17: 11–17Google Scholar
Council of the European Union 2010 Directive 2010/63/EU of the European Parliament and of the Council on the Protection of Animals used for Scientific Purposes. Official Journal of the European Union L276: 33–79Google Scholar
Deussing, JM 2006 Animal models of depression. Drug Discovery Today: Disease Models 3: 375–383. http://dx.doi.org/10.1016/j.dd mod.2006.11.003Google Scholar
Feenders, G and Bateson, M 2011 Hand-rearing reduces fear of humans in European starlings, Sturnus vulgaris. PLoS ONE 6: e17466. http://dx.doi.org/10.1371/journal.pone.0017466CrossRefGoogle ScholarPubMed
Feenders, G and Bateson, M 2012 Development of stereotypic behaviour in caged European starlings, Sturnus vulgaris. Developmental Psychobiology, in press. http://dx.doi.org/10.1002/dev.20623CrossRefGoogle Scholar
Feenders, G, Klaus, K and Bateson, M 2011 Fear and exploration in European starlings (Sturnus vulgaris): a comparison of hand-reared and wild-caught birds. PLoS One 6: e19074. http://dx.doi.org/10.1371/journal.pone.0019074CrossRefGoogle ScholarPubMed
Ficken, MS 1977 Avian play. The Auk 94: 573–582CrossRefGoogle Scholar
Fureix, C, Jego, P, Henry, S, Lansade, L and Hausberger, M 2012 Towards an ethological animal model of depression? A study on horses. PLoS ONE 7(6): e39280. http://dx.doi.org/10.1371/journal.pone.0039280CrossRefGoogle Scholar
Gill, EL 1994 Environmental enrichment for captive starlings. Journal of the Institute of Animal Technology 45: 89–93Google Scholar
Gill, EL, Chivers, RE, Ellis, SC, Field, SA, Haddon, TE, Oliver, DP, Richardson, SA and West, PJ 1995 Turf as a means of enriching the environment of captive starlings (Sturnus vulgaris). Animal Technology 46: 97–102Google Scholar
Greenwood, VJ, Smith, EL, Church, SC and Partridge, JC 2003 Behavioural investigation of polarisation sensitivity in the Japanese quail (Coturnix coturnix japonica) and the European starling (Sturnus vulgaris). Journal of Experimental Biology 206: 3201–3210. http://dx.doi.org/10.1242/jeb.00537CrossRefGoogle Scholar
Gross, WB and Siegel, PB 1997 Adaptation of chickens to their handlers and experimental results. In: Appleby, MC and Hughes, BO (eds) Animal Welfare. CABI: Oxford, UKGoogle Scholar
Hansen, SW and Jeppesen, LL 2006 Temperament, stereotypies and anticipatory behaviour as measures of welfare in mink. Applied Animal Behaviour Science 99: 72–182. http://dx.doi.org/10.1016/j.applanim.2005.10.005CrossRefGoogle Scholar
Harlow, HF 1964 Early social deprivation and later behavior in the monkey. In: Abrams, A, Gurner, HH and Tomal, JEP (eds) Unfinished Tasks in the Behavioral Sciences. Williams & Wilkins: Baltimore, USAGoogle Scholar
Henry, L, Le Cars, K, Mathelier, M, Bruderer, C and Hausberger, M 2008 The use of a mirror as a ‘social substitute’ in laboratory birds. Comptes Rendus Biologies 331: 526–531. http://dx.doi.org/10.1016/j.crvi.2008.04.005CrossRefGoogle ScholarPubMed
Honess, PE, Johnson, PJ and Wolfensohn, SE 2004 A study of behavioural responses of nonhuman primates to air transport and re-housing. Laboratory Animals 38: 119–132. http://dx.doi.org/10.1258/002367704322968795CrossRefGoogle Scholar
Jones, MA, Mason, GJ and Pillay, N 2011 Correlates of birth origin effects on the development of stereotypic behaviour in striped mice, Rhabdomys. Animal Behaviour 82: 149–159. http://dx.doi.org/10.1016/j.anbehav.2011.04.010CrossRefGoogle Scholar
Jones, RB 1987 Assessment of fear in adult laying hens: correlational analysis of methods and measures. British Poultry Science 28: 319–326. http://dx.doi.org/10.1080/00071668708416964CrossRefGoogle ScholarPubMed
Jones, RB, Mills, AD, Faure, JM and Williams, JB 1994 Restraint, fear, and distress in Japanese quail genetically selected for long or short tonic immobility reactions. Physiology & Behaviour 56: 529–534. http://dx.doi.org/10.1016/0031-9384(94)90297-6CrossRefGoogle ScholarPubMed
Kettlewell, PJ and Mitchell, MA 1994 Catching, handling and loading of poultry for road transportation. World's Poultry Science Journal 50: 54–56CrossRefGoogle Scholar
King, DL 1966 A review and interpretation of some aspects of the infant-mother relationship in mammals and birds. Psychological Bulletin 65: 143–155. http://dx.doi.org/10.1037/h0023010CrossRefGoogle ScholarPubMed
Latham, NR and Mason, GJ 2008 Maternal deprivation and the development of stereotypic behaviour. Applied Animal Behaviour Science 110: 84–108. http://dx.doi.org/10.1016/j.applanim.2007.03.026CrossRefGoogle Scholar
Line, SW, Morgan, KN, Markowitz, H and Strong, S 1989 Heart rate and activity of rhesus monkeys in response to routine events. Laboratory Primate Newsletter 28: 1–4Google Scholar
Maddocks, SA, Goldsmith, AR and Cuthill, IC 2002 Behavioural and physiological effects of absence of ultraviolet wavelengths on European starlings Sturnus vulgaris. Journal of Avian Biology 33: 103–106. http://dx.doi.org/10.1034/j.1600048X.2002.330117.xCrossRefGoogle Scholar
Martin, P and Bateson, P 2006 Measuring Behaviour: An Introductory Guide, 2nd Edition. Cambridge University Press: Cambridge, UKGoogle Scholar
Mason, GJ 2006 Are wild-born animals ‘protected’ from stereotypy behaviour when placed in captivity? In: Mason, GJ and Rushen, J (eds) Stereotypic Behaviour: Fundamentals and Applications to Welfare. CAB International: Wallingford, UK. http://dx.doi.org/10.1079/9780851990040.0000CrossRefGoogle Scholar
Mason, GJ and Rushen, J 2006 Stereotypic Behaviour: Fundamentals and Applications to Welfare. CAB International: Wallingford, UK. http://dx.doi.org/10.1079/9780851990040.0000CrossRefGoogle Scholar
Matheson, S, Asher, L and Bateson, M 2008 Larger, enriched cages are associated with ‘optimistic’ response biases in captive European starlings (Sturnus vulgaris). Applied Animal Behaviour Science 109: 374–383. http://dx.doi.org/10.1016/j.applanim.2007.03.007CrossRefGoogle Scholar
Matthews, K, Christmas, D, Swan, J and Sorrell, E 2005 Animal models of depression and antidepressant activity. Neuroscience and Biobehavioral Reviews 29: 503–513. http://dx.doi.org/10.1016/j.neubiorev.2005.03.005CrossRefGoogle Scholar
McArthur, R and Borsini, F 2006 Animal models of depression in drug discovery: a historical perspective. Pharmacology Biochemistry and Behavior 84: 436–452. http://dx.doi.org/10.10 16/j.pbb.2006.06.005CrossRefGoogle ScholarPubMed
Meehan, CL, Garner, JP and Mench, JA 2004 Environmental enrichment and development of cage stereotypy in orange-winged Amazon parrots (Amazona amazonica). Developmental Psychobiology 44: 209–218. http://dx.doi.org/10.1002/dev.20007CrossRefGoogle Scholar
Mendl, M, Burman, OHP and Paul, ES 2010 An integrative and functional framework for the study of animal emotion and mood. Proceedings of the Royal Society B277: 2895–2904. http://dx.doi.org/10.1098/rspb.2010.0303Google Scholar
Miller, ML, Gallup, AC, Vogel, AR and Clark, AB 2010 Handling stress inhibits, but then potentiates yawning in budgerigars (Melopsittacus undulatus). Animal Behaviour 80: 615–619. http://dx.doi.org/10.1016/j.anbehav.2010.05.018CrossRefGoogle Scholar
Morgan, KN and Tromborg, CT 2007 Sources of stress in captivity. Applied Animal Behaviour Science 102: 262–302. http://dx.doi.org/10.1016/j.applanim.2006.05.032CrossRefGoogle Scholar
Nogueira, SSC, Bernadi, LG and Nogueira, SLG 2004 A note on comparative enclosure facility usage by wild and captive-born capybaras (Hydrochoerus hydrochaeris). Applied Animal Behaviour Science 89: 139–143. http://dx.doi.org/10.1016/j.applanim.2004.04.007CrossRefGoogle Scholar
Plotsky, PM and Meaney, MJ 1993 Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Molecular Brain Research 18: 195–200. http://dx.doi.org/10.1.016/0169-328X(93)90189-VCrossRefGoogle ScholarPubMed
Reinhardt, V and Reinhardt, A 2000 Blood collection procedure of laboratory primates: a neglected variable in biomedical research. Journal of Applied Animal Welfare 3: 321–333. http://dx.doi.org/10.1207/S15327604JAWS0304_4CrossRefGoogle Scholar
Schmid, R, Doherr, MG and Steiger, A 2006 The influence of the breeding method on the behaviour of adult African grey parrots (Psittacus erithacus). Applied Animal Behaviour Science 98: 293–307. http://dx.doi.org/10.1016/j.applanim.2005.09.002CrossRefGoogle Scholar
Schnell, CR and Gerber, R 1997 Training and remote monitoring of cardiovascular parameters in non-human primates. Primate Report 49: 61–70Google Scholar
Spruijt, BM, van den Bos, R and Pijlman, FTA 2001 A concept of welfare based on reward evaluating mechanisms in the brain: anticipatory behaviour as an indicator for the state of reward systems. Applied Animal Behaviour Science 72: 145–171. http://dx.doi.org/10.1016/S0168-1591(00)00204-5CrossRefGoogle ScholarPubMed
van Zeeland, YRA, Spruit, BM, Rodenburg, TB, Riedstra, B, van Hierden, YM, Buitenhuis, B, Korte, SM and Lumeij, JT 2009 Feather damaging behaviour in parrots: a review with consideration of comparative aspects. Applied Animal Behaviour 121: 75–95. http://dx.doi.org/10.1016/j.applanim.2009.09.006CrossRefGoogle Scholar
Vestergaard, KS, Skadhauge, E and Lawson, LG 1997 The stress of not being able to perform dustbathing in laying hens. Physiology & Behavior 62: 413–419. http://dx.doi.org/10.1016/S0031-9384(97)00041-3CrossRefGoogle Scholar
Zimmerman, PH, Buijs, SAF, Bolhuis, JE and Keeling, LJ 2011 Behaviour of domestic fowl in anticipation of positive and negative stimuli. Animal Behaviour 81: 569–577. http://dx.doi.org/10.1016/j.anbehav.2010.11.028CrossRefGoogle Scholar