Length of stay in rehabilitation influences magnitude of the acute stress response in birds of prey
DOI:
https://doi.org/10.53607/wrb.v42.274Keywords:
rehabilitation, raptor, corticosterone, habituation, heterophil, lymphocyteAbstract
Wild animals are occasionally injured or become ill as a result of natural causes
or human activity. As a way to remediate the damage imposed by humans on
wildlife populations, these animals may be taken in for rehabilitation. Federal
laws for rehabilitators set limits for the length of time a bird can remain in
rehabilitation before a final decision on release or euthanasia is made. Little is
known about the consequences of longer stays in captivity within that limited
window with regard to stress physiology of the animals. The authors hypothesised
that length of stay in rehabilitation would influence the ability of raptors
to mount a full stress response upon release from rehabilitation. Blood samples
were taken from each bird upon admission for rehabilitation and immediately
prior to their release, a process by which the animals are exposed to a significant,
acute stressor of capture, handling, and examination. A blood sample
was collected for analysis of heterophil to lymphocyte ratios (H:L), which
are indicative of long-term baseline stress. The authors found that as length of
stay increased, the difference in corticosterone levels reached during an acute
stressor from admission samples to release samples decreased. Baseline stress,
as indicated by H:L, was not significantly affected by length of stay. The results
suggest that birds of prey in rehabilitation habituate to captivity the longer
they stay in captivity and may lose some degree of natural responsiveness to
stressors.
Downloads
References
Black P.A., McRuer D.L. & Horne L. 2011. Hematologic
parameters in raptor species in a rehabilitation setting
before release. Journal of Avian Medicine and Surgery 25(3),
–298, doi: 10.1647/2010-024.1.
Butler S.J., Whittingham M.J., Quinn J.L. & Cresswell W.
Time in captivity, individual differences and foraging
behavior in wild-caught chaffinches. Behaviour 143,
–548.
Campo J.L. & Davila S.G. 2002. Estimation of heritability
for heterophil:lymphocyte ratio in chickens by restricted
maximum likelihood. Effects of age, sex, and crossing.
Poultry Science 81, 1448–1453, doi: 10.1093/ps/81.10.1448.
Carroll G., Turner E., Dann P. & Harcourt R. 2016. Prior
exposure to capture heightens the corticosterone and
behavioural responses of little penguins (Eudyptula minor)
to acute stress. Conservation Physiology 4, doi: 10.1093/
conphys/cov061
Davis A.K. & Maerz J.C. 2011. Addressing stress levels of
captive-reared amphibians with hematological data: implications
for conservation initiatives. Journal of Herpetology
(1), 40–44, doi: 10.1670/10-180.1.
Davis A.K. & Maney D.L. 2018. The use of glucocorticoid
hormones or leucocyte profiles to measure stress in vertebrates:
what’s the difference? Methods in Ecology and
Evolution 9, 1556–1568, doi: 10.1111/2041-210X.13020.
Dickens M.J., Earle K.L. & Romero L.M. 2008. Initial transference
of wild birds to captivity alters stress physiology.
General and Comparative Endocrinology, 160(1), 76–83, doi:
1016/j.ygcen.2008.10.023
Drummond H. & Ancona S. 2015. Observational field studies
reveal wild birds responding to early-life stresses with
resilience, plasticity, and intergenerational effects. The
Auk: Ornithological Advances 132, 563–576, doi: 10.1642/
AUK-14-244.1.
Dufty Jr. A.M. & Belthoff J.M. 1997. Corticosterone and the
stress response in young Western screech-owls: effects of
captivity, gender, and activity period. Physiological Zoology
(2), 143–149, doi: 10.1086/639564.
Giambelluca S., Cammarata M., Dara S., Orefice T., Camina-
Cardenal A. & Vazzana I. 2017. The impact of captivity on
some haematological parameters of griffon vultures (Gyps
fulvus). Veterinaria Italiana 53(3), 243–249, doi: 10.12834/
VetIt.743.3616.2.
Genovese K.J., He H., Swaggerty C.L. & Kogut M.H. 2013. The
avian heterophil. Developmental and Comparative Immunology
(3), 334–340, doi: 10.1016/j.dci.2013.03.021.
Goessling J.M., Kennedy H., Medonca M.T. & Wilson A.E.
A meta-analysis of plasma corticosterone and heterophil:
lymphocyte ratios – is there conservation of physiological
stress responses over time? Functional Ecology 29,
–1196, doi: 10.1111/1365-2435.12442.
Granati G., Cichella F. & Lucidi P. 2021. High-tech training
for birds of prey. Animals 11, 530, doi: 10.3390/
ani11020530
Grasman K.A. 2002. Assessing immunological function in toxicological
studies of avian wildlife. Integrative & Comparative
Biology 42(1), 34–42, doi: 10.3390/ani11020530.
Guerra, R.R., Glenison, F.D., Bernadino, M.G.S., Nailson Jr,
A.N., Monalisa, F.V.F. & Guerra, F.S. 2018. Hematological
standards, hormonal indexes and gonadal morphology
of Roadside Hawks (Rupornis magnirostris). Archives of
Veterinary Science 23, 63–76, doi: 10.5380/avs.v23i1.58580
Heidinger B.J., Nisbet I.C.T. & Ketterson E.D. 2008. Changes
in adrenal capacity contribute to a decline in the stress
response with age in a long-lived seabird. General and
Comparative Endocrinology 156, 564–568, doi: 10.1016/j.
ygcen.2008.02.014.
Herman J.P., McKlveen J.M., Ghosal S., Kopp B., Wulsin A.,
Makinson R., Scheimann J. &Myers B. 2016. Regulation of
the hypothalamic-pituitary-adrenocortical stress response.
Comparative Physiology 6(2), 603–621, doi: 10.1002/cphy.
c150015.
Hing S., Narayan E.J., Thompson R.C.A. & Godfrey S.S. 2016.
The relationship between physiological stress and wildlife
disease: consequences for health and conservation. Wildlife
Research 43(1), 51–60, doi: 10.1071/WR15183.
IBM Corp. 2017. SPSS Statistics for Windows, version 25.0.
Armonk, NY: IBM Corp.
Kluen E., Ronka K. & Thorogood R. 2022. Prior experience
of captivity affects behavioural responses to ‘novel’ environments.
PeerJ 10, e13905, doi: 10.7717/peerj.13905
Laurence A., Houdelier C., Calandreau L., Arnould C.,
Favreau-Peigne A., Leterrier C., Boissy A. & Lumineau
S. 2015. Environmental enrichment reduces behavioural
alterations induced by chronic stress in Japanese quail.
Animal 9(2), 331–338, doi: 10.1017/S1751731114002523.
Love O.P., Shutt L.J., Silfies J.S. & Bird D.M. 2003. Repeated
restraint and sampling results in reduced corticosterone
levels in developing and adult captive American Kestrels
(Falco sparverius). Physiological and Biochemical Zoology:
Ecological and Evolutionary Approaches 76(5), 753–761, doi:
1086/376431.
Mason G.J. 2010. Species differences in response to captivity:
stress, welfare, and the comparative method. Trends
in Ecology and Evolution 25(12), 713–721, doi: 10.1016/j.
tree.2010.08.011.
Mellor D.J. & Beausoleil N.J. 2015. Extending the “Five
Domains” model for animal welfare assessment to incorporate
positive welfare states. Animal Welfare 24, 241–253,
doi: 10.7120/09627286.24.3.241.
Mellor D.J., Beausoleil N.J., Littlewood K.E., McLean A.N.,
McGreevy P.D., Jones B. & Wilkins C. 2020. The 2020 five
domains model: including human-animal interactions
in assessments of animal welfare. Animals 10, 1870, doi:
3390/ani10101870.
Miller, E.A. (ed.) 2012. Minimum standards for wildlife rehabilitation.
St. Cloud, MN: National Wildlife Rehabilitators
Association. 116 p.
Miller E.A. & Schlieps, J. (ed.) 2021. Standards for wildlife
rehabilitation. Bloomington, MN: National Wildlife
Rehabilitators Association. 419 p.
Müller C., Jenni-Elermann S. & Jenni L. 2011. Heterophils/
lymphocytes-ratio and circulating corticosterone do
not indicate the same stress imposed on Eurasian kestrel
nestlings. Functional Ecology 25(3), 566–576, doi:
1111/j.1365-2435.2010.01816.x.
Pakkala J.J., Norris D.R. & Newman A.E.M. 2013. An experimental
test of the capture-restraint protocol for estimating
the acute stress response. Physiological and Biochemical
Zoology 86(2), 279–284, doi: 10.1086/668893.
Potts A. 2016. Captive enrichment for owls (Strigiformes).
Journal of Wildlife Rehabilitation 36(2), 11–29.
Pravosudov V.V. 2005. Corticosterone and memory in birds.
In A. Dawson & P. Sharp (eds.): Functional avian endocrinology.
Pp. 257–269. New Delhi: Narosa Publishing House.
Rich E.L. & Romero L.M. 2005. Exposure to chronic stress
downregulates corticosterone responses to acute stressors.
American Journal of Physiology: Regulatory, Integrative, and
Comparative Physiology 288, R1628–R1634, doi: 10.1152/
ajpregu.00484.2004.
Sapolsky R.M., Romero L.M. & Munck A.U. 2000. How do
glucocorticoids influence stress responses? Integrating permissive,
suppressive, stimulatory, and preparative actions.
Endocrine Reviews 21, 55–89, doi: 10.1210/edrv.21.1.0389.
Scheun J., Ludynia K., Snyman A. & Ganswindt A. 2021.
Non-invasive hormone monitoring as a robust method
for determining adrenocortical activity in injured, emaciated
and oil-contaminated African penguins undergoing
rehabilitation. General and Comparative Endocrinology 303,
, doi: 10.1016/j.ygcen.2020.113703
Schoenle L.A., Zimmer C. & Vitousek M.N. 2018.
Understanding context dependence in glucocorticoid-fitness
relationships: the role of the nature of the challenge,
the intensity, and frequence of stressors, and life
history. Integrative and Comparative Biology 58, 777–789, doi:
1093/icb/icy046.
Straub J., Forbes N., Pees M. & Krautwald-Junghanns
M.-E. 2003. Effect of handling-induced stress on the
results of spectral Doppler electrocardiography in falcons.
Research in Veterinary Science 74, 119–122, doi: 10.1016/
s0034-5288(02)00159-5.
Tome M.E., McNabb F.M.A. & Gwazdauskas F.C. 1985.
Adrenal responses to chronic and acute water stress in
Japanese quail Coturnix japonica. Comparative Biochemistry
and Physiology Part A: Physiology 81(1), 171–179, doi:
1016/0300-9629(85)90284-1.
Wilcoxen T.E., Boughton R.K., Bridge E.S., Rensel M.A. &
Schoech S.J. 2011. Age-related differences in baseline and
stress-induced corticosterone in Florida scrub-jays. General
and Comparative Endocrinology 173, 461–466, doi: 10.1016/j.
ygcen.2011.07.007.
Wilcoxen T.E., Horn D.J., Hubble C.N., Huber S.J., Flamm
J., Knott M., Lundstrom L., Salik F., Wassenhove S.J. &
Wrobel E.R. 2015. Effects of bird feeding activities on the
health of wild birds. Conservation Physiology 3, doi: 10.1093/
conphys/cov058.
Willette M., Rosenhagen N., Buhl G., Innis C. & Boehm J.
Interrupted lives: welfare considerations in wildlife
rehabilitation. Animals 13, 1836, doi: 10.3390/ani13111836
Wingfield J.C. 2003. Control of behavioural strategies for
capricious environments. Animal Behaviour 66, 807–816,
doi: 10.1006/anbe.2003.2298.
Published
How to Cite
Issue
Section
Categories
License
Copyright (c) 2024 Naomi Klingbeil, Jacques T. Nuzzo, D. Jane Seitz, Beth Chan, Travis E. Wilcoxen

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
The copyright for articles in this journal is retained by the author(s), with first publication rights granted to the Wildlife Rehabilitation Bulletin and NWRA. Articles published as open-access in this journal are free to use and share with proper attribution in educational and other non-commercial purposes. To obtain reprint permission for articles that are not open access, please contact the journal editor.