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Towards
Positive
Animal
Welfare
16
..
Vol.
2015
II WAZA 16 (2015)
Contents
Markus Gusset & Gerald Dick
Editorial.................................................................. 1
Georgia J. Mason
Using Species Differences in Health
and Well-being to Identify Intrinsic Risk
and Protective Factors........................................... 2
David Shepherdson & Nadja Wielebnowski
The Power of Multi-institutional and
Longitudinal Studies for Zoo
Animal Welfare Research.......................................6
Kathy Carlstead & Janine Brown
Using Science to Understand Zoo Elephant
Welfare: Evaluation of Ovarian Cyclicity and
Keeper–Elephant Relationships........................... 10
Lance J. Miller, Randall S. Wells, Rita Stacey,
F. William Zeigler, Jessica C. Whitham
& Michael Adkesson
Animal Welfare Management of Bottlenose
Dolphins at the Chicago Zoological
Society’s Brookfield Zoo...................................... 14
David Orban, Hani Freeman, Catharine Wheaton,
Jill Mellen, Joseph Soltis & Katherine Leighty
Use of Science to Enhance Animal Welfare
at Disney’s Animal Kingdom................................ 18
Zjef Pereboom & Jeroen Stevens
Applied Animal Welfare Research in Zoos:
The More the Better............................................. 22
Ron Kagan, Stephanie Allard & Scott Carter
Exotic Animal Welfare – A Path Forward..............26
Imprint
Christopher W. Kuhar, Andi M. Kornak
Editors: Markus Gusset & Gerald Dick & Kristen E. Lukas
WAZA Executive Office Beyond Animal Welfare Science........................... 30
IUCN Conservation Centre
Rue Mauverney 28 Vicky Melfi & Geoff Hosey
CH-1196 Gland Evidence-based Zoo Animal Welfare:
Switzerland From Principles to Practice.................................. 34
Phone: +41 22 999 07 90
Fax: +41 22 999 07 91 Jason Watters, Kate Sulzner,
Debbie Marrin, Sandy Huang, Corinne MacDonald,
Layout and typesetting: michal@sky.cz Susan Ostapak, Andrew Poole & Heather Hayle
Drawings: Kimio Honda (WAZA thanks for his generous donation!) Assessing Quality of Life in
Print: Agentura NP, Staré Město, Czech Republic Geriatric Zoo Animals........................................... 37
Edition: 600 copies | © WAZA 2015 Terry L. Maple
Four Decades of Psychological Research
This edition of WAZA Magazine is also available on on Zoo Animal Welfare......................................... 41
www.waza.org.
Printed on FSC paper.
ISSN: 2074-4528
WAZA 16 (2015) 1
Markus Gusset1 & Gerald Dick2
Editorial
Whilst conservation of wildlife is the
core purpose of modern zoos and
aquariums, animal welfare is our core
activity. This year, WAZA is going
to release strategic guidance docu-
ments for both animal conservation
and welfare: the third iteration of the
World Zoo and Aquarium Conserva‑
tion Strategy and the first‑ever World
Zoo and Aquarium Animal Welfare
Strategy. This gives testimony to the
equal value and emphasis that WAZA
places on wildlife conservation and
animal welfare.
Animal welfare is understood to vary
on a continuum from very poor to
The Five Domains model for understanding animal welfare, divided into physical/functional
very good. The promotion of positive and mental components, provides examples of how internal and external conditions give rise
animal welfare states requires differ- to negative (aversive) and positive (pleasant) subjective experiences, the integrated effects
ent approaches to minimising nega- of which give rise to an animal’s welfare status (modified from Mellor & Beausoleil 2015;
Anim. Welf. 24: 241–253).
tive welfare states. Modern zoos and
aquariums should work to minimise
the occurrence of negative states As welfare is a state within an Reference to the first four domains
in their animals and, concurrently, animal and is understood in terms enables systematic consideration
should make efforts to promote posi- of what the animal experiences of a wide range of conditions that
tive states. subjectively, this model identifies the may give rise to a range of subjective
two main sources of those mental experiences found within the fifth
The “Five Domains” model presents experiences. The first is the feelings “mental” domain. The net impact of
a useful framework for undertaking and sensations (collectively known as all of these experiences is assessed
systematic and structured assess- “affects”) that motivate animals to un- as representing the animal’s welfare
ments of animal welfare in these dertake behaviours considered to status. Modern zoos and aquariums
terms. This model outlines four physi- be essential for their survival. These should provide opportunities for the
cal/functional domains of “nutrition”, include thirst motivating an animal to animals in their care to experience
“environment”, “physical health” and drink, hunger motivating it to eat and positive welfare states.
“behaviour”, and the fifth domain, pain indicating things to avoid. These
which is the animal’s “mental” state and other survival‑related factors are In this edition of the WAZA Magazine,
(see figure). The Five Domains model typically covered within the domains we have compiled various conceptual
forms the basis of the World Zoo and of “nutrition”, “environment” and and practical approaches to how
Aquarium Animal Welfare Strategy. “physical health”. progress towards positive animal
welfare can be achieved by zoos and
The fourth domain of “behaviour” aquariums. This includes articles on
captures the second source of sub- taxa that are challenging and contro-
jective experiences, which can be versial to keep in human care, such
negative or positive, and relates to as elephants, dolphins, polar bears
animals’ perception of their external and great apes. Collectively, these
circumstances. Negative examples articles demonstrate the value of sci-
include: threat eliciting fear, isola- entific research, often multi‑institu-
tion leading to loneliness and low tional and longitudinal, to provide an
stimulation to boredom; and positive evidence base for ensuring that the
examples include: security engender- animals kept in our care experience
ing confidence and pleasure giving positive welfare states – in accord-
rise to a sense of reward. ance with the Five Domains model.
We hope that this edition of the
WAZA Magazine will substantially
strengthen our community’s efforts
to make caring about animals in zoos
1
WAZA Chief Conservation Officer and aquariums continuous with car-
2
WAZA Executive Director ing for them in the wild.
2 WAZA 16 (2015)
Georgia J. Mason1,*
Using Species Differences in Health
and Well‑being to Identify Intrinsic
Risk and Protective Factors
Summary Species Differences Using Species
in Animal Welfare Differences to Test
The diverse species living in zoos vary Hypotheses about Intrinsic
in their propensities for good captive The 10,000+ species kept in zoos Risk and Protective Factors
health and welfare. This variation are not all managed in fully evi-
yields opportunities to answer ap- dence‑based, optimised ways. Con- What biological characteristics
plied and fundamental research ques- sequently, although zoo animals are predict how well different species
tions via comparative methods. These typically healthier, longer‑lived and adjust to captive life? These can be
methods can harness this variation to more fecund than their free‑living identified empirically via comparative
statistically identify intrinsic risk and conspecifics, in some species captive methods, in which statistical rela-
protective factors influencing how individuals often survive and breed tionships between species‑typical
well species of different niches adjust less well than might be expected, and traits and outcomes of interest are
to captivity. Known or potential risk display physiological and behavioural investigated using data from mul-
factors include certain foraging styles, signs of stress. Even taxonomically tiple species (each being one unit
and being wide‑ranging or migratory, close species can vary. Ring‑tailed le- of replication). Such techniques are
timid and/or vulnerable to extinction. murs, for example, typically show few common in evolutionary and eco-
Empirically identifying which specific veterinary, breeding or behavioural logical research (Mason 2010; Mason
traits help predict captive welfare problems, while gentle and black et al. 2013). However, only recently
provides an objective way to specify lemurs are harder to breed success- have they been used to investigate
behavioural needs; suggests how to fully and more prone to stereotypic animal welfare, perhaps because
improve husbandry; and could help behaviour (Mason 2010). Similar while their logic is simple, the need to
decide which species to prioritise for contrasts exist within many genera control for three potential confounds
conservation in zoos. Such data could (Clubb & Mason 2007; Müller et al. can make implementation complex
also be used to test certain funda- 2012; Pomerantz et al. 2013). (Clubb & Mason 2007; Mason 2010;
mental evolutionary hypotheses. Müller et al. 2012; Pomerantz et al.
Differences between captive and an- 2013). One of these potential con-
cestral environments help explain such founds is inherent similarity between
variation: in captivity, the forms of closely related species, making them
food and shelter provided may be statistically non‑independent (Fig. 1).
evolutionarily new; climates may be The second is that intrinsic differ-
different; there is close contact with ences in pace of life and reproductive
humans; and abilities to range, explore strategy must be factored in, when
and make choices are constrained. using dependent variables related
Species’ natural lifestyles may help to life history (e.g. reproductive
determine whether any of these variables or average lifespan) to infer
differences are obstacles to success. the effects of captivity. The third is
In free‑living wild animals adjusting to husbandry (e.g. relative exhibit size or
novel habitats (e.g. colonising cities), management related to studbooks),
species thrive best if pre‑adapted to which may systematically vary with
cope well with change, and/or when taxon; to pinpoint true influences of
mismatches between new and ances- natural lifestyle, any species differ-
tral environments are relatively small ence in husbandry must therefore be
(reviewed by Mason 2010; Mason et controlled for.
al. 2013). The same principles seem
applicable to animals brought into
captivity: differences between captive
1
Department of Animal Science, and ancestral environments will be
University of Guelph, Guelph, ON, Canada minor and/or easily adjusted to for
* E‑mail for correspondence: some species, but large and/or hard to
gmason@uoguelph.ca accommodate for others.
WAZA 16 (2015) 3
Figure 1 a b
The plot in (a) shows hypothetical data from 10 carnivore species, showing an apparent
relationship between natural reliance on burrowing and infant mortality in captivity, which
could indicate that certain species should be allowed to construct their own burrows.
However, this conclusion is premature: (b) reveals that half the hypothetical data come from
Panthera (circles) and half from mustelids (stars). Because each group shares traits inherited
from a common ancestor, the Panthera are inherently similar, likewise the mustelids.
The non‑independence of these taxonomically similar data points makes it inappropriate
to draw a regression line through them as in (a). Custom statistical techniques that take
relatedness into account are therefore needed.
What Potential Risk and
Protective Factors May Figure 2
Operate in Zoos?
Being intrinsically wide‑ranging or
migratory. Ros Clubb and I investi-
gated whether the degrees to which
captivity constrains hunting, ranging
or other aspects of natural lifestyle
predict stereotypic behaviour and
captive infant mortality in carnivores
(e.g. Clubb & Mason 2007). Being
large and wide‑ranging, and travel-
ling relatively long distances each Stereotypic behaviour in carnivores is more time consuming in large, naturally wide‑ranging
day in the wild, emerged as risk species: across 20 species, body weight and minimum home‑range sizes extracted from field
studies predicted this behaviour’s severity in affected individuals – PB = polar bear, L = lion,
factors (Fig. 2). A decade after these AF = arctic fox, AM = American mink (Clubb & Mason 2003; figure reprinted with permission from
data were collated, Jeanette Kroshko Nature 425: 473–474). The relationship became more significant if only pacing was considered
re‑did the work for her MSc thesis, (Clubb & Mason 2007). Note that the figure is a simple cross‑species plot; final analyses
controlled for phylogenetic non‑independence.
adding additional data, new species
and more stringent controls for small
sample sizes. She could not replicate
the infant mortality result. However, Pomerantz et al. (2013) found similar lifestyle, such as more opportunities
she confirmed that species‑typical effects in primates: across 24 species, to disperse or explore, multiple den
natural home‑range sizes and daily average natural day journey length sites and/or greater day‑to‑day envi-
travel distances predict the intensity tended to predict levels of pac- ronmental variability, might be good
of stereotypic behaviour (irrespec- ing and route‑tracing (while these ways to improve exhibits, especially
tive of body size); newly found that animals’ other common abnormal to tackle stereotypic route‑tracing.
average “prey chase” distance does behaviour, hair‑pulling, was pre- They also suggest that being natu-
too, suggesting that certain hunt- dicted by natural group size). To- rally sedentary and little‑ranging
ing styles place species at risk; and gether, these studies suggest that pre‑adapts species to captivity.
showed that pacing and route‑trac- offering the correlates of a ranging
ing were the specific stereotypic
activities best predicted by these
variables.
4 WAZA 16 (2015)
Looking to future work on other As for future work, bird species that Conservation status in the wild. Con-
taxa, seeking similar patterns in birds readily develop new foraging modes servation breeding has been said to
could be fruitful because in the in the wild cope well when translo- be more challenging for endangered
wild, “resident” avian species (those cated or exposed to other evolution- birds than their non‑endangered
staying in one location year‑round) arily new environments (reviewed close relatives, while species that
are typically better than migrants at by Mason 2010; Mason et al. 2013), breed well in research laborato-
adapting to new environments (e.g. and dietary generalists have been ries (e.g. Norway rats and rhesus
establishing self‑sustaining popula- proposed to adjust well to captivity. monkeys) are often invasive when
tions when translocated; reviewed Together, this suggests that species living free. Furthermore, one study
by Mason 2010; Mason et al. 2013). with flexible diets might be particu- suggested that across captive canids,
Restricted ranging has also been larly easy to keep in zoos; a simple endangered species had higher pup
suggested to be a welfare risk factor hypothesis to test. Focussing on mortality than unthreatened species.
for some cetaceans and callitrichids; abnormal behaviour, oral stereo- Potential reasons for these possible
further testable hypotheses for fu- typic behaviours in hoofstock (e.g. links could be that species‑typical
ture research. tongue‑twirling) and parrots (e.g. risk factors predicting vulnerability
feather‑plucking) have been suggest- in the wild are similar to those likely
Natural diets or foraging style. As ed to derive from redirected natural to predict vulnerability in captivity:
mentioned, “prey chase” distances foraging. Once again, this hypothesis being migratory or wide‑ranging
predict pacing in carnivores, sug- is testable; if correct, natural food rather than sedentary; specialist
gesting that mimicking this aspect handling times or daily foraging time rather than generalist; and timid
of foraging could be an effective budgets should predict tendencies to rather than bold (reviewed by Mason
enrichment. However, this analysis develop these abnormal behaviours. 2010; Mason et al. 2013).
was based on few species and needs
replication. More robust and impres- Timidity. Timid species are fearful and So do “weed species” succeed eve-
sive are findings from Müller et al. stressed even when faced with famil- rywhere, while others are vulnerable
(2012) who analysed data from 78 iar threats, showing little habituation. both in the wild and in zoos? Some
ruminant species to relate natural This is problematic when eliciting preliminary evidence supports this.
foraging niche to captive survivor- stimuli are actually harmless. Heini Jonathan Jeschke and David Strayer
ship. They cleverly controlled for Hediger suggested decades ago collected data on 99 vertebrate spe-
species differences in normal intrinsic that differential fearfulness could cies moved between North America
life expectancy by calculating the help explain why zoo life is stress- and Europe, cataloguing the fates of
ratios of mean lifespan in captivity ful for some species but not others. translocated populations. Together,
to the maxima ever recorded. Across Furthermore, recent avian research Jonathan Jeschke and I investigated
females (for whom sample sizes shows that in the wild, species that whether species coping well with
were larger and intra‑specific aggres- are particularly scared of humans such translocations also apparently
sion not an issue), “relative lifespans” have shown the greatest population adjust readily to captivity. We clas-
negatively co‑varied with spe- declines in Europe and are least likely sified each species as to whether or
cies‑typical percentages of browse to colonise cities (reviewed by Mason not being “commonly captive” (e.g.
(vegetation from woody plants) 2010; Mason et al. 2013). It thus often farmed, used in research, held
in the natural diet, showing that the seems plausible that timid species
needs of grazing species have been may be relatively hard to keep well
more readily accommodated by zoos in captivity, while bold species are
than those of browsers. pre‑adapted to succeed; a fascinat-
ing hypothesis to test.
WAZA 16 (2015) 5
in zoos or kept by private individuals). Conclusions References
“Common captives” proved signifi-
cantly more likely to establish after The diversity of species kept in zoos • Clubb, R. & Mason, G. J. (2007)
translocation than species rarely kept can yield insights into animal welfare Natural behavioural biology as
captive, suggesting that similar traits that are both practically and funda- a risk factor in carnivore welfare:
predispose animals to cope with both mentally important. It is recognised how understanding species dif-
types of novel environment (Mason that not all aspects of natural life ferences could help zoos improve
et al. 2013). need to be mimicked in captivity, but enclosures. Applied Animal Be‑
that some – those meeting a spe- haviour Science 102: 303–328.
However, there are some counter‑ex- cies’ behavioural needs – should be. • Mason, G. J. (2010) Species differ-
amples (Mason et al. 2013), and Comparative approaches can provide ences in responses to captivity:
Jeanette Kroshko’s research found objective ways to identify such stress, welfare and the compara-
no relationships between IUCN Red needs. They also allow the test of tive method. Trends in Ecology
List status and captive carnivores’ hypotheses that would be challeng- and Evolution 25: 713–721.
vulnerability to infant mortality or ing to test experimentally, and make • Mason, G., Burn, C. C., Dallaire,
stereotypic behaviour. This could good, cost effective use of existing J. A., Kroshko, J., McDonald
reflect differences between taxa; the data. Practically, their outcomes can Kinkaid, H. & Jeschke, J. M.
many complex reasons behind threat help suggest new ways to improve (2013) Plastic animals in cages:
status; or that differential manage- husbandry. They could also help behavioural flexibility and
ment may mask such relationships: zoos make population management responses to captivity. Animal
Müller et al. (2012) showed that decisions. As several recent analy- Behaviour 85: 1113–1126.
ruminant species managed with ses reveal, keeping 10,000+ species • Müller, D. W. H., Bingaman
international studbooks achieve comes at a price: population sizes Lackey, L., Streich, W. J., Fickel,
longer relative lifespans, suggest- are tiny for most. Keeping larger J., Hatt, J.-M. & Clauss, M. (2011)
ing that threatened taxa receive populations of fewer species seems Mating system, feeding type and
more assiduous care. More research advisable, but which to select is de- ex situ conservation effort deter-
investigating the hypothesised links bated. Considering intrinsic abilities mine life expectancy in captive
between vulnerability in the wild and to fare well in captivity seems wise ruminants. Proceedings of the
in zoos is therefore needed, especial- in such discussions, in order to favour Royal Society B 278: 2076–2080.
ly given that threatened species are those inherently most likely to form • Pomerantz, O., Meiri, S. & Terkel,
under‑represented in zoos; could this healthy, self‑sustaining populations. J. (2013) Socio‑ecological factors
perhaps reflect that these species are correlate with levels of stereo-
intrinsically harder to keep? The types of comparative approach typic behavior in zoo‑housed
described here could also yield novel primates. Behavioural Processes
insights into the evolution of behav- 98: 85–91.
iour and stress responses. For exam-
ple, they could reveal which aspects
of behaviour are flexible, to test
hypotheses about the evolution of
phenotypic plasticity; help elucidate
why species’ responses to anthropo-
genic disturbance vary; and provide
insights into historical domestica-
tions. Data from the diverse species
held in zoos are thus a potentially
superb, largely untapped resource for
fundamental biologists.
6 WAZA 16 (2015)
David Shepherdson1,* & Nadja Wielebnowski1
The Power of Multi‑institutional
and Longitudinal Studies for Zoo
Animal Welfare Research
Summary Introduction
Zoo animal welfare research is often Traditionally, sample size has been approach. Another study by Wieleb-
compromised by small sample sizes the bane of zoo research. For obvious nowski et al. (2002) on husbandry and
and a multitude of key variables reasons, studies tend to have small exhibit variables related to clouded
not usually under the control of the sample sizes and are restricted to leopards provides another example
researcher. However, careful study one or two institutions. These kinds of the impact this approach can have
design and the use of multi‑institu- of studies limit the degree to which for welfare management of a species.
tional comparative approaches and/or findings can be applied or generalised The primary challenge encountered
consistent long‑term data collection to the larger zoo population, either with the multi‑institutional approach
on even a small number of individuals because the circumstances of the is the logistical complexity and costs
over time can provide valuable scien- subjects or the institutions are unique of working with multiple institutions.
tific data, which can in turn be used or because the full range of variables Data security and ownership can also
to impact management and care are not adequately represented in the be a challenge.
decisions to improve animal welfare. dataset.
We highlight these two approaches A second approach, perhaps less
and provide specific examples of their Here, we explore and give examples common, is to collect detailed
impact on animal care and welfare. of two increasingly popular meth- and consistent records on smaller
odologies for improving the predic- numbers of individuals over long
tive power of zoo research. The periods of time and correlate changes
obvious answer to the problem of in individuals with changing events
limited sample size is to increase the over time. Oregon Zoo has been col-
number of animals and institutions lecting physiological and behavioural
involved in a given study. The study data from its Asian elephant herd
of stereotypic behaviour in polar for over 30 years, and Glaeser et al.
bears conducted by Shepherdson (2012) recently published an analysis
et al. (2013) is one example of this of female reproductive physiology
in Asian elephants based on this
extensive dataset. A major challenge
with this approach is maintaining
consistency in data collection over
long time periods in spite of changes
in personnel, exhibits, analytical
tools and techniques. In spite of their
respective challenges, both types of
studies illustrate nicely the benefits
of these approaches to allow for solid
scientific research in the zoo environ-
ment that also benefits animal care
and welfare.
1
Oregon Zoo, Portland, OR, USA
* E‑mail for correspondence:
david.shepherdson@oregonzoo.org
WAZA 16 (2015) 7
Figure 1 © Michael Durham/Oregon Zoo
Polar bear enrichment: working
to obtain food items frozen in ice.
tapes. A challenge of multi‑institu-
tional studies is consistency of data
collection and analysis. In this study,
behavioural data were collected via
video tape at each institution and
subsequently analysed at Oregon
Zoo by a small group of highly
trained observers. Faecal samples,
collected every two weeks, were
sent to Saint Louis Zoo’s endocrine
laboratory for analysis.
Using these techniques, we found
that on average polar bears spend
11% of their time engaged in ste-
reotypic behaviour, but that was
highly variable from institution to
institution. We found that stereotypic
behaviour was negatively correlated
with enrichment, number of bears
in the exhibit and whether bears
could see out of their exhibit. Also,
zoos that practiced positive rein-
forcement training were linked to
lower rates of pacing. Further, we
found that higher faecal glucocor-
ticoid concentrations were associ-
ated with higher rates of pacing and
Multi‑institutional Study smaller dry land exhibit area.
of Stereotypy in Polar Bears
These results suggest a link between
Polar bears are infamous for their A total of 20 North American zoos stress physiology and stereotypic
propensity to display repetitive, ap- (including Canada and the USA) behaviour in zoo polar bears. These
parently stereotypic pacing behav- agreed to partner with us on this findings also suggest that some eas-
iour in zoo exhibits. The goals of this year‑long study. Input variables ily available tools, namely environ-
study were to assess the magnitude consisted of exhibit, husbandry and mental enrichment (Fig. 1) and posi-
of the problem, attempt to identify climate factors. Output variables tive reinforcement training, may be
environmental correlates of the were performance of stereotypic effective at reducing the incidence of
behaviour and investigate poten- behaviour and faecal glucocorticoid these behaviours. Exhibit designers
tial links to reduced well‑being and levels. Input variables were collected should take note that providing polar
faecal glucocorticoid concentrations by direct observation and measure- bears with a view out of their exhibit
(Shepherdson et al. 2013). ment and by questionnaire surveys, and larger land areas are associated
with the exception of enrichment with both behavioural and physi-
that was assessed directly from video ological benefits.
8 WAZA 16 (2015)
Multi‑institutional Study
of Adrenal Activity,
Husbandry and Exhibit
Variables in Clouded
Leopards
Clouded leopards in zoos are known
to display a variety of behavioural
problems; for example, fur‑plucking,
tail‑biting, excessive pacing or hid-
ing, and severe mate incompatibility.
These problems generally indicate
poor animal well‑being and severely
hinder successful population man-
agement. In this study, we collected
hormone and behaviour data for
several weeks on 74 clouded leopards
at 12 zoos (Wielebnowski et al. 2002).
Using non‑invasive faecal hormone
monitoring, we found that some of
the observed behavioural problems
were associated with an increase
in faecal glucocorticoid concentra-
tions. This increase, in turn, was cor- Figure 2 © Michael Durham/Oregon Zoo
related with the following variables: Multi‑generational herd of Asian elephants
exhibit height, predator visibility at Oregon Zoo: social interactions and
and public display. For example, the Three Decades soft substrates are important for
elephant well‑being.
higher the exhibit the lower the fae- of Physiological and
cal glucocorticoid concentrations; Behavioural Monitoring
and, if predators were visible and ani- of Asian Elephants
mals were on constant public display, at Oregon Zoo
faecal glucocorticoid concentrations
were higher. Oregon Zoo has a long‑standing Asian elephants (Glaeser et al. 2012).
history of contributing substantially It showed that cycle length, while
In a follow‑up study, we tested the to the global knowledge on Asian relatively consistent over an individ-
impact of changes in exhibit features elephant reproduction. For example, ual’s lifespan, can vary substantially
experimentally (Butterworth et al. the Asian elephant reproductive cycle between individual elephants. The
2011). Available exhibit height was was first characterised at Oregon Zoo average Asian elephant cycle is about
altered through adding or removing (Hess et al. 1981). Indeed, Oregon 16 weeks long.
climbing structures, and the amount Zoo has the longest continuous
and type of available hiding spaces dataset on female and male Asian Because of our long‑term hormone
was changed. Data showed that elephant reproductive hormones ever monitoring of several successful
adding both climbing structure and collected and analysed, and data col- pregnancies over time, we can also
hiding space resulted in a decline of lection continues to this date. predict the due date for an upcoming
faecal glucocorticoid concentrations birth within a few days of the event
in the study animals. Once published, Based on the long‑term physiologi- and we can measure signs of impend-
these data were also used to inform cal data obtained through weekly ing birth using hormonal indicators.
the husbandry guidelines for the blood sample collection on all of In addition, this in‑depth physi-
management of this species. our elephants, it was found that ological monitoring together with
zoo elephants were able to become behavioural observations is used to
mature and ready to conceive much inform the social management of our
earlier than their wild counterparts. elephant herd (currently seven ele-
For example, males can breed suc- phants, three males and four females;
cessfully as early as five years of Fig. 2). Female cycles are monitored
age in zoos, while males in the wild to ensure that they are with a breed-
become sexually mature at around ing male only when appropriate and
11 years. A recent publication summa- desirable.
rised 30 years of data on eight femaleWAZA 16 (2015) 9
Monitoring the bulls helps us to Conclusions References
establish the musth cycles and bulls
can also be managed accordingly Multi‑institutional comparative as • Butterworth, A., Mench, J. A. &
to avoid unwanted breeding and well as longitudinal study designs Wielebnowski, N. (2011) Practi-
aggression. Based on our hormone have yielded much valuable informa- cal strategies to assess (and
studies, we know that a strong surge tion and are certainly key tools for improve) welfare. In: Animal
of testosterone occurs during musth. the study of zoo animal welfare. To Welfare, 2nd ed. (ed. by Appleby,
Since we have been monitoring male succeed with both of these types of M. C., Mench, J. A., Olsson, I. A.
elephants of all ages, we were able studies, the zoo community needs to S. & Hughes, B. O.), pp. 200–214.
to document the onset of musth be actively supporting and funding Wallingford: CABI Publishing.
in young males and correlate the projects of this type. Zoos, espe- • Glaeser, S. S., Hunt, K. E., Martin,
hormonal data with onset of sexual cially medium‑ to larger‑sized zoos, M. S., Finnegan, M. & Brown, J. L.
and other social behaviours. Fur- need to make an effort to establish (2012) Investigation of individual
thermore, we found that our adult an active “on grounds” research and group variability in estrous
males tend to experience their musth department with qualified research cycle characteristics in female
cycles around the same time. Indeed, staff to lead such study efforts. Asian elephants (Elephas maxi‑
one male coming into musth appears Also, engaging the academic com- mus) at the Oregon Zoo. Theriog‑
to trigger other bulls to start their munity that most zoo researchers enology 78: 285–296.
musth cycle. It is not known yet what are already linked to is an impor- • Hess, D. L., Schmidt, M. J. &
exactly triggers this synchronisation tant part of ensuring that valuable Schmidt, A. M. (1981) Endocrine
and why it is beneficial for bulls to scientific data that can be published and behavioral comparisons dur-
synchronise musth. We are in the in peer‑reviewed journals is properly ing the reproductive cycle in the
process of analysing the long‑term collected, analysed and disseminated Asian elephant Elephas maximus.
dataset on males and hope to learn in a timely fashion. Biology of Reproduction 24 (Suppl.
even more details about musth 1): 93A.
cycles and male reproduction during A recently completed, large‑scale • Shepherdson, D., Lewis, K. D.,
the next few years. multi‑institutional study exemplifies Carlstead, K., Bauman, J. &
what can be accomplished if exten- Perrin, N. (2013) Individual and
Most recently we have started analy- sive collaboration and zoo support environmental factors associated
ses of past and current samples for is garnered. The elephant welfare with stereotypic behavior and
cortisol and we plan to look at these project, described in more detail by fecal glucocorticoid metabolite
data in combination with behaviour Carlstead & Brown (this issue), paves levels in zoo housed polar bears.
and correlate them with various the way for integrating previous Applied Animal Behaviour Science
life events and husbandry variables. approaches in zoo welfare research. 147: 268–277.
A benefit of taking part in the el- North American zoo researchers • Wielebnowski, N. C., Fletchall,
ephant welfare project (see below) is from different fields came together N., Carlstead, K., Busso, J. M. &
that we can now add movement and to address a welfare science need Brown, J. L. (2002) Noninvasive
recumbence using GPS devices and (addressing the question of welfare assessment of adrenal activity
accelerometers inserted into ankle status and associated variables associated with husbandry and
bracelets. Our long‑term monitoring in elephants in North American zoos) behavioral factors in the North
approach has therefore not only pro- and engaged with prominent welfare American clouded leopard popu-
vided us with the ability to effectively scientists at several universities. The lation. Zoo Biology 21: 77–98.
manage our herd with regards to Association of Zoos and Aquariums
reproductive and social health and (AZA) supported the approach and
welfare, but has also yielded much helped to ensure wide participation
valuable scientific data over the of its member institutions. Indeed, Moving forward, a study of this
years that contribute to the general almost all AZA zoos holding el- type integrates both approaches for
knowledge base of Asian elephant ephants participated in this study of the future: multi‑institutional and
biology, physiology and behaviour unprecedented scale and scope. Due longitudinal monitoring on a major
worldwide. to the fact that the study contained sector of a zoo animal population
almost the entire North American to establish a baseline of welfare
zoo population of African and Asian indicators and answer questions of
elephants, it was decided that data the relative impact of various man-
collected in this study can serve agement variables on welfare. We
to provide a baseline of AZA zoo hope that these examples will spark
elephant welfare similar to epidemio- additional welfare research on small
logical models provided by human and large scales and lead to increased
medicine studies. global networks of zoo and university
welfare researchers working jointly
to advance the emerging field of zoo
animal welfare science.10 WAZA 16 (2015)
Kathy Carlstead1,* & Janine Brown2
Using Science to Understand
Zoo Elephant Welfare:
Evaluation of Ovarian Cyclicity and
Keeper–Elephant Relationships
Summary Asking the Elephants
Significant attention has been The science of zoo animal welfare is to a broad range of facility‑based
directed towards the housing and developing into a field that guides measures (input variables). Data for
care of Asian and African elephants improvements in animal husbandry individual elephants were collected
in zoos, and many questions have through research that is multi‑dis- on‑site by zoo personnel, including
been raised about whether they ciplinary and multi‑institutional. photographs, video recordings, blood
can meet elephants’ environmental A team of zoo scientists, academic and faecal samples, veterinary ex-
and social needs in a manner that consultants and elephant managers aminations and technology‑assisted
promotes good welfare. Four years set up a study to evaluate Asian and observations of elephant movement.
ago, a research team set out to evalu- African elephant welfare in Associa-
ate the welfare of elephants in zoos tion of Zoos and Aquariums (AZA)-ac- The research made extensive use
accredited by the Association of Zoos credited zoos (Mellen et al. 2008) by of survey data obtained from staff
and Aquariums (AZA). Data were analysing animal‑based data on a va- members at each zoo. Elephant man-
collected on elephants’ daily lives, riety of welfare indicators. In a sense agers were asked to provide detailed
how they interact with each other we were asking the elephants what descriptions of facilities and manage-
and their keepers, and their physi- environmental and husbandry factors ment practices (e.g. exhibit space,
ological function. An epidemiological are the most important for enhanc- social groupings, flooring, feeding
approach was then taken to evaluate ing their welfare. With a 94% com- methods, training and handling pro-
husbandry and management factors mitment from AZA zoos holding cedures, veterinary care programme,
impacting welfare by looking at asso- elephants, the team collected a large enrichment programme) at each zoo
ciations between resource‑based en- amount of data on 266 elephants for each elephant, since not all indi-
vironmental/life‑history variables and in 70 zoos. The study was funded by viduals at a zoo experience the same
animal‑based indicators of welfare. a grant from the Institute of Museum housing and/or procedures. Keepers
We present a brief overview of two of and Library Services. provided information about their
our findings: factors associated with own attitudes towards and opinions
reproductive cycle status in females, An epidemiological approach was of elephants, and their relationships
and the quality of relationships be- used to examine multiple input varia- with elephants.
tween keepers and elephants. bles that predict indicators of welfare
(Carlstead et al. 2012). The welfare Here, we review some of the study
framework we used for elephants results relevant to reproductive
consisted of “gold standard” welfare function in female elephants, and
indicators, as well as some new meas- the quality of relationships between
ures that were developed and vali- keepers and elephants. More results
dated. This multi‑factorial approach of the study have been submitted
to welfare was intended to provide as a series of papers for concurrent
a more holistic view of best manage- publication in the open‑access journal
ment practices for elephants. All PLoS ONE.
welfare indicators (outcomes) were
animal‑based (e.g. body condition,
1
Honolulu Zoo Society, Honolulu, foot and joint health, walking rates
HI, USA (formerly) and recumbence, stereotypy, ovarian
2
Center for Species Survival, Smithsonian cycling, prolactin, cortisol) and were
Conservation Biology Institute, statistically analysed, using univariate
Front Royal, VA, USA and multivariable models, in relation
* E‑mail for correspondence:
kcarlstead@honzoosoc.orgWAZA 16 (2015) 11
Figure 1 Examples of concentrations
of serum progesterone in
(a) normal cycling, (b) irregular cycling
and (c) non‑cycling elephants.
a
making a positive appraisal of the
quality of the zoo environment when
diverse enrichment provides dynamic,
b changing surroundings, stimulating
investigation and other behaviours.
In wild savannah elephants, similar
positive appraisals of a changing en-
vironment, particularly with respect
to cues signalling incipient water and
forage availability, are important for
stimulating ovarian cycling when
conditions are favourable for concep-
c tion and pregnancy (Wittemyer et
al. 2007).
Univariate results indicated that
social experience was also associ-
ated with ovarian cycling for female
African elephants. Females that
are socially separated, even if they
have access to one or more other
elephants through a barrier, have
a decreased chance of cycling. We
know that sociality is important for
elephants behaviourally, and this sug-
Management Factors gests that it also may be important
Associated with Ovarian physiologically in terms of supporting
Cycles of Female Elephants normal ovarian function.
Reproductive success contributes Rates of normal cycling, non‑cycling Although a larger percentage of
to the sustainability of zoo elephant and irregular cycling were 73.2, 22.5 female Asian elephants had normal
populations. Lack of reproductive and 4.2% for Asian elephants, and ovarian cycles, univariate analyses
function has long been considered an 48.4, 37.9 and 13.7% for African indicated that more time spent
indicator of reduced welfare. Ques- elephants, respectively, all of which in spaces with free choice of being
tions were asked about the impacts differed between species (Brown et indoors or outdoors was associated
that zoo environments may have on al. 2015). Age was strongly associated with an increased likelihood of nor-
the biological systems regulating with an increased risk of non‑cycling mal cycles. Time spent in spaces with
reproductive activity. Some female for both species. In addition, three free indoor/outdoor choice was also
elephants in AZA zoos fail to show management factors were found to negatively correlated with faecal cor-
normal 13–17 weeks ovarian cycles, be related to ovarian cycle status: tisol concentrations for female Asian
which may be influenced by social enrichment and sociality for African elephants, and older, non‑cycling
and/or environmental management elephants, and choice of space for females had higher serum cortisol
practices. For this study, bi‑weekly Asian elephants. values compared to cycling females
blood samples were collected from of the same age. While not conclusive
75 Asian and 93 African female We used a diversity index of enrich- until further experimental research is
elephants of reproductive age (8–55 ment that takes into account the type conducted, this is a suggestion that
years) over a 12-month period for of enrichment used and the frequen- being able to move freely between
analysis of serum progestogens and cy of its use. Multivariable modelling the indoor and outdoor areas of
prolactin (Fig. 1). indicated that enrichment diversity exhibits might reduce stress that
increases the chance that a female interferes with normal reproductive
African elephant will cycle normally. function in elephants.
This is possibly due to elephants12 WAZA 16 (2015)
Figure 2 © Manny Dayao
A Honolulu Zoo elephant keeper makes a shower more enriching
for Mari and Vaigai by spraying them from a novel location.
Keeper–Elephant
Relationships
In addition to ovarian cycling, we Using multivariable modelling, we The quality of relationships between
also evaluated prolactin as another identified four input variables related humans and animals can be consid-
welfare indicator. Prolactin is a pi- to the manifestation of this endo- ered positive, neutral or negative for
tuitary hormone that has over 300 crine disorder among female African animal welfare. Negative impacts of
known functions involving multiple elephants. Age was positively associ- human–animal relationships are well
systems, including reproduction and ated with the chance that a female known for farm animals, with studies
stress. In other species, prolactin has will be hyperprolactinemic, as was showing that caretakers’ attitudes
direct and indirect effects on follicle being exposed to a higher number and behaviour towards their ani-
development, and is finely regulated of social groups. The latter may be mals can cause fear and stress in the
by positive and negative feedback related to social instability, a known animals (reviewed by Waiblinger et al.
mechanisms. Too much prolactin, stressor for elephants. We also found 2006). Therefore, we used elephant
called hyperprolactinemia, is a com- that increased enrichment diversity stress responses to keepers as an
mon cause of infertility in women, and feeding diversity (food presented indicator of welfare. We character-
and is associated with a disruption in a foraging device, hidden or hang- ised the quality of the relationships
in normal ovarian cycle activity. ing) is associated with a female being between elephants and their caretak-
Hyperprolactinemia was absent less likely to have hyperprolactine- ers by comparing keeper attitudes
in female Asian elephants, but 53% of mia. Again, seeing these links with towards and opinions of elephants
non‑cycling female African elephants environmental enrichment indicates with varying levels of elephant serum
were hyperprolactinemic. By contrast, that having more things to do in ex- cortisol measured in response to
no cycling females exhibited consist- hibits, including having to look or the blood sampling procedure by
ently elevated prolactin, so there work harder for food, may promote keepers. Keepers’ perceptions about
appears to be a relationship between more normal physiological function and attitudes towards elephants
this condition and compromised in elephants. were assessed via a questionnaire
ovarian activity in female African
elephants.WAZA 16 (2015) 13
Zoo Elephant Welfare, References
Going Forward
• Brown, J. L., Paris, S., Pra-
from which their answers were then From our study of elephant welfare do‑Oviedo, N., Meehan, C.,
grouped into a smaller number of fac- in North American zoos we are gain- Hogan, J. N., Morfeld, K. &
tors that describe their interactions ing tools to help improve conditions Carlstead, K. (2015) Reproduc-
with elephants. The keeper factors for our elephants. The results re- tive health assessment of female
were averaged for all keepers at a zoo ported here suggest that zoos should elephants in North American
and then entered into a multivari- commit to robust environmental zoos and association of husband-
able model predicting serum cortisol enrichment and feeding programmes ry practices with reproductive
values of individual elephants. that increase both the types of meth- dysfunction in African elephants
ods employed and the frequency (Loxodonta africana). PLoS ONE,
Lower stress responses in African of implementation, and continue in review.
elephants were associated with careful selection of elephant keepers • Carlstead, K., Mench, J. A.,
having keepers who reported a high with positive attitudes and empathy Meehan, C. & Brown, J. L. (2013)
degree of interactions with elephants towards elephants. An epidemiological approach
that are positive (versus neutral or to welfare research in zoos: the
negative). Keepers also answered It is important to remember that elephant welfare project. Journal
questions on the Davis Interpersonal welfare is complex, especially for of Applied Animal Welfare Science
Reactivity Index, a widely used re- elephants, and many of the factors 16: 319–337.
search tool to assess human‑directed that we evaluated are interrelated. • Mellen, J. D., Barber, J. C. & Miller,
empathy. Higher scores of keepers Additional experimental studies are G. W. (2008) Can we assess the
for “empathic concern” were corre- needed to tease apart what input fac- needs of elephants in zoos? Can
lated with lower cortisol concentra- tors are most important for specific we meet the needs of elephants
tions in African elephants. For Asian welfare outcomes. Hopefully, using in zoos? In: Elephants and Ethics:
elephants, the more the keeper science to provide valid evidence Toward a Morality of Coexist‑
believes in the importance of positive of welfare impacts will guide our ence (ed. by Wemmer, C. M. &
physical contact between keeper and decisions around next steps to con- Christen, C. A.), pp. 307–324.
elephant, such as rubbing, touching tinue our focus on the welfare of all Baltimore, MD: Johns Hopkins
and petting, the lower elephants’ elephants in zoos. University Press.
stress responses. This was irrespec- • Waiblinger, S., Boivin, X., Peders-
tive of whether contact with the Acknowledgements en, V., Tosi, M.-V., Janczak, A. M.,
elephants was under protected or Visser, E. K. & Jones, R. B. (2006)
free‑handling conditions. Although Project principal investigators: Anne Assessing the human–animal
we were not able to directly assess Baker, Janine Brown, Kathy Carlstead, relationship in farmed species:
keeper behaviours towards elephants, Candice Dorsey, Mike Keele, Jill Mel- a critical review. Applied Animal
we did find that self‑reports of talking len, Joy Mench, David Shepherdson Behaviour Science 101: 185–242.
to elephants casually or using verbal and Nadja Wielebnowski. Project • Wittemyer, G., Ganswindt, A. &
commands when training are be- manager: Cheryl Meehan. Academic Hodges, K. (2007) The impact of
haviours correlated to these positive consultants: Georgia Mason, Anne ecological variability on the re-
keeper attitudes. Marie de Passillé and Jeff Rushen. Ad- productive endocrinology of wild
ditional researchers: Christie Alligood, female African elephants. Hor‑
Therefore, these results suggest that Mary Bonaparte‑Saller, Brian Greco, mones and Behavior 51: 346–354.
keepers shape the quality of their Jennifer Hogan, Mathew Holdgate,
relationships with elephants, with the Katherine Leighty, Lance Miller, Kari
opportunity to enhance elephant wel- Morfeld, Natalia Prado‑Oviedo and
fare with their perceptions, attitudes Joseph Soltis.
and behaviours towards them (Fig. 2).
Continued study of keeper–elephant
relationships could eventually help
inform keeper selection and training.14 WAZA 16 (2015)
Lance J. Miller1,*, Randall S. Wells1, Rita Stacey1, F. William Zeigler1,
Jessica C. Whitham1 & Michael Adkesson1
Animal Welfare Management of
Bottlenose Dolphins at the Chicago
Zoological Society’s Brookfield Zoo
Summary Preventative Health Animal Training
Programme
In 1961, the Chicago Zoological Soci- Positive reinforcement training is the
ety’s Brookfield Zoo became the first As part of our ongoing animal welfare primary tool, coupled with strong
inland facility to exhibit bottlenose management, a robust preventative trainer–animal relationships, used
dolphins for public viewing. Since health programme plays a critical to assist with animal husbandry and
then, dolphin welfare has improved role in maintaining optimal animal veterinary procedures. Our preventa-
due to increases in knowledge about welfare. Bottlenose dolphins at the tive health programme sampling is
day‑to‑day husbandry, advances Chicago Zoological Society’s Brook- accomplished through conditioning
in medical technology and research field Zoo are assessed daily by animal the animals to voluntarily partici-
on veterinary care, husbandry and care staff and receive semi‑annual pate. Having the animals participate
wild dolphins. These efforts allow the preventative veterinary exams. Diag- in their own care gives them more
Chicago Zoological Society to take nostic testing is performed quarterly choice and control within their en-
a holistic approach to the animal and includes comprehensive blood vironment, two aspects thought to
welfare management of dolphins. tests, ultrasound examinations and enhance animal welfare. Training ani-
This involves a collaboration of many cytological examinations of chuff mals for these different procedures
departments (animal care, veterinary (breath exhalate), gastric and faecal also allows for better development of
services, behavioural husbandry, samples. Weekly measurements of human–animal relationships that can
nutrition, animal welfare research weight and blubber thickness as well benefit animal welfare.
and field research) working to- as monthly length and girth measure-
gether to ensure that each individual ments are collected to ensure that In addition to the dolphins participat-
dolphin thrives. From operating the animals fall within body condition ing in their preventative health pro-
world’s longest‑running study of norms developed from wild bottle- gramme, they also participate in our
a wild dolphin population in Sarasota nose dolphins. This extensive data- “Dolphins in Action” programme.
Bay, FL and the extensive experience base of medical information specific This educational programme allows
gained through the management to each dolphin provides a power- visitors to see the dolphins engaged
of animals at Brookfield Zoo, the ful tool for assessing any changes in species‑appropriate behaviours
Chicago Zoological Society has an in animal health or welfare, which we with the goal of connecting them
unmatched wealth of knowledge on consider best practice in monitoring to nature. Previous research has
the care and welfare of bottlenose dolphins in zoos and aquariums. demonstrated that these types of
dolphins. programmes are potentially reward-
ing for the animals by giving them
more stimulation, choice and control
within their environment (Miller et al.
2011). Thus, positive reinforcement
training can provide many animal
welfare benefits.
1
Chicago Zoological Society,
Brookfield, IL, USA
* E‑mail for correspondence:
lance.miller@czs.orgWAZA 16 (2015) 15
Figure 1 © Chicago Zoological Society
Three generations of bottlenose dolphins at the Chicago Zoological Society’s Brookfield Zoo.
Social Enrichment Nutrition
While other enrichment opportuni- Maintaining stability of the group is Research on the diets of bottlenose
ties are provided (ice blocks, balls, important for social dynamics. This, dolphins under professional care have
etc.), it is likely that a species‑ap- in turn, aids in improving the learning been found to differ from wild bottle-
propriate social environment is the experience through familiarity and nose dolphins (Slifka et al. 2013). This
best form of enrichment for dolphins. acceptance of each animal within the has led to further research examin-
As social mammals, they engage social grouping. For example, expe- ing the impact of those diets on the
in a wide variety of interactions, and rienced females raising young act as health and welfare of the dolphins at
the number of potential interactions role models for daughters, nieces Brookfield Zoo. Iron storage dis-
increases exponentially with increas- and grand‑daughters that have yet ease is recognised in dolphins under
ing group size. We make every effort to reproduce. Inexperienced females professional care. It was thought that
to try to recreate naturalistic social often share in the parenting process, differences in the diets of managed
groupings based on findings from providing them with valuable lessons versus wild dolphins could affect the
our long‑term field research (e.g. they will need later in life. incidence of this disease. However,
Wells 2014). Typical composition of examination of the iron levels in the
the dolphins at Brookfield Zoo over species of fish commonly fed to the
the past two decades has included dolphins at Brookfield Zoo suggests
nursery groups of mothers and their that they receive equal to, or less
offspring from multiple generations, than, their wild counterparts. Further
along with individual or paired breed- research is needed to understand
ing males (Fig. 1). how iron storage disease and differ-
ences in diets may impact the health
and welfare of dolphins. The Chicago
Zoological Society is continuing ef-
forts to optimise animal welfare and
has altered diets to better reflect the
diversity, type and seasonal changes
of species common to bottlenose
dolphins in Sarasota Bay, FL.You can also read
