Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 March 2020 | 12(4): 15426–15435
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
doi: https://doi.org/10.11609/jott.5622.12.4.15426-15435
#5622 | Received 15 December 2019 | Final
received 28 February 2020 | Finally accepted 04 March 2020
Analysis of stereotypic behaviour and enhanced management in captive Northern
Giraffe Giraffa camelopardalis
housed at Zoological Garden Alipore, Kolkata
Tushar Pramod Kulkarni
Associate, Giraffe Conservation
Foundation, Eros, Windhoek, Namibia.
Editor: Karin Schwartz, WildTrack, Milwaukee, Wisconsin, USA. Date of publication: 26 March 2020
(online & print)
Citation:
Kulkarni, T.P. (2020). Analysis of stereotypic behaviour and enhanced management in captive Northern
Giraffe Giraffa camelopardalis
housed at Zoological Garden Alipore, Kolkata. Journal of
Threatened Taxa 12(4): 15426–15435. https://doi.org/10.11609/jott.5622.12.4.15426-15435
Copyright: © Kulkarni 2020. Creative Commons Attribution 4.0 International
License. JoTT
allows unrestricted use, reproduction, and distribution of this article in any
medium by providing adequate credit to the author(s) and the source of
publication.
Funding: This research received no external funding.
Competing interests: The author declares
no competing interests.
Author details: Tushar Kulkarni
has undertaken collaborative work with Zoological Garden Alipore, Kolkata,
India and with West Bengal Zoo Authority (WBZA), West Bengal, India, on giraffe
behaviour studies, education and genetic studies of
giraffe at Zoological Garden Alipore. He has also associated with Giraffe
Conservation Foundation (GCF), Namibia, for a number of years and have
collaborated on a range of giraffe conservation and management
initiatives. He has presented the
current work at International Giraffid Conference held at Brookfield zoo,
Chicago, USA, in May 2016.
Acknowledgements: I would like to thank Darren E. Minier
(Oakland Zoo), Dr. Kanailal
Ghosh, Ashish Kumar Samanta, Susanta
Bhattacharyya, Ramchandra Nath and Sitaram (Zoological Garden Alipore), Sarah
Garry (Plymouth University), Douglas Tyler Laemmle and Cory Fagg
(Fort Wayne Children’s Zoo), Allison (Suda) Malkowski and Chelsea Mihalick
(Roosevelt Park Zoo), Nate Aalund (Saint Louis Zoo),
Lou Keeley (Lincoln Park Zoo), Amy Phelps (San Francisco Zoo), Jason Pootoolal (Toronto Zoo), Dr.
Julian Fennessy (Giraffe Conservation Foundation) and
Dr. Michael Brown (Giraffe Conservation
Foundation/Smithsonian Conservation Biology Institute) for their valuable
support during the course of this study.
Abstract: In the wild, giraffes live complex social lives
exhibiting fission-fusion social systems.
They have sophisticated communication which likely forms a crucial
component regulating subgroup dynamics.
They spend a large part of their day browsing and traveling over large
distances. In captivity, lack of
continuous browsing opportunities and limited space can lead to various
abnormal and stereotypic behaviours. These stereotypic behaviours
can have cascading detrimental health consequences. A behavioural analysis
of stereotypic behaviours in giraffes under human
care was conducted to evaluate sources of variation within a population and
provide management recommendations. The
aim of this investigation was threefold: 1. to examine current behaviour of giraffes in Zoological Garden Alipore, Kolkata
to advise on their enhanced management; 2. to highlight any behavioural
abnormalities and recommend enrichment mechanisms; and 3. to compare the
observed stereotypic behaviours with behaviour described in other zoological institutions and in
the wild to provide a focal trajectory in the development of guidelines. Four individuals (two adult males, one adult
female, and one male calf) were observed outdoors for seven days, three times a
day for 30 minutes by instantaneous scan sampling method. During the observation period, the giraffe
exhibited oral stereotypy more than any other behaviour
recorded, though this was recorded disproportionally between individuals. The giraffe spent a larger amount of time
exhibiting oral stereotypy compared to feeding/foraging activities. The study suggests incorporating diet and
feeding strategies with provision of natural browse as well as offering
enrichment methods to increase the foraging time using various time-engaged
feeding devices to mitigate the observed abnormal stereotypic behaviour.
Additionally, recommendations are made for expanding the size of the
open enclosure to meet guidelines by the Central Zoo Authority, as a minimum.
Keywords:
Animal welfare, behavioural abnormalities,
enrichment, Giraffe, stereotypy.
Introduction
Giraffes Giraffa spp.
are tallest of the land mammals, largest of the ruminants, and are mega
herbivores. Over the past decade the
first-ever comprehensive DNA sampling and analysis (genomic, nuclear, and
mitochondrial) from all major natural populations of giraffe was undertaken
throughout their range in Africa. As a
result, an update to the traditional taxonomy now exists. This study revealed that there are four
distinct species of giraffe and likely five subspecies (Fennessy et
al. 2016; Winter et al. 2018).
The four species are Masai Giraffe G. tippelskirchi, Northern Giraffe G. camelopardalis, Reticulated Giraffe G. reticulata,
and Southern Giraffe G. giraffa. Nubian giraffe G. c. camelopardalis,
Kordofan Giraffe G. c. antiquorum and West
African Giraffe G. c. peralta are the three
subspecies of the Northern Giraffe, while Angolan Giraffe G. g. angolensis, and South African Giraffe G. g. giraffa fall under the Southern Giraffe. Rothschild’s Giraffe is genetically identical
to the Nubian Giraffe, and thus subsumed into it (Winter et
al. 2018). Based on this research,
we refer to the updated giraffe taxonomy of four species.
The pursuit of forage constitutes a large portion of
the daily activities of giraffe (Dagg & Foster
1976) with studies suggesting that wild giraffe spend approximately 51–59% of
the day feeding/foraging (Fennessy 2004). Giraffes move constantly while feeding due to
spatially heterogeneous distribution of forage and the protection mechanisms of
browse plants (EAZA 2006). As such,
daily foraging and rumination times make up a large proportion of their
activities. Food and energy intake,
therefore, remains distributed over the whole day for giraffe due to their
specialized feeding ecology. Pellew (1984) observed wild Masai
Giraffe in Serengeti National Park, Tanzania and 96% of feeding was on trees or
shrubs, with Acacia species most frequently consumed during the wet
season. Removal of Acacia leaves
is difficult because most species have thorns (Dagg
& Foster 1976; Pellew 1984) or stinging ants (Dagg & Foster 1976), and giraffes must use their
tongues to remove the tree’s leaves (Dagg &
Foster 1976).
As giraffes have evolved to use their prehensile
tongues to remove leaves from trees, oral stereotypies like non-food object
licking behaviours likely result from a captive
environment that does not provide ample opportunities to satiate this need
(Sato & Takagaki 1991; Kolter 1995; Koene & Visser 1996; Baxter
& Plowman 2001; Fernandez et al. 2008).
Although giraffes rarely exhibit stereotypic behaviours
in the wild (Veasey et al. 1996) other studies of giraffe under human care suggest
that 79.1 % of captive giraffe in surveyed zoos (Bashaw et al. 2001) with
reported prevalence of tongue playing stereotypic behaviours
reached as high as 25% of total observed behaviours (Koene & Visser 1996).
Giraffe are foregut fermenters (Mertens 2007). Captive giraffe are often fed diets too high
in starch and sugars (as are found in sugar-rich produce), and the reduced
fiber could cause explosive fermentation in the foregut, increasing the risk of
occurrence of rumen acidosis among giraffe (EAZA 2006). Rumen acidosis contributes to several
physiological and behavioural problems in captive
giraffes including oral stereotypy (EAZA 2006).
A fully grown giraffe with maintenance requirements (including moderate
locomotion levels) consumes about 8.5–12 kg of dry matter (DM) per day on a
captive diet (1.2–1.3 % of body weight) (EAZA 2006). Lintzenich &
Ward (1997) recommend 60–70 % of forage in diets for giraffes. Hofmann (1973)
classifies the giraffe as browsers.
Browse closely resembles their natural food and food acquisition
patterns. Also, being ruminants, a
considerable proportion of tongue movement occurs during rumination. In captive settings, lack of browse or
opportunities to browse to induce rumination do not promote natural tongue
manipulation and could lead to increase in oral stereotypies (Schaub et al.
2004; Hummel et al. 2006; Duggan et al. 2015).
In zoological institutions, therefore, a major task for giraffe
husbandry is to simulate the feeding and foraging behaviours,
as lack of behavioural foundations representing
natural behavioural ecology can lead to behavioural pathologies (e.g., oral stereotypies or
pacing), and impaired health (e.g., rumen acidosis).
Enclosure space has a profound influence on the behavioural activity budget of the giraffes housed in it
(Garry 2012). Giraffe naturally have a
mean home range size of 282km2 (du Toit 1990) and have been found to
cope well in restricted captive conditions; however, enclosures too restrictive
due to space constraints for group size and density of animals have also been
correlated with increased stereotypic licking in giraffes, okapi, horses (Redbo et al. 1998; Bashaw et al. 2007). The Central Zoo Authority (CZA), Ministry of
Environment and Forests, Government of India prescribes minimum size of outdoor
enclosure of 1,500m2 for housing two giraffes (Bonal
et al. 2014).
This study was conducted with a threefold
objective. Firstly, to examine current behaviour of Northern Giraffes in Zoological Garden
Alipore, Kolkata to advise on their enhanced management. Secondly, to highlight any behavioural abnormalities and recommend enrichment
mechanisms. And lastly, to compare the
observed stereotypic behaviours with behaviour described in other zoological institutions and in
the wild to provide a focal trajectory in the development of guidelines.
Materials and Methods
To characterize stereotypical behaviour
in captive giraffe, behavioural observations were
conducted at the Zoological Garden Alipore, Kolkata, India. The giraffe enclosure housed seven
individuals, consisting of three adult males, two adult females, and two calves
(a male and a female). The outdoor
enclosure was 20m x 20m in width (400m2) (Figure 1), with an indoor
facility that contained the feeding and drinking area. The feeding and drinking area was not
visible during the observation sessions, although the giraffes had open access
day and night to both areas. Therefore,
observations on feeding and drinking behaviour could
not be included in the study.
The food offered to the giraffe at Zoological Garden
Alipore included higher proportions of concentrates and sugar-rich produce (in
the form of fruits and vegetables). No
browse was offered as a part of the diet.
The feed was offered in open feeders and was accessible to all giraffes
equally. The proportion of concentrates
and produce a single giraffe would eat was not estimated. The giraffe were fed twice a day at 08.00 and
15.00 h, making them susceptible to large amounts of starch and sugar loads in
the rumen at any one time.
For the study, four giraffe were selected as a sample
of the herd (Table 1).
The four giraffe representing different ages and
sexes; the dominant male, the subordinate male, a female and the youngest calf
(male), were observed for seven days from 24–31 October 2015, using
instantaneous scan sampling method.
Observations could not be done on Thursday, 29 October 2015 as the zoo
remains closed on Thursdays. Behaviours were recorded
every two minutes during each 30-minute session, three-times a day at 09.00,
13.00 and 17.00 h. A total of 84 observations were recorded, resulting in 1,260
data points.
The behaviours were
categorized into an ethogram of 13 headings based on overall observed behaviour patterns (Table 2).
The average counts into an ethogram across the group
were computed and aggregated into half-hourly blocks of time. To test if the observed levels of oral
stereotypy at Zoological Garden Alipore were different than previously reported
values in the wild and in other zoos, a series of one-sample t-tests were
conducted. To assess if observed prevalence
of stereotypic behaviour was greater than the null
model of 0 in the wild, a series of one-sample t-tests were used comparing the
observed prevalence of stereotypy for each individual’s behavioural
observations to 0 to account for the assumption that giraffe do not exhibit
stereotypic behaviour in the wild (Bashaw et al.
2001). To assess if observed prevalence
of stereotypic behaviour was different than
previously reported studies, a series of one-sample t-test was conducted,
comparing the observed prevalence of stereotypy for each individual’s behavioural observations to 0.25 to account for the
reported prevalence of stereotypic tongue playing reported by Koene & Vissner (1996). To evaluate differences in stereotypic behaviours across age and sex classes over time, a linear
mixed effects model was developed using proportion of time exhibiting
stereotypic behaviour as the response variable.
Age/sex class and time of day time of day were used as the fixed effects and
individual identity as a random effect. To account for proportional data,
arcsine was used to transform the response variable.
Results
Examination of behaviour
Figure 2 represents the behaviours
recorded among all four giraffes during the total observation period at
Zoological Garden Alipore (see Table 1 for identification of individuals).
During the week-long period, the giraffe primarily
exhibited four behaviours: licking stereotypy,
ruminating, walking, and resting more than any other behaviour
recorded. The remainder of the recorded behaviours were observed less than 5% each of the total
time observed.
Behavioural abnormalities (Licking stereotypy)
Licking stereotypy (LS) was observed among the giraffe
accounting for 25% of the total observations, peaking in the evenings
(39%). LS was observed in all four
giraffe, but disproportionally among the individuals. The subordinate male (B2) was recorded 35% of
time engaged in LS, compared to 26% for the calf (C), 20% for female (F) and
19% for the dominant male (B1). All
captive giraffes consistently exhibited significantly higher proportion of
stereotypic behaviour than giraffe in the wild
(Veasey et al. 1996). These findings
were consistent across all individuals of different age and sex classes,
including: B1 (t=3.10, df =20, p<0.01),B2 (t=5.13,
df = 20, p<0.01), C (t= 4.052, df=20,
p<0.01), and F (t=4.07, df=20, p<0.01) (Figure
3). No significant difference was found
in the proportion of observed stereotypic behaviour
and reported values of 0.25 from other zoological collection. This finding was true for all observed
giraffe: B1 (t=-1.04, df= 20, p=0.31), B2 (t=1.42, df=20, p=0.17), C (t = 0.06, df=20,
p=0.95), and F (t= -1.18, df=20, p=0.25).
In evaluating the mixed effects model to test for the
effect of time of day on the proportion of stereotypic behaviour,
a significant effect of time of day on proportion of stereotypic behaviour was found with the highest proportions observed
during evening observation periods.
Although the observed calf displayed an inverse temporal relationship
with the highest proportion of stereotypic behaviours
observed during the morning periods, the temporal effect was strong enough such
that this relationship did not significantly vary across giraffe identity.
Discussion
The daily behaviours of the
group of giraffe studied in this investigation was markedly different than the
daily behaviours of their wild conspecifics. In particular, the amount of time spent
indulging in oral stereotypical behaviours. Oral stereotypy, which was observed highest
among all the behaviours in this study, is
predominantly a giraffe behaviour observed in
captivity as a result of diet, feeding method (foraging), appetitive behaviour, enclosure space, complexity of the environment
and enrichment (Veasey et al. 1996; Mason & Mendl
1997). The giraffes at the zoo were
observed to perform stereotypical non-food object licking behaviours
such as licking the enclosure doors, walls, and fence, which has been
associated as a coping technique for captive animals in suboptimal environments
(Mason 1991). Stereotypic behaviours are reported to have diminishing effects on the
welfare of animals which perform them (Mason & Latham 2004; Mason et al.
2007).
Diet and feeding
Stereotypies in captive herbivores who are fed on
diets largely consisting of concentrated feeds, presented in limited time and
space, are often a result from a lack of opportunity to fulfill their innate
motivation to perform foraging, consumption and digestive behaviour
patterns (Appleby & Lawrence 1987; Terlouw et al.
1991). This in turn is detrimental to
their welfare. The giraffe at Zoological
Garden Alipore were fed higher proportions of sugar-rich produce (commercial
fruits and vegetables) and concentrates, and no browse. Sugar-rich produce contain nutritionally very
fast fermenting sugars and starch and are low in plant fiber. Bergeron et al. (2006) suggests the
hypothesis of occurrence of oral-stereotypic behaviours
in captive ungulates having diets deficient in fiber, stating that the animals
don’t fill their gut and thus are not satisfied. Additionally, these feeds induce little
chewing and hence little saliva production.
In such cases oral stereotypy is suggested to benefit gut health by
generating saliva which helps to rectify gastrointestinal pH (Bergeron et al.
2006). Intake of high proportion of
concentrates can induce a rapid or even ‘explosive’ fermentation in the rumen,
increasing the risk of occurrence rumen acidosis. Rumen acidosis could contribute to several
problems in captive giraffes including oral stereotypy (EAZA 2006). By lowering the concentrations of sugar-rich
produce and increasing the concentration of fiber in giraffe diet, Zoological
Garden Alipore should be able to minimize the observed oral disturbances, and
also a number of health problems associated with unhealthy rumens. It is recommended that the zoo should
restrict sugar-rich produce to very small quantities and special purposes like
training or medication (EAZA 2006). Concentrates should be fed restrictively to
minimize the fermentation effects for overcoming the observed oral stereotypy.
Feeding duration and schedule have been linked to the
performance of stereotypic behaviour (Bashaw et al.
2001). In the wild, higher frequency of feeding behaviour
occurs in the early morning and late afternoon but occurs throughout the day (Fennessy 2004). The
observed giraffe exhibited oral stereotypy throughout the day but increased in
oral stereotypy behaviour in the evening, post
feeding times. The giraffe were offered
meals only twice in a day resulting in peaks of energy intake during feeding
hours. In the wild, however, energy
intake remains distributed over the whole day because of their specialized
feeding ecology. By increasing the
number of meals offered, the energy intake can be prorated throughout the
day. This will, in turn, lower the
incidence of rapid microbial fermentation in the rumen and reduce the
acidosis-induced tongue play, which the giraffe demonstrated through the oral
stereotype behaviour.
It is, therefore, recommended that the giraffe are fed at least three
separate meals daily (EAZA 2006), with fresh browse or lucerne
available at all times to guarantee additional fiber and reduced oral
stereotypic behaviour.
The disproportionately observed LS behaviour
among the individuals can be correlated with the incongruous feeding pattern
adopted by the zoo as they desegregate the amounts of food consumed by
individual giraffe. The giraffe are fed
in feeders equally accessible to the entire herd, and as such, the proportion
of food intake by an individual giraffe could not be measured. Allowing equal access to feeders can also
spur dominant individuals to monopolize the feed stations and consume more. It is, therefore, recommended that the zoo
provide separate feeders for each individual giraffe. This will enable to monitor food and energy
intake by each individual and also prohibit dominant individual(s) from
monopolizing a feed station and consuming too much concentrates or sugar-rich
feed.
The diet of the giraffe lacked provision of browse:
nontoxic, palatable tree branches and trimmings, closely resembling the natural
food of giraffe. In the wild, browsing
requires extensive use of their long prehensile tongues which is difficult to
replicate in captivity if giraffe are fed more food concentrates that are thornless and relatively easy to process. A resultant LS behaviour
was observed as the giraffe had inadequate opportunity for use of their long
prehensile tongues in their natural feeding repertoire (Sato & Takagaki 1991) thus consuming food rapidly. The importance of browse for both the
nutritional value and the behavioural well-being of
animals cannot be overstated and natural browse should be provided to the
greatest possible extent, i.e., 40–60 pounds of browse per individual each day
(Burgess 2004; EAZA 2006; Miller & Fowler 2012). Giraffe are highly efficient in processing
foliage, and as such, browse should not be considered enrichment, but a formal
requirement of their diet. Only browse
that has been approved for use with giraffe should be fed. A well-developed logistics, either by
contacts with the local forestry department, i.e., Department of Forests, Govt.
of West Bengal, or by a browse plantation (Höllerl et
al. 2006) is recommended to ensure year-round supply of sufficient browse for
giraffe at Zoological Garden Alipore.
Enclosure Space
In the wild, large herbivorous species have to walk
long distances between feeding patches (du Toit & Yetman
2005). For giraffe, energy consumptive
activity like walking is strongly biphasic with increased movements occurring
post-dawn/early morning and pre-dusk/early evening, as compared to hottest
period of the day (midday) (Fennessy 2004). Additionally giraffe are the only species to
ruminate whilst walking (du Toit & Yetman
2005). Spatial limitations due to
smaller enclosure caused eradication of the need to walk, and the giraffe were
not observed to: walk, ruminate whilst walking for any long time periods.
It has been proposed that enclosure size influences
the proportion of abnormal behaviour exhibited by confined animals (Maple 1979;
Macedonia 1987; Kirkwood 1998). This
appears very likely given the nature of giraffe movements in the wild who often
have large home ranges (Baxter & Plowman
2001). In captivity, smaller enclosures
limit opportunity to move and exercise due to inadequate space. Reduced opportunity to exercise may lead to
decreased periods of sleep and increased time available for undesirable
behaviour (Bashaw et al. 2001). Also,
enclosures that are restrictive due to too large group size and density can
have a negative impact on the animal’s well-being (Garry 2012). The giraffe in the Zoological Garden Alipore
were housed in a small enclosure space (400m2), far too restrictive
for the group of seven. CZA prescribes
minimum size of outdoor enclosure of 1,500m2 for housing two giraffe
(Bonal et al. 2014), extrapolated to a minimum size
of 5,250m2 which is recommended.
This is a significant difference.
CZA also states that the enclosure for all the species displayed or kept
in a zoo shall be of such size that all animals get adequate space for free
movement and exercise and no animal is unduly dominated or harassed by any
other animal (Bonal et al. 2014). It is, therefore, recommended that Zoological
Garden Alipore should expand the enclosure to meet the guidelines by CZA as a
minimum. Allowing greater access to
exhibit space may also reduce the observed oral stereotypic behaviour and allow
a more natural activity cycle (Forthman 1998).
Enrichment
Providing opportunities for an animal to engage in its
environment is an integral part of the daily husbandry routine, and is as
important to an animal’s care as diet and clean living quarters (Macphee & Mellen 2000). The existing giraffe enclosure at Zoological
Garden Alipore was deficient in environmental complexity, lacking natural
browse, and feeding and behavioural enrichments,
leaving excess free time which giraffe appear to have filled by performing
oral-stereotypic behaviours. In the wild giraffe prefer to rest in
microhabitats, such as under trees within the riparian woodland, allowing shade
and wind to optimise heat loss or gain (Fennessy 2004). In
captive environments, it is presumed that rumination is suppressed when
giraffes cannot rest or relax (EAZA 2006).
It is recommended that Zoological Garden Alipore provides special
resting places in the outdoor enclosure, not too close to visitors or other
busy places, to encourage the giraffe to lay down, rest, and ruminate (EAZA
2006).
In the wild giraffe use their prehensile tongues to
remove small leaves from thorny plants, pluck off pods and flowers. Giraffe at the Zoological Garden Alipore are
only offered food in open feeders and take mouthfuls without much tongue
effort. As a result, their need for a
certain amount of tongue movement was not met and they used their tongues for
movements other than feeding, e.g., non-food stereotype object licking behaviours (EAZA 2006).
Hence food presentation for giraffe in captivity should offer challenges
to display increased tongue movements, encouraging the individuals to elicit
more natural feeding behaviours. As compared to their wild conspecifics in the
wild, the goal for captive giraffe should be to spend up to 60% of their time
engaged in feeding or foraging activities (Fennessy
2004). Therefore, providing enrichment
methods to increase time-engaged feeding for giraffe is strongly
recommended. Closed-topped feeders
(Bashaw et al. 2001) (Image 1), are recommended instead of traditional rack or
trough-style feeders. These feeders
require the giraffe to employ their prehensile tongue in obtaining food and
increase feeding bout duration. Browse
devices like hay racks, browse balls and puzzle feeders (Image 1) are recommended
as they encourage giraffe to use their tongues to pull out the food, increasing
their feeding durations and foraging time (Burgess 2004; EAZA 2006).
These devices are preferably spaced throughout the
enclosure and rotated either on a schedule or randomly to provide more
stimulation for the giraffe. Placing
them at different heights also allows for foraging opportunities for all
giraffe and encourages them to utilise all areas of the enclosure. CZA state that the timing of distribution of
food, placement of food and way of distribution of food to the animals should
be regulated in such a manner that the animals get maximum opportunity to
express natural instincts and skills and behaviour related to feeding (Bonal et al. 2014).
Conclusion
The giraffe in Zoological Garden Alipore, India lack
continuous feeding stimulation and a balanced proportion of forage and
concentrates. The facility lacked
methods to monitor proportions of individual food intake and availability of
browse. The outdoor enclosure did not meet the minimum size prescription
advised by CZA and also lacked any feeding and behavioural
enrichments. The combined effect of
these limitations clearly causes the giraffe to exhibit predominant stereotypic
licking behaviour.
Other impacts on their welfare were not observed in the short study
period but will likely result from the cumulative effects and limitations
described above.
By increasing proportions of fiber in the diet and
using a combination of different forages along with browse, the zoo will be
able to reach the feeding goals for the giraffe. Expanding the outer enclosure to 5,250m2
for the existing herd of seven giraffe can emphatically influence the need for
free movement and exercise. Introducing
enrichment methods to improve the feeding behaviours
(longer and more feeding periods resulting in longer rumination) and positively
changing the animal’s environment would encourage eliciting the animal’s
natural behavioural repertoire to achieve
improvements in the observed oral disturbance pattern.
Table 1. Details of subjects involved in the
observational study at Zoological Garden Alipore, India.
Giraffe |
Identity code |
Age |
Description |
Dominant male |
B1 |
14 years |
Dominant bull and sire of calf (C) |
Subordinate male |
B2 |
13 years |
Second largest bull |
Female |
F |
4 years |
Dam of calf (C) |
Calf |
C |
1.5 months |
Male calf |
Table 2. Giraffe behaviour
categories and descriptions recorded.
|
Behaviour |
Description of behaviours collected |
1 |
Resting |
Subject is standing motionless, eyelids go down or
remain half closed, or is laying on the ground, either neck held up right or
low to the ground |
2 |
Ruminating |
Subject regurgitates food to the mouth and chews it
again while standing motionless, sitting on the ground or moving from one
place to another |
3 |
Self grooming |
Subject is nibbling, licking itself, appearing to
clean itself while in standing position or sitting on the ground |
4 |
Walking |
Subject is moving from one place to another at a
normal walking pace |
5 |
Galloping |
Subject is moving from one place to another in a
three beat gait e.g. canter, faster than a walk |
6 |
Reaching out for food |
Subject in standing or in splaying position is
trying to reach the leaves of trees outside the enclosure by sticking out the
tongue through the gaps of the metal netted fence |
7 |
Sniffing / Tasting soil or grass |
Subject is splaying and sniffing or tasting the
soil, or nibbling grass at the edges inside the enclosure |
8 |
Vigilant |
Subject is observing the visitors or focusing on
visitor activity |
9 |
Interaction with others |
Subject is interacting with another individual e.g.
touching nose, mouth, back, tail, licking / biting mane, bumping rump |
10 |
Licking stereotypy |
Subject is indulging in invariant and repetitive
licking of walls, metal doors, metal fence, etc., along with tongue playing |
11 |
Suckling |
Subject (calf) suckling or trying to suckle the
mother |
12 |
Out of sight |
Subject is inside the indoor facility and not
visible |
13 |
Others |
Any other behaviours that are not listed above |
For
figures & image - - click here
References
Appleby, M.C. & A.B. Lawrence (1987). Food restriction as a cause of stereotypic behaviour in tethered gilts. Animal Science 45:
103–110. https://doi.org/10.1017/S0003356100036680
Bashaw, M.J., L. Tarou, T.
Maki & T. Maple (2001). A survey
assessment of variables related to stereotypy in captive giraffe and okapi. Journal
of Applied Animal Science Behavior 73: 235–247. https://doi.org/10.1016/S0168-1591(01)00137-X
Bashaw, M.J., M.A. Bloomsmith,
L.M. Terry & F.B. Bercovitch (2007). The structure of social relationships among captive
female giraffe (Giraffa camelopardalis).
Journal of Comparative Psychology 121: 46-53. https://doi.org/10.1037/0735-7036.121.1.46
Baxter, E. & A.B. Plowman (2001). The effect of increasing dietary fibre
on feeding rumination and oral stereotypies in captive giraffes (Giraffa camelopardalis).
Animal Welfare 10: 281–290.
Bergeron, R., A.J. Badnell-Waters,
S. Lambton & G. Mason (2006).
Stereotypic Oral Behaviour in Captive Ungulates:
Foraging, Diet and Gastrointestinal Function, pp. 19–57. In: Mason G. & J. Rushen (eds.). Stereotypic Animal Behaviour:
Fundamentals and Applications to Welfare, 2nd Edition. CABI,
Wallingford, 384pp. https://doi.org/10.1079/9780851990040.0019
Bonal, B.S., I. Dhamija, B.R.
Sharma, S.C. Sharma & B.K. Gupta (eds.) (2014). Zoos in India-legislation, policy, guidelines
& strategy, 5th revision. Central Zoo Authority (Statutory Body under
the Ministry of Environment, Forests and Climate Change, Govt. of India),
India, 271pp.
Burgess, A. (eds.). (2004). The Giraffe Husbandry Resource Manual. AZA
Antelope and Giraffe Taxon Advisory Group. Disney’s Animal Kingdom,
Orlando, FL, 184pp.
Dagg, A.I. & J.B. Foster (1976). The Giraffe: Its Biology, Behavior and Ecology.
Van Nostrand Reinhold Company, New York, 210pp.
du Toit, J.T. (1990). Home range-body mass relations: a field study on
African Browsing ruminants. Oecologia 85:
301–303. https://doi.org/10.1007/BF00319416
du Toit, J.T. & C.A. Yetman
(2005). Effects of body size on the
diurnal activity budgets of African browsing ruminants. Oecologia
2: 317–325. https://doi.org/10.1007/s00442-004-1789-7
Duggan, G., C.C. Burn & M. Clauss
(2015). Nocturnal behavior in captive
giraffe (Giraffa camelopardalis)—a
pilot study. Zoo Biology 35: 14–18. https://doi.org/10.1002/zoo.21248
EAZA Giraffe EEPs (2006). EAZA Husbandry and Management Guidelines for Giraffa camelopardalis.
Burgers’ Zoo, Arnhem, 132pp.
Fennessy, J.T. (2004). Ecology of the desert-dwelling giraffe Giraffa camelopardalis angolensis in northwestern Namibia. PhD Thesis.
University of Sydney, Sydney, NSW, Australia, xvi+265pp.
Fennessy, J., T. Bidon, F. Reuss, V. Kumar, P. Elkan, M.A. Nilsson, M. Vamberger, U. Fritz & A. Janke (2016). Multi-locus analyses reveal four giraffe species
instead of one. Current Biology 26: 2543–2549. https://doi.org/10.1016/j.cub.2016.07.036
Fernandez, L.T., M.J. Bashaw, R.L. Sartor, N.R. Bouwens & T.S. Maki (2008). Tongue twisters: feeding enrichment to reduce oral
stereotypy in giraffe (Giraffa camelopardalis). Zoo Biology 27: 200–212. https://doi.org/10.1002/zoo.20180
Forthman, D.L. (1998). Toward optimal care for confined ungulates, pp.
236–261. In: Shepherdson, D.J., J. D. Mellen & M.
Hutchins (eds.). Second Nature: Environmental Enrichment for Captive
Animals. Smithsonian Institution Press, Washington, DC, 376pp.
Garry, S. (2012). Analyses of
captive behaviour and enclosure use in Rothschild’s
giraffes (Giraffa camelopardalis
rothschildi) housed at Paignton
Zoo Environmental Park. The Plymouth Student Scientist 5: 4–30.
Hofmann, R.R. (1973). The ruminant stomach. East African Monographs in
Biology Vol. II. East African Literature Bureau, Nairobi, 354pp.
Höllerl, S., B. Stimm, J. Hummel
& M. Clauss (2006). Browse provision for captive herbivores. Design and
management of a browse plantation, pp. 211–212. In: Andrea, F., M. Clauss, K. Eulenberger, J-M.
Hatt, I. Hume, G. P. J. Janssens & J. Nijboer (eds.). Zoo Animal Nutrition, Vol. 3.
Filander Verlag, Fürth.
Hummel, J., M. Clauss, E.
Baxter, E.J. Flach & K. Johansen (2006). The influence of roughage intake on the occurrence of
oral disturbances in captive giraffids, pp. 235–252. In: Fidgett, A., M. Clauss, K. Eulenberger, J.-M. Hatt, I. Hume,
G Janssens & J. Nijboer (eds.). Zoo Animal
Nutrition Vol. 3. Filander Verlag, Fürth.
Kirkwood, J.K. (1998). Design for the accommodation for wild animals: How do
we know when we have got it right? In: Plowman A.B. & P.M.C. Stevens (eds.).
Proceedings of the 5th International Zoo Design Conference. Paignton,
England.
Koene, P. & E.K. Visser
(1996). Tongue playing behavior in
captive giraffes, pp. 106–111. In: 1st International Symposium on Physiology
and Ethology of Wild and Zoo Animals. Klima, Berlin.
Kolter, L. (1995). Control of behavior and the development of disturbed
behavior patterns, pp. 248–256. In: Ganslosser, U.,
J.K. Hodges & W. Kaumanns W (eds.). Research
and captive propagation. Filander Verlang, Fürth, Germany, 338pp.
Lintzenich, B.A. & A.M. Ward (1997). Hay and pellet ratios: considerations in feeding
ungulates. In: Nutrition Advisory Handbook, Fact Sheet 006.
Macedonia, J.M. (1987). Effects of housing differences upon activity budgets
in captive sifakas (Propithecus verreauxi). Zoo Biology 6: 55–67. https://doi.org/10.1002/zoo.1430060107
MacPhee, M. & J, Mellen
(2000). Framework for planning,
documenting, and evaluating enrichment programs (and the director’s, curator’s,
and keeper’s roles in the process), pp. 221–225. In: AAZPA Annual Conference
Proceedings. American Association of Zoological Parks and Aquariums, Wheeling,
WV.
Maple, T.L. (1979). Great apes in captivity: The good, the bad and the
ugly, pp. 239–273. In: Maple T.L., J. Erwin & G. Mitchell (eds.). Captivity
and behavior: Primates in breeding colonies, laboratories and zoos. Van
Nostrand Reinhold, New York, 286pp.
Mason, G.J. (1991). Stereotypies: a critical review. Animal Behaviour 41: 1015–1037. https://doi.org/10.1016/S0003-3472(05)80640-2
Mason, G.J. & M. Mendl
(1997). Do the stereotypies of pigs,
chickens and mink reflect adaptive species differences in the control of
foraging? Applied Animal Behaviour Science 53:
45–58. https://doi.org/10.1016/S0168-1591(96)01150-1
Mason, G.J. & N. Latham (2004). Can’t stop, won’t stop: is stereotypy a reliable
animal welfare indicator. Animal Welfare 13: 57–69.
Mason, G., R. Clubb, N.
Latham & S. Vickery (2007). Why
and how should we use environmental enrichment to tackle stereotypic behavior? Applied
Animal Behavior Science 102: 163–188. https://doi.org/10.1016/j.applanim.2006.05.041
Mertens, D.R. (2007). Digestibility and intake chapter: 32. In: Barnes,
R.F, C.J. Nelson, K.J. Moore & M. Collins (eds.). Forages, The Science
of Grassland Agriculture, 6th edition, Vol. 2. Blackwell Publishing,
U.K., 808pp.
Miller, R.E. & M.E. Fowler (eds.) (2012). Fowler’s Zoo and Wild Animal Medicine, Volumes 6,
7 & 8. Saunders, USA, 688pp. https://doi.org/10.1016/C2009-0-63976-3
Pellew, R.A. (1984). The feeding ecology of a selective browser, the giraffe
(Giraffa camelopardalis
tippelskirchi). Journal of Zoology 202:
57–81. https://doi.org/10.1111/j.1469-7998.1984.tb04288.x
Redbo, I., P. Redbo-Torstensson,
F.O. Odberg, A. Hedendahl
& J. Holm (1998). Factors
affecting behavioral disturbances in racehorses. Animal Science 66:
475–48. https://doi.org/10.1017/S1357729800009644
Sato, S. & I. Takagaki
(1991). Tongue-playing in captive
giraffe, pp. 22–29. In: 22nd International Ethological Conference.
Kyoto: Otani University.
Schaub, D., M. Clauss, E.J. Flach, H.R. Wettstein, C. Tack
& J.-M. Hatt (2004). Influence of physical and chemical composition of
diet on oral stereotypies in captive giraffes (Giraffa
camelopardalis). Proceedings of the European
Association of Zoo and Wildlife Veterinarians 5: 27–28. https://doi.org/10.5167/uzh-3550
Terlouw E.M.C., A.B. Lawrence & A.W. Illius
(1991). Influences of feeding level and
physical restriction on the development of stereotypies in sows. Animal Behaviour 42: 981–991. https://doi.org/10.1016/S0003-3472(05)80151-4
Veasey, J.S., N.K. Waran
& R.J. Young (1996). On comparing
the behaviour of zoo housed animals with their wild
conspecifics as a welfare indicator, using the Giraffe (Giraffa
camelopardalis) as a model. Animal Welfare
5: 139–153.
Winter, S., J. Fennessy
& A. Janke (2018). Limited introgression
supports division of giraffe into four species. Ecology and Evolution 8:
10156–10165. https://doi.org/10.1002/ece3.4490