The effects of captivity on the behaviour of Aonyx cinerea

in five British institutions

By
Varvara Vladimirova

Submitted as part requirement for the Degree of MSc (Hons) Animal Welfare and
Conservation, Writtle College and the University of Essex. September-2014.
Abstract

Asian small clawed otter (Aonyx cinerea) population is declining in the wild and they
are listed as “Vulnerable” on the IUCN Red List. In addition, there is very limited
information about their behaviour, both in captivity and in the wild. The main goal of
this research was to observe and compare captive groups of small-clawed otters in
five British zoos focusing on time budget, activity patterns, enclosure use, and effects
of visitors and feeding. At the same time, the study focused on the prevalence of
abnormal behaviours. The hypotheses of this study were that time budget and
enclosure use would vary between the institutions due to the variety of enclosure
sizes and enrichment availability. Visitors would have a positive effect on otters and
public feeding would result in increased frequency of begging and activity. There
were clear differences between the institutions in this study which suggests that
enclosure size and design, visitors and predictable schedules play a major role in the
behaviour of otters. Activity levels were significantly different between the institutions
(p<0.001). Natural behaviours such as foraging, grooming, social play and
enrichment related activities were very low in all of the institutions. Results of
enclosure use showed that water use was the lowest in the zoo with the smallest
pool size, as expected. In almost all of the institutions, the use of ‘hideout’ was very
high in comparison to the use of “close to visitors”. High activity behaviour was
directly related to the number of visitors in all of the institutions. There were
significantly higher anticipatory behaviours before feeding than after in almost all of
the institutions. It is well known that visitors play an important role in zoological
institutions; however, it is also important to remember that animal welfare is very
important, especially when dealing with animals that require conservation such as
Asian small clawed otters. Therefore, institutions should improve animal welfare by
minimizing predictable events, providing their animals with plenty of shelters,
enrichment and vegetation to promote species-specific behaviour and reduce
undesirable ones.

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 Contents
Abstract.......................................................................................................................i

List of Tables............................................................................................................ iv

List of Figures...........................................................................................................iv

Acknowledgments.....................................................................................................1

1 Introduction.........................................................................................................2

1.1 Threats to the otter population.............................................................................3

1.2 Otters in captivity.................................................................................................3
1.3 Challenges of captive environment......................................................................4
1.3.1 Abnormal and stereotypic behaviours..........................................................5
1.3.2 Predictable schedules..................................................................................6
1.3.3 Visitor effect..................................................................................................9
1.3.4 Limitations of captive environment.............................................................11
1.3.5 Maintaining captive population...................................................................12
1.4 Time budget.......................................................................................................13
1.5 Enclosure use....................................................................................................14
1.6 Enrichment........................................................................................................ 16
1.7 Objectives and aims.......................................................................................... 17

2 Materials and Methods......................................................................................18

2.1 Data collection...................................................................................................18

2.2 Animals and housing......................................................................................... 18
2.3 Behaviour measurement....................................................................................19
2.4 Time budget.......................................................................................................22
2.5 Enclosure use....................................................................................................22
2.6 Visitor analysis...................................................................................................22
2.7 Feeding............................................................................................................. 22
2.8 Data analysis.....................................................................................................23

3 Results.................................................................................................................. 24

3.1 Time budget.......................................................................................................24

3.2 Enclosure use....................................................................................................25
3.3 Visitor analysis...................................................................................................26

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 3.4 Feeding............................................................................................................. 27

4 Discussion.........................................................................................................30

4.1 Time budget.......................................................................................................30

4.2 Enclosure use....................................................................................................34
4.3 Visitors...............................................................................................................36
4.4 Feeding time......................................................................................................38
4.5 Study limitations.................................................................................................40
4.6 Recommendations.............................................................................................40

5 Conclusion...........................................................................................................42

6 References............................................................................................................ 44

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 List of Tables
Table 1. Summary of otter population, enclosure size and feeding times in five zoos in UK..............................19

Table 2. Summary of the focal otters................................................................................................................ 20

Table 3. Analysed behaviours for otters in institutions......................................................................................21

Table 4. Mean activity budget as a percentage of visible time for groups of Asian small clawed otters in

five zoos............................................................................................................................................. 25

Table 5. Mean percentage of time spent engaged in behaviours as a function of crowd size............................27

List of Figures
Figure 1 Mean enclosure use as a percentage of visible time for groups of Asian small clawed otters in five zoos...............26

Figure 2 Percentage and standard deviation of low activity observed in otters in five institutions before and after

feeding.................................................................................................................................................................. 28

Figure 3 Percentage and standard deviation of anticipatory behaviour observed in otters in five institutions before

and after feeding.................................................................................................................................................... 29

iv
Acknowledgments

I would like to thank my supervisor Dr. Jonathan Amory for his help and advice
throughout my dissertation. I have learnt a great deal from him. I sincerely thank the
curators, keepers and research staff of Colchester zoo, London zoo, Chessington
Park, Battersea Park and WWT London Wetland Centre for their generous
cooperation and assistance during the study. I also want to express my gratitude to
Jason Palmer - the Animal Collection Manager and IUCN Otter Specialist Group
member, Nicky Needham - Programmes and Policy Coordinator BIAZA, Sarah
Duncan - International Studbook keeper for ASC otters and Jan Reed-Smith -
IUCN/SSC Otter Specialist Group member for their assistance and helpful advice.
Also, I would like to thank my husband Dr. Miguel Martinez for his support.

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 1 Introduction

Asian small clawed otters (Aonyx cinerea) are carnivores from the family Mustelidae
(Hussain et al., 2011). This species is native to almost all of the Southern and
Southeast Asian areas including Philippines, Indonesia, southern China, Bangladesh,
Bhutan and Nepal (Lombardi et al., 1998). They are the smallest of the 13 otter
species (Foster-Turley and Santiapillai, 1990) and one of the five otter species found
in Asia (Reed-Smith et al., 2009), often sharing their habitat with smooth-coated and
Eurasian otters (Hussain and de Silva, 2008). Small clawed otters were reported to
thrive in lower montane evergreen forests, peat swamp, freshwater wetlands,
freshwater swamp forests and coastal wetlands and mangroves (Roberton, 2007).
Studies also show that otters do not like open areas that do not offer shelter (Melisch
et al., 1996) and that they prefer moderate to low vegetation in riparian systems
(Hussain and de Silva, 2008). Being semi-aquatic animals, they forage in water but
breed and spend a lot of time on land (Larivière, 2003; Hussain et al., 2011). They
mainly feed on crabs, snails and other molluscs, as well as insects and small fish
(Wayre, 1978). Occasionally, they hunt rodents, snakes and amphibians (Hussain
and de Silva, 2008). Small clawed otters are apex predators and they play an
important role in the revival of indigenous animals by controlling invasive species
(Ben-David et al., 1998; Parker et al., 2005). Moreover, their presence and behaviour
can be used as an indicator of the pollution in aquatic habitats since they are very
sensible to water quality (Melisch et al., 1996; Perdue et al., 2013).

Otters are very social, vocal and intelligent animals (Larivière, 2003; Heap et al.,
2008). They usually form groups of up to 12 individuals in the wild, with only the
dominant pair breeding (Foster-Turley and Engfer, 1988). Otters always sleep in
close connection with the group (Foster-Turley, 1978). Unlike other otter species,
small clawed otters form monogamous bonds, mating for life and both parents take
part in rearing the young (Perdue et al., 2013). In addition, older siblings are involved
in raising the younger ones (Foster-Turley, 1990). Most research related to the social
behaviour of small clawed otters has been carried out in captivity, where they were
observed to have a very strong pair bond (Hussain et al., 2011). However, there is
little known about their intragroup social networks (Lemasson et al., 2014).

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There is a contradiction on when these animals are most active. They were reported
to be nocturnal and crepuscular in areas close to people in northern Malaysia and
India (Hussain et al., 2011), but diurnal in other parts (Heap et al., 2008; Larivière,
2003).

1.1 Threats to the otter population

Small clawed otter population is declining in the wild and they are listed as
“Vulnerable” on the IUCN Red List (IUCN, 2011). Human activities have a major
effect on the decline of small clawed otters and its conspecifics: smooth-coated and
Eurasian otters (Hussain and de Silva, 2008; Hussain et al., 2011).

The habitat of the small clawed otters is being destroyed as a result of the
development of aquaculture causing loss of mangroves, increased use of pesticides
which pollutes streams, and other human activities such as deforestation and tea and
coffee plantations (Hawke et al., 2000; Hussain and de Silva, 2008). Another
important threat to otter population is the reduction of the prey biomass such as fish
(Dehadrai and Ponniah, 1997). Illegal trade is the next important threat to the
species. Otters are killed for the medicinal value of their organs and for their pelts
(Hussain et al., 2011). The otter population has declined prominently in the western
range causing them to move from west to east (Hussain and de Silva, 2008). Otters
became extinct in parts where they were once common such as mangroves of east
Calcutta and Sunderbans (Sanyal, 1988). This population reduction has been
observed in many parts of its range and, although there is insufficient data, it was
estimated that in the last 60 years its range has been shrunk considerably (Melisch et
al., 1996; Hussain, 2002; Hussain and de Silva, 2008).

1.2 Otters in captivity

Small clawed otters are now part of the Species Survival Plan (SSP) programme
which is managing viable captive otter populations and assists in conservation of the
species in the wild (Foster-Turley and Engfer, 1988). Other benefits of keeping wild
small clawed otters in captivity include research and public education. Research of

3
captive otter population provides useful information about their behaviour and
cognitive abilities (Perdue et al., 2013). Potentially, it could also improve our
knowledge of them in the wild where they are hard to study, as they live in hard to
reach habitats (Kruuk, 1995). Public education supports survival and breeding for
possible reintroduction into the wild (Foster-Turley and Santiapillai, 1990).

Maintaining a self-sustaining viable captive population is important. Small clawed

otters are common in the UK in zoological institutions with more than 40 animals
(Wright, 2003). Otters were reported to live up to 20 years in captivity (Perdue et al.,
2013) and from 12 to 18 years in the wild (Partridge and Jordan, 1995).

1.3 Challenges of captive environment

The main goals of the modern zoos are to maintain viable captive population, to
research, to raise awareness by educating the public and to support the declining
population in the wild (Kirkwood, 2003; Anderson et al., 2003). However, these goals
are not always fulfilled. There have been reports of abnormal behaviours exhibited in
small clawed otter which affects their welfare (Ross, 2002). Limited research has
been carried out on time budget, enclosure use, social behaviour and ecology of
Asian small-clawed otters in captivity (Foster-Turley and Santiapillai, 1990) and
almost none in the wild (Reed-Smith et al., 2009). Therefore there is not enough
knowledge on how well these species are thriving in captivity. There is information,
however, on other otter species, but their behaviour deviates from small clawed
otters, thus, we can use the knowledge of other otter species as guidance.

When researching the effects of captivity on otters, other captive animals can be
used as models. The maintenance of a wild animal in captivity is expensive and
requires adequate knowledge to tend to the needs of each species (Reed-Smith et
al., 2009). The main issues raised by keeping animals in captivity, leading to welfare
problems and expression of abnormal behaviour, are the limitation of captive
environment (Fernandez et al., 2009; Mason et al., 2010; Szokalski et al., 2012), the
visitor effect (Sellinger and Ha, 2005; Quadros et al., 2014), a predictable schedule

4
(Gilbert–Norton et al., 2009; Hsu et al., 2010; Galhardo et al., 2011) and the
maintenance of the animal population (Mason et al., 2007).

1.3.1 Abnormal and stereotypic behaviours

Abnormal behaviours, including stereotypic behaviours, are a growing concern due to

their negative implications on otters and other captive animals (Mason, 1991; Hawke
et al., 2000; Mohapatra et al., 2010; Vandellest et al., 2011; Svendsen et al., 2013).
For example, it has been reported that 90-100% of captive singly housed macaques
have some form of abnormal behaviour (Camus et al., 2013). Abnormal behaviour is
usually defined as any behaviour which would not be performed by animals in the
wild. Stereotypic behaviour is defined as a repetitive behaviour which could occur in
the wild but the frequency of this behaviour is higher in captive animals (Hawke et al.,
2000). These behaviours develop in animals where the captive environment is not
suitable for them to carry out their natural or instinctive behaviours (Carlstead, 1996).
Abnormal behaviours are usually functionless and it is commonly known that animals
usually express them as a way of coping with a stressor such as impoverished
environment, boredom or unhappiness (Dawkins, 1998; Reed-Smith, 2012). Thus, it
is a good indicator of a sub-optimal welfare of an animal (Dallaire et al., 2012).

Otters have been reported to express abnormal behaviours such as neck twisting,
overgrooming, hair plucking, pacing and other forms of anticipatory behaviours
(Hawke et al., 2000; Ross, 2002) but only few have been investigated. These
behaviours were also reported in other animals such as bears (Tan et al., 2013;
Mattiello et al., 2014), tapirs (White et al., 2003), big cats (Mohapatra et al., 2014),
primates (Tarou et al., 2005) and other mammals (Chellender et al., 2012; Mononen
et al., 2012). This information can be used to improve our knowledge of these
behaviours in otters. Neck twisting is defined as unnatural twisting and rolling of the
neck during locomotion (Vickery and Mason, 2004; Gothard, 2007). It was reported in
llamas, bears and some primates (Beisner and Isbell, 2009; Hosey et al., 2013) and
sometimes is referred to as a head throw (Tan et al., 2013). There is not enough
information on what triggers this behaviour in captive animals and how to eliminate it.
Other abnormal behaviours in otters are overgrooming and hair or fur plucking.

5
Indicators separating overgrooming from grooming include areas of missing or
thinning hair (Hosey, 2005). It was shown to be triggered by stress from a lack of
foraging and aggressive inmates (Tarou et al., 2005). There are two types of hair
plucking: social-plucking and auto-plucking. The former is defined as individual
roughly pulling at hair of conspecific, whereas the latter occurs when an individual is
roughly pulling hair from own body (Ross, 2002). Grooming and plucking hair were
observed in mammals and birds due to the inability to satisfy their foraging needs
and, therefore, redirect their energy on other behaviours (Boccia and Hijazi, 1998;
Meehan et al., 2003; Beisner and Isbell, 2009). Research has shown that it is
possible to reduce these behaviours by additional enrichment (Ross, 2002; Shyne,
2006).

Stereotypic behaviours are almost impossible to abolish once acquired (Mason et al.,
2007; Novak et al., 2012). The only recent study on reduction of abnormal behaviour
in otters was focused on hair-plucking. Early studies also suggested to change the
social structure when hair plucking, fighting, pacing or avoidance behaviours were
present (Lombardi et al., 1998). It is apparent that housing with conspecifics is the
most effective way of reducing abnormal behaviour (Bourgeois and Brent, 2005;
Gilbert and Baker, 2011). In addition, foraging and grooming devices, as well as
increased enclosure space and toys were observed to reduce abnormal behaviour in
captive animals (Kaufman et al., 2004). The effect of these enrichments varies
between species (Kaufman et al., 2004; Rommeck et al., 2009), and the intensity of
abnormal behaviours was reported to depend on the gender. For example male
primates exhibit more of abnormal behaviour than females (Novak et al., 2002;
Corrine et al., 2014).

1.3.2 Predictable schedules

Important daily events such as feeding are highly scheduled and predictable; causing
anticipation in many captive animals, nonetheless, there are few studies on
occurrence and significance of anticipatory behaviour in zoos (Jensen et al., 2013;
Watters, 2014). Animals might not be visible during the opening times of the zoo, and
visitors can become unhappy if they cannot see the animal. Therefore, events such

6
as public feeding ensure that the animal will be visible. However, this often has
negative effects on the animal welfare (Hsu et al., 2010; Galhardo et al., 2011).

Anticipatory behaviour is defined as “a response elicited by stimuli that leads to and

facilitate consummatory behaviour” (Spruijt et al., 2001). This behaviour has been
reported in many species and varies between them (Bassett and Buchanan–Smith,
2007; Gilbert–Norton et al., 2009; Hsu et al., 2010; Galhardo et al., 2011).
Anticipatory behavior is usually expressed as an increase in high activity prior to an
event (Mason et al., 2007; Feeney et al., 2011). Other studies show that anticipation
usually results in increased abnormal behaviour and decreased activity as animals
are waiting for food (Bassett and Buchanan-Smith, 2007). On the other hand, studies
emphasize that anticipatory behaviours can promote heightened welfare and can be
a positive event for an animal such as increasing attentiveness and activity of the
animal (Jensen et al., 2013).

One of the types of anticipatory behaviour is feeding anticipation. It commonly

appears in animals when the feeding schedule is predictable, resulting in stereotypic
and abnormal behaviours (Bassett and Buchanan-Smith, 2007; Hansen and M∅ ller,
2008). In small clawed otters, anticipatory behaviours are expressed in a form of door
manipulation, pacing and begging (Hawke et al., 2000; Ross, 2002). These
behaviours were also observed in studies of other captive animals, and this
knowledge can assist in improving otter welfare.

Pacing is the most common stereotypic behaviour reported in many species (Shyne,
2006) and it is defined as repeated walking movements in same path (Mason, 1991).
It was observed in animals when the feeding routine is fixed. For this reason,
researchers suggested randomising feeding times (Dierenfield et al., 1994;
Mohapatra et al., 2014). In addition, pacing was expressed in anticipation of food and
due to lack of foraging devices, or when feeding was postponed (Shyne, 2006;
Svendsen et al., 2013; Mohapatra et al., 2014). A common way of reducing this
behaviour is to provide animals with additional foraging enrichment (Ross, 2002;
Jenny and Schmid, 2002). Working for food was shown to reduce the expression of
these behaviours in captive animals, including otters. For example, Hawke et al.
(2000) managed to reduce pacing by randomising the feeding time and placing food

7
with the use of a catapult, therefore, the feeding time was unpredictable for them and
they did not depend on keepers for food. Randomising feeding time is not always a
solution since one of the goals of the zoo is to satisfy visitors and fixed feeding times
allow for animals to be visible. To avoid this problem in big cats, instead of food they
are given enrichment in a form of spices, such as cinnamon, chilli powder and cumin.
This enrichment was shown to not only decrease abnormal behaviour, but also to
increased activity levels (Skibiel et al., 2007). It was already suggested to use this
type of enrichment for otters (Reed-Smith, 2001), yet it is not widely used. Other type
of foraging enrichment is timer-controlled feeding boxes which were also shown to
reduce stereotypic pacing in tigers (Jenny and Schmid, 2002).

Another common type of anticipatory behaviour in otters is begging, also known as

food soliciting, which is defined as barking for food and a ritualised form of bipedal
observing behaviour (Butler, 1994). It is expressed in animals towards staff and
members of public during and immediately after feeding in anticipation of food
(Maslanka and Crissey, 2002; Gothard, 2007). Begging and calling prior to feeding
time is considered to be an unnatural and abnormal behaviour in captive otters (Heap
et al., 2008). It was reported in many animals, mainly primates, when feeding time or
the interval between the feeding times was predictable (Kistler et al., 2009; Choo et
al., 2011; Tan et al., 2013). In otters and some other animals, it was also suggested
to occur as a result of hunger (Lyons et al., 1997; Gothard, 2007; Watters, 2014).
Therefore, it is important to fulfil the feeding requirement for otters which is 25% of
their body weight of food per day (Foster-Turley, 1978). In addition, the metabolic
rate of otters is very high, causing the food to be digested within an hour (Hawke et
al., 2000). As a result otters were shown to beg when the feeding frequency is below
the recommended which is 3 to 4 times a day (Heap et al., 2008). In the wild, sea
otters increase foraging when there is a decline in food quantity and quality (Krebs,
1978). However, since otters in captivity often associate food with keepers their
response to food deprivation would be begging or fossicking. Fossicking is a
searching behaviour exhibited in otters as a result of frustration of being subjected to
an arbitrary feeding routine and inability to forage for their own food (Mellowship,
1990).

8
Studies report that animals often express other behaviours prior to a predictable
event. For example, door manipulation was reported to occur in otters as well as
other captive animals, but only few studies have investigated it (Ross, 2002). Animals
were also shown to change the enclosure usage an hour prior to feeding. They were
shown to move either to the location of the food delivery before the feeding time or
spend time in a certain part of the enclosure prior to other events such as public
shows (Jensen et al., 2013; Gilbert–Norton et al., 2009).

1.3.3 Visitor effect

As mentioned before, one of the main goals of the zoos is to enhance the visitor
experience by providing them with the opportunity to get in close contact with animals
and thus increasing their contribution to conservation (Clayton et al., 2008; Sherwen
et al., 2014). Visitors prefer to see active animals expressing species-specific
behaviours (Wolf and Tymitz, 1980; Anderson et al., 2003), and otters have a high
exhibition value due to their fascinating land behaviours (Duplaix-Hall, 1972).
However, visitors were often shown to have a negative effect on the behaviour of
many captive animals (Hosey, 2000; Hosey, 2005; Sellinger and Ha, 2005; Quadros
et al., 2014) and it is important to consider animal’s welfare as well as visitor
satisfaction. The effect of visitors on otter behaviour is not well studied; however,
there is extensive material on the effect of visitors in other captive animals. Previous
studies have shown that the size of visitor crowds, volume of sound made and level
of interaction with the animals have a negative effect on animal behaviour (Davey,
2007; Choo et al., 2011). Large crowds can result in increased aggressive behaviour
both towards conspecifics and visitors (Fernandez et al., 2009; Rajagopal et al.,
2011; Sherwen et al., 2014), cause stress (Hosey, 2000; Menargues et al., 2013;
Sherwen et al., 2014), reduce affiliative behaviour such as social play (Jones, 2003;
Hosey, 2008), increase abnormal behaviour (Mallapur et al., 2005; Sellinger and Ha,
2005; Carder and Semple, 2008) and increase vigilance and social negative
behaviours (Davey, 2007). High visitor numbers were also shown to lead to changes
in enclosure use and to reduce the time spent visible to the public (Sellinger and Ha,
2005; Todd et al., 2007; Quadros et al., 2014). Loud ambient noise levels can also
affect the behaviour of captive animals resulting in increased locomotion,

9
vocalisations, avoidance and stress (Birke, 2002; Owen et al., 2004; Choo et al.,
2011). Visitors often attempt to interact with animals which results in increased
aggression, begging and even a display of threats at visitors (Hosey and Druck,
1987; Chamove et al., 1988; Gothard, 2007). When measuring stress levels in
animals it is important to measure hormone levels as well as behaviour due to the
fact that some animals may be stressful without performing any changes in
behaviour. For example, studies illustrate that felids do not show any changes in
behaviour with visitor presence; however, they display physiological stress
(Montanha et al., 2009; Fanson and Wielebnowski, 2013). Begging often occurs in
animals which are fed by the public (Tan et al., 2013, Gothard, 2007). The
expression of all these behaviours in animals can have a negative impact on their
welfare and the visitor experience (Sherwen et al., 2014).

Existing information suggests that visitors do not always have a negative effect on
captive animals. They can also have neutral and even enriching effect on the
behaviour of captive animals and are thought to be a source of stimulation for them
(Margulis et al., 2003; Davey, 2006; Sherwen et al., 2014). The effect of visitors on
the behaviour of animals usually depends on the species and the majority of studies
have focused on captive primates (Fernandez et al., 2009; Sherwen et al., 2014).
The way the animals perceive visitors can be a reason for the differences in
behaviours towards them. For example, apes share visual gestures with humans and
they can perceive some of them as threats. For instance, a human smile can
resemble aggressive bared-teeth display in social primates (Parr and Waller, 2006).
It may also be suggested that prey would be expressing visitor avoidance behaviour
more often than predators because it is natural for them to avoid being captured in
the wild (Mason, 2010). Therefore, the effect that visitors have on the animals is
species specific. Recent studies also suggest that gender can also play a role in
visitor effect on the behaviour. For example, male gorillas increased aggressive
behaviour with higher visitor number, whilst females did not alter their behaviour
(Stoinski et al., 2012).

There are few recent studies testing effect of visitors on the behaviour of otters.
In one of the studies they were shown to increase play, foraging and begging
towards the visitors which were identified as positive by the authors (Owen et al.,

10
2004). On the other hand, another study found no effect of visitors on the behaviour
of otters (Gothard, 2007). Although otters usually thrive near human-dominated
areas, they tend to avoid human presence (Rosas et al., 2007). Therefore, further
research is required to investigate whether otters express negative or positive
behaviour with presence of visitors, or if there is no effect. Regardless of the visitor
effect on the animals, it is important that animals have a shelter from them.
Guidelines for an otter enclosure stated that they require a place to hide from the
public view when desired and that the long-term noise should be avoided (Heap et
al., 2008; Reed-Smith et al., 2009).

1.3.4 Limitations of captive environment

Animal movements are not restricted in the wild and the range of their habitat is often
much larger than the habitat provided for them in captivity. Limitations of a captive
environment usually lead to stereotypic behaviour, aggression and a reduction of
natural species-specific behaviours in many species (Fernandez et al., 2009; Ross et
al., 2009; Mason et al., 2010; Szokalski et al., 2012).

The size of the enclosure is a pivotal factor that affects animal behaviour. For
example, increased grooming was observed in baboons when transferred to a bigger
enclosure (Bartolini and Bicca-Marques, 2011). The area and resources provided are
suggested to be sufficient enough for the animal if the animal is not displaying any
unnatural behaviour (Rose and Robert, 2013). Stereotypic behaviour can be reduced
by transferring animal to a more enriched and larger enclosure ( Dallaire et al., 2012).
Animals that occupy large home ranges in the wild are affected the most by captivity
and are more likely to exhibit abnormal behaviours and have welfare problems
(Clubb and Mason, 2007), however, contradictory results have been reported. For
example, wild cats were shown to be more active and paced less in larger enclosures
(White et al., 2003; Bashaw et al., 2007), whilst, other research shows that pacing did
not differ depending on the size of the enclosure (Lyons et al., 1997). As mentioned
before, additional enrichment is usually beneficial for the otters; however, few studies
show the effect of the enclosure size on their behaviour. Early studies show that
constant bouts of bouncing behaviour interspersed with a single non repetitive pace

11
or run along the edge of the enclosure are behaviours expressed in otters when the
enclosure is too small (Mellowship, 1990). The size of the enclosure is a very
important factor for the Asian small clawed otters. They should have ample room to
swim, play, explore, and dive into water in captivity (Sarah Duncan, personal
knowledge). The recommended minimum size of the otter enclosure is 60 m2 for a
pair of otters, with additional 5 m2 per otter (Heap et al., 2008). Although there is no
record of the home range of small clawed otters in the wild, the home range of sea
otters was reported to be up to 45 km2 (Bowyer et al., 1995).

1.3.5 Maintaining captive population

As mentioned previously, one of the main goals of zoological parks is to maintain

captive populations of species which are declining in the wild. To fulfil this goal it is
important to maintain stable, genetically diverse population in captivity which would
allow to reintroduce it into the wild when necessary (Flesness and Foose, 1990;
Mench and Kreger, 1996). There are issues associated with fulfilling this goal. For
example, since the population of captive animals is usually small, it does not
represent the genetic diversity in the wild, and thus, captive animals evolve captive-
adapted strains (Mason et al., 2007). Another problem is the difficulty to maintain
reproduction levels. Some species thrive in captivity whilst others have difficulties to
reproduce, exhibiting behavioural problems (Clubb and Mason, 2003). An early study
reported otters to have a very low reproduction success in the UK (Timmis, 1971).
Jason Palmer (personal knowledge), the Animal Collection Manager and IUCN Otter
Specialist Group member, stated that Asian small clawed otters are not hard to
maintain or breed in captivity and that the UK has had many years of good
successful breeding groups. He did, however, suggest that at present it is better not
to breed captive small clawed otters, since their population is captivity in UK is
extremely inbred.

12
1.4 Time budget

It is important to take into account time budgets of the wild animals when designing
an enclosure for them as it will allow to decide the right furnishing and size giving the
animal the best possible quality (Ross et al., 2009). Analysing the complexity of
different environments can assist in providing otters with appropriate environmental
enrichment which can encourage natural behaviour (Cummings et al., 2007). Time
budget can function as a welfare assessment because welfare is determined by the
levels of activity, aggression, sleep and undesirable behaviours (Squires, 2003). An
enclosure that allows animals to express more species-specific behaviours is
enriching for the animal and provides a better experience for the visitors (Fabregas et
al., 2012).

There are only few studies on the activity patterns of otters in captivity (Lekagul and
McNeely, 1988; Gothard, 2007). However, the observations were composed of sole
collections in individual zoos. A meta-analysis of the time budget in several captive
premises is required to form more representative conclusions. Information about the
time budget of otters in the wild could assist in determining whether animal welfare in
captivity is acceptable. Studies of wild otters show that they are active and inquisitive
animals which like to dig, root around, exercise and play (Heap et al., 2008; Reed-
Smith et al., 2009). Therefore, it is important to have plenty of enrichment to stimulate
such behaviours as playing and foraging (Heap et al., 2008). Early studies show that
wild otters spend roughly the same time awake and asleep (Stephens, 1954; Pellis,
1984). In addition, they spend a large proportion of their day playing. In particular,
play fighting is considered to be a very important activity in small clawed otters
(Patridge, 1991). There is no information on the percentage of resting and swimming
of these species in the wild but grouped information of sea otters, a closely related
species, shows that resting ranges from 27 to 62% and swimming from 3 to 26% of
the time budget (Finerty et al., 2009). To promote the natural behaviour of such
active animals as otters, the enclosure should be filled with enrichment such as
hollow logs, tree stumps, bushes, saplings and most importantly areas of sand,
gravel and grass for grooming (Patridge, 1991).

13
The main issue, when assessing the activity level of any animal in captivity is low
foraging. Captive animals usually do not spend as much time on feeding and foraging
as they would have in the wild because they are mostly fed processed food that does
not require natural foraging tactics or energy expenditure (Watts, 1988; Bond and
Linburg, 1990; Weller and Bennett, 2001). Existing data shows that small clawed
otters spent from 40 to 60% of time foraging in the wild (Lombardi, 2002). Studies on
sea otters also show that they tend to forage more when their population in the area
is higher (Estes et al., 1981). It is important to compare the percentage of foraging in
captive and wild otters because low levels of foraging can lead to unoccupied time,
potentially causing boredom, inactivity and abnormal behaviour (Gothard, 2007).
These behaviours are undesirable for both animal welfare and visitor interest.

1.5 Enclosure use

Studies of enclosure use in animals are necessary to determine the perfect design of
captive environment that matches the biological requirements of the animals and
assures their welfare (Ross et al., 2009). The design of the enclosure has to meet
both the requirements of the species and to educate and entertain the public
(Anderson et al., 2003). In addition, the enclosure has to allow animals to express a
broad range of naturally occurring behaviours. Studies of enclosure use allow us to
learn more about species preferences. For example, research observed that
chimpanzees preferred corners, which led the authors of the study to suggest that
corners share characteristics of closely spaced barriers such as trees, bushes and
rocks and therefore, are preferred by chimpanzees (Ross et al., 2009). Studying
enclosure use can also indicate which parts of the enclosure require changes. For
instance, in a study of captive sitatunga, they spend 54% of the time in 28% of the
enclosure (Rose and Robert, 2013). This suggests that the rest 72% of the enclosure
required improvement. The authors found that sitatunga spend a lot of time in long-
grass beds as they do in the wild where they hide from predators and high
temperatures. For this reason, it was suggested to add long-grass beds to the
remaining 72% of the enclosure. Other cases show that sometimes the design of the
enclosure can have a negative effect on animals. For example, some artificial
enrichment can cause in stress and discomfort to the animal and have potential

14
negative effect on its welfare and behaviour (Morgan and Tromborg, 2007). Thus,
social and biological factors, as well as environmental preferences influence the
space use of animals (Ross et al., 2009).

There are only few studies on the enclosure use in small clawed otters (Reed-Smith
et al., 2009). Measuring how they utilise the space provided would allow us to identify
positive and negative aspects of their environments and whether the habitat is used
efficiently (Ross et al., 2009). When designing an enclosure for any captive animal,
large and complex exhibits are always preferred because they reduce stress in
animals allowing them to express species-specific behaviours and control the level of
interaction with visitors (Choo et al., 2011). Suggestions on the design of the otter
enclosure are that otters have to be given a choice of substrate, temperature, food
gathering, nesting and marking territories (King et al., 2005). Similarly to other otter
species, Asian small clawed otters do not like bare and open areas that do not offer
any shelter (Melisch et al., 1996). Otters are active animals and like to manipulate
objects. For this reason, the important elements of a complex and successful otter
exhibit should include a large variety of enrichment including a choice of large and
small rocks, fake logs, removable water plants, crevices to hide their food, trees, tree
roots, stumps, grasses, boulders, dens, caves, climbing structures, bushes, deadfall,
waterfalls, floating log piles, rafts, islands and a variety of substrates (Reed-Smith et
al., 2009). It is possible to identify what type of habitat they prefer using otter
spraints, tracks and holts. Asian small clawed otters were also shown to prefer
different habitats depending on which part they live in. For example, they found that
otters prefer to live near high-altitude streams in protected areas in India (Perinchery
et al., 2011), while they prefer low-elevation and moderate to low vegetation
structure in riparian systems in other parts of Southeast Asia (Hussain and de Silva,
2008). Otters were shown to shift to other areas after rainfall (Perinchery et al., 2011)
possibly due to change in abundance of the food such as crabs in freshwater
streams (Gratwicke, 2004).

As mentioned before, small clawed otters are semi-aquatic and thus the ratio of land
to water should be considered when constructing an enclosure for these animals.
Otters spend a lot of time in water but require land for resting, grooming, digging, and
foraging (Heap et al., 2008). In the wild, they only use a relatively narrow strip of

15
water and only occasionally move outside it (Kruuk, 2006). Most otters spend around
three-quarters of their lives on land (Foster-Turley and Santiapillai, 1990) and the
recommended percentage of water in the otter enclosure is from 20 to 30% (Heap et
al., 2008). Behaviourally healthy otters kept in appropriate enclosure conditions
spend more of their daytime hours on land than in the water (Reed-Smith et al.,
2009) and they were shown to swim more often in a more stimulating environment
(Harris, 1968). Sarah Duncan, the International Studbook keeper for ASC otters,
pointed out that it is also important to take into consideration the diverse exit from the
water with the use of fallen logs, rocky surfaces and more (Sarah Duncan, personal
knowledge).

1.6 Enrichment

Wild animals are able to choose when and where to forage, what to eat, whom to
interact with and where to sleep (Cummings et al., 2007). These choices are limited
for animals in captivity. Enrichment plays an important part of many captive animals
welfare. It is not viable to provide animals with everything they would have had in the
wild, due to the fact that most of the enrichments in captivity are artificial and do not
induce interaction with the surroundings in captive animals which restricts the
development of cognitive abilities and species-specific behaviours (Morgan and
Tromborg, 2007). It is still possible to enrich their lives and reduce undesirable
behaviours by using enrichments as similar as possible to their natural environment.

Appropriate enrichment was shown to encourage social interactions by reducing

aggression, abnormal behaviour and boredom, and by increasing activity level and
percentage of species-specific behaviour, which includes interactive and exploratory
behaviours performed and improve health overall (Bashaw et al., 2003; Mason et al.,
2007; Dishman et al., 2009; Kistler et al., 2009; Ryan et al., 2012). Enrichment has
successfully improved welfare of many captive animals (Swaisgood and
Shepherdson, 2005; Shyne, 2006). For example, Skibiel et al. (2007) showed that
captive felids reduced time pacing and increase activity level with additional
enrichment. However, the same enrichment can have a different effect on similar
species (Cooper et al., 1996; Tilly et al., 2010). Also, various environmental

16
enrichments can have different intensity of the effect on their behaviour. In other
words, the more complex the enrichment the better effect it has on the behaviour of
the animal (Ryan et al., 2012). The most effective enrichment types in reducing
stereotypy are thought to be the ones that are most time-consuming (Lumeij and
Hommers, 2008; Dallaire et al., 2012).

Small clawed otters are highly intelligent species (Perdue et al., 2013) and in the
wild, they need to go through thorns, husks; exoskeletons and shells to get to their
food, therefore, artificial feeding interventions can mimic their wild environment and
have positive effects on otter behaviour and welfare (Mellen and MacPhee, 2001).
Enrichment was shown to be advantageous in captive small clawed otters. For
example, food delivered via grapevine balls reduced hair plucking and aggression
(Ross, 2002). Freezing otter meals inside ice blocks was also shown to reduce
stereotypic behaviours and increased foraging in otters (Casson, 1990). Novel food
items have also been reported to be a good enrichment in animals (Skibiel et al.,
2007). Small clawed otters have a high interest in novel items and fruits which they
treat as toys, and they also shown high interest in insects as they like to catch and
eat bugs (Foster-Turley, 1978). Studies showed that they hunt for crickets even when
it is insignificant for their diet, despite the availability of other food and the absence of
deprivation (Foster-Turley and Markowitz, 2005).

1.7 Objectives and aims

The main goal of this research was to observe and compare captive groups of small-
clawed otters (Aonyx cinerea) in five zoos within the UK. In particular, this study
focused on time budget and activity patterns, enclosure use, visitor effect and public
feeding time effects. The study also focused on the prevalence of abnormal
behaviours. The hypotheses were that time budget and enclosure use would vary
between the zoos due to the variety of enclosures sizes and enrichment availability.
Visitors would have a positive effect on otters and public feeding would result in
increased percentage of begging and high activity.

17
2 Materials and Methods

2.1 Data collection

Asian small clawed otters were observed in five zoos in the UK. The observation was
scheduled from July until August, and data collection was conducted between 9 am
and 3 pm in each zoo for four days. An instantaneous scan sampling of the otter
groups was done once every 2 minutes, immediately recording the behaviour, the
enclosure use and the number of visitors. Furthermore, factors that could affect otter
behaviour such as temperature, precipitation, institutional management or any other
activities were also recorded.

2.2 Animals and housing

The otter groups chosen for this study were housed at five different zoos in UK:
Chessington World of Adventures (Chessington zoo), Battersea zoo Children’s Zoo
(Battersea zoo), WWT London Wetland Centre (LWC), Colchester zoo and London
zoo. Subjects were 17 captive small clawed otters. All the zoos had a male and a
female otter with the exception of London zoo which had 9 females, and Battersea
zoo which had two males. Otters in London and Battersea zoos were sterilized. All
the animals were born in captivity and had been housed in their respective zoos for
at least one year which means that all of the subjects were settled in their enclosures
and the social groups were also well established. Each group of otters was fed 3 to 5
times a day depending on the zoo. Water was available ad libitum in all enclosures.
More information about the focal animals can be found in Tables 1 and 2.

The enclosure was partially made of low glass and rock wall in all the institutions
except for Colchester zoo, where there was a large partially soundproofed glass
partition. The access to visitors varied between the institutions. In Chessington,
Battersea and Colchester, the visitor viewing areas were on 2 of the 4 sides. Visitor
viewing points in Colchester zoo were through a high glass wall and from a bridge
which is approximately 2 m away from the enclosure. In LWC, the visitors only had
access to the front of the enclosure.

18
Enrichment varied between the institutions. All of the institutions had growing
vegetation, but Colchester had much more in comparison and filled almost all of the
enclosure, whilst in Battersea there was much less vegetation in comparison to other
institutions. There was a large amount of bamboo available only in Colchester and
London zoos. All of the institutions had a waterfall and a large variety of substrates
available: sand, gravel, grass, boulders, large and small rocks apart from Colchester
where there was no sand available. In London zoo, there were glass panels so that
otters can be seen swimming underwater and a water slide. Both London zoo and
LWC had tunnels. In addition, otters in Colchester zoo were sharing the enclosure
with a binturong and in Chessington zoo there was music throughout the day.

Table 1. Summary of otter population, enclosure size and feeding times in five zoos in
UK. Institutions had public feeds (*) which were occurring at fixed time every day,
other feeding times were approximate.

Institution No. of Enclosure size Feeding times

otters
Chessington zoo 2 5.73x4.75=27.22 m2 8.20-8.40, 10.15*,
13.00-14.00,
15.00-16.00
Colchester zoo 2 9.5x30.94=293.9 m2 8.20-8.40, 13.15*, 16.30
Battersea zoo 2 14x12=168 m2 8.30, 11.00*, 14.30*,
16.30–17.00
London zoo 9 26.52x5.44=144.27 m2 12.30*,
16.00–17.00
LWC 2 25x8=200 m2 8.00, 11.00*, 14.00*, 16.30*

2.3 Behaviour measurement

Behaviours were grouped together into low and high activities and anticipatory
behaviours, as well as being analysed separately. All the behaviours presented in
this experiment can be found in Table 3. When the otters were inactive, resting, or
sleeping, the activity level was classified as ‘low activity’. When the otters were
involved in social play, enrichment related, locomotion, swim or foraging the activity
level was classified as ‘high activity’. This grouping of high and low activity

19
behaviours was adapted from Anderson et al. (2003). These groupings were used in
the analysis of visitor and feeding effect. Any other undesirable behaviour was
classified as “other abnormal”. Play-fight behaviour was distinguished from
aggressive fight using Pellis (1984) as guidance as these behaviours are thought to
be quite similar.
Table 2. Summary of the focal otters. All otters were parent reared.

Institution Animal Sex (F/M) Date of birth

Chessington zoo Lancelot M 26/03/2004
Mina F 03/10/2009
Colchester zoo Ravi M 15/11/2008
Lena F 24/07/2005
Battersea zoo Dodger M 1999
Ghandki M 16/09/09
London zoo 1 F 23/01/2001
2 F 11/11/2004
3 F 09/08/2005
4 F 09/08/2005
5 F 10/05/2006
6 F 10/05/2006
7 F 10/05/2006
8 F 10/05/2006
9 F 18/08/2007
LWC 1 M 03/10/2009
2 F 20/07/2011

20
Table 3. Analysed behaviours for otters in institutions. Adapted from Hawke et al.
(2002) and Gothard, (2007).

Behaviour Description

Low activity Rest Animal stays in one place, not alert to

environmental changes. Sometimes not
directly observed. If otter did not emerge
from resting spot after 10 min it was
assumed to be resting.
Inactive Standing or lying and not engaged in any
other behaviour.
High activity Locomotion Moving by way of walking, running, climbing
or swimming.
Forage Actively searching for food or eating.
Auto-grooming Self-grooming with the digits of their forefeet
or rubbing their entire body on a dry surface
such as smooth rock, or grass.
Allo-grooming Two animals are gently gnawing each other.
Enrichment related Any behaviour directed at an enrichment
device (e.g., sniff, pull, chew, drag, and
chew).
Social play Two or more animals chasing each other or
play-fighting.
Abnormal Anticipation Either standing on hind legs or calling to
visitors, often in eye contact with the visitors.
Sometimes manipulating the door.
Other abnormal Non anticipatory abnormal behaviours such
as neck twist/head throw or hair plucking.
Aggression Individual engages in contact aggression,
such as biting, clawing, wrestling, pushing or
non-contact aggression such as threat or
attempted aggression.
Other Full view of the individual is obstructed and
behaviour cannot be accurately determined
with the exception of being in the resting spot
for more than 10 minutes.

21
2.4 Time budget

The time budget data for each group of otters was combined over the 4 day sample
period and mean percentages were calculated for all behaviours to construct a table
and total frequencies were used for statistical analysis. Important behaviours were
merged as shown in Table 3.

2.5 Enclosure use

The enclosure was divided into various zones and then combined together to form
three general zones: “hideout” for any space which is further away from humans
serving as a hiding place for the animal where otters would be hard to spot most of
the time; “close to visitors” for parts of the enclosure from which visitors were clearly
visible to otters; and “water” for any water source which includes water slides,
waterfall and water pools.

2.6 Visitor analysis

The otter behaviour data was collected concurrently with the number of visitors. In
this study, the observer was counted as a visitor when clearly visible to the otters.
Only visitors situated in front of the enclosure were counted, excluding those passing
by the enclosure. The amount of visitors standing alongside the enclosure was
scored on each scan. Later, the data was grouped into three categories: 0 to 5
visitors was classified as low (L), 6 to 10 visitors as medium (M), and any number of
visitors over 11 was classified as high (H). The influence of the visitors was analysed
by comparing the behaviour of otters depending on different categories of visitors.

2.7 Feeding

Behaviours were grouped into anticipatory and low activity an hour before and after
feeding and used in the analysis. Some of the data was analysed differently due to
species circumstances. The behaviour in Chessington was recorded prior to cleaning

22
instead of prior to feeding because the otter enclosure was always cleaned prior to
feeding. In addition, the otters in London zoo were occasionally given a snack of
locusts 20 minutes before the feeding time. For this reason, otter behaviour between
the two feeding times was not included in the analysis to avoid any errors.

2.8 Data analysis

Chi-squared test of association was carried out on the total frequencies of behaviours
observed in each group of otters. The same test was carried out when examining
zone use by each group of otters on total frequencies. Individual contributions to chi-
squared were inspected to identify the main effects where significant associations
were found. A chi-squared test of association was used on the effect of number of
visitors on the behaviour of otters, testing whether frequencies of behaviours differ
significantly from the expected number. To test whether feeding time affects otter
behaviour, Wilcoxon test was carried out on the behaviour of each group of otters an
hour before and after the feeding time. In addition, descriptive statistics were used to
interpret the results. Genstat 17 was used for any statistical analysis carried out in
this study and Figures were constructed using Microsoft Excel 2010.

23
3 Results

3.1 Time budget

The proportion of time devoted to the different activities was highly variable among
the institutions (See Table 4) and high activity levels were significantly different
between them (❑2= 970.38, p<0.001). Otters were most active in London zoo and
least active in Battersea zoo.

Foraging was low in all of the institutions ranging from 3.8% in Colchester zoo to 10%
in London zoo. Both allogrooming and auto-grooming were generally low in the all of
the institutions, with the lowest percentage in Battersea zoo (0.1%) and the highest in
Colchester zoo (1.4%) for allogrooming, and the lowest percentage in Chessington
zoo (1.4%) and the highest in Colchester zoo (3.5%) for auto-grooming. Enrichment
related activities were very low in London zoo (2.1%) and Battersea zoo (2.2%) when
comparing to other institutions. Social play was the highest in Colchester zoo
(14.2%) and very low in Battersea zoo (0.6%).

Chi-squared test did not show any significant difference in otter low activity
behaviours and overall the percentage of rest was high in the institutions. There were
no high levels of inactivity in any of the institutions.

There was a significant difference in the presence of abnormal behaviours amongst

the institutions (❑2= 577.10, p<0.001). Otters in Battersea zoo expressed almost
twice as much of abnormal behaviours than expected, whereas, these behaviours
were rarer than expected in Colchester and LWC. Other abnormal behaviours were
not included in the statistical analysis because the only non-anticipatory abnormal
behaviours in otters was neck twisting which was expressed only by one of the otters
in Chessington zoo and was observed for 3.2% of the time. Overall aggression level
was very low in all otters. It was extremely low in Colchester zoo (0.1%) and highest
in London zoo (1.3%).

24
All of the otters were always visible during the observation period, apart from the
times where they were in the resting spot. Moreover, otters in Colchester zoo were
out of view 27.5% of the observation time due to extensive foliage.

Table 4. Mean activity budget as a percentage of visible time for groups of Asian
small clawed otters in five zoos. Asterisk indicates a significant difference (p<0.001)
in the behaviour between the groups.

Chessington Colchester Battersea London LWC

Behaviour zoo zoo zoo zoo
Rest 58.7 43.5 53.9 54.2 63.9
Inactive 2.2 0.7 5.3 7.6 1.8
Locomotion* 9.3 10.8 12.5 11 15
Forage* 6.6 3.8 5.9 10.0 6.2
Autogrooming* 1.4 3.5 1.7 3.4 2.5
Allogrooming* 0.6 1.4 0.1 0.3 0.3
Enrichment related* 3.7 4.2 2.2 2.1 3.9
Social play* 2.4 3.8 0.6 2.3 1.8
Anticipation* 6.5 0.3 16.5 0.0 4.1
Aggression* 0.4 0.1 0.8 1.3 0.6
Out of view 0.0 27.5 0.0 0.0 0.0

3.2 Enclosure use

The proportion of time otters spent in different zones was highly variable among the
institutions. Water use was significantly different between the institutions ( ❑2 =
197.42, p<0.001). In Colchester zoo, water use was less than half of the expected
value and was the lowest amongst the institutions (7.4%). The highest water use was
observed in London zoo (23.6%).

The “close to visitors” zones usage was significantly different between the institutions
(❑2 = 1136.51, p<0.001). Otters in Battersea zoo used the “close to visitors” zone
twice as much as expected, otters in Colchester zoo used it half as much as
expected, and in LWC otters used it seven times less than expected. The use of
‘close to visitors’ zones was very small in London (2.7%) and Colchester zoos (9%).
In all of the institutions, the percentage of ‘hideout’ used was very high in comparison
to use of “close to visitors” ranging from 43.9% in Battersea zoo to 77.4% in

25
Colchester zoo. Battersea zoo was the only institution in which the use of “close to
visitors” (46.5%) and “hideout” (43.9%) was roughly the same (Figure 1).

90.0 Chessington
Colchester
80.0 Battersea
London
70.0 LWC
Percentage use of the zone

60.0
*
50.0

40.0

30.0 *

20.0

10.0

0.0
water hideout close to visitors

Figure 1 Mean enclosure use as a percentage of visible time for groups of Asian
small clawed otters in five zoos. Asterisk above the bars indicates a significant
difference (p<0.001) between the groups.

3.3 Visitor analysis

High activity behaviour was directly related to the number of people in all of the
institutions. There was a general trend of activity increasing from low to medium and
to high number of visitors. There was no significant difference in the levels of “low
activity” between the groups of visitors.

The percentage of abnormal behaviours was different between the institutions and
the level of abnormal behaviour expressed with ‘high’ visitor number were much
higher than expected in all of the institutions except Colchester zoo where there was
no significant difference. Only in Battersea zoo there was a trend in otters increasing

26
abnormal behaviour with increasing visitor number. In other institutions, when looking
at the percentages there appears to be no trend. All the percentages for each of the
behaviour groups with various visitor group sizes and chi squared results can be
seen in Table 5. Since aggression levels were so low in all of the institutions, they
were not used in the statistical analysis as it would unlikely provide a reliable result.

Table 5. Mean percentage of time spent engaged in behaviours as a function of

crowd size. (L – low, M – medium, H – high). High activity behaviour was directly
related to the number of people in Colchester (❑2 = 25.35, p<0.001), Battersea (❑2=
138.01, p<0.001), Chessington (❑2 = 84.47, p<0.001), LWC (❑2 = 386.73, p<0.001)
and London (❑2 = 432.41, p<0.001). Abnormal behaviour was significantly different
between the visitor groups in Battersea zoo (❑2 = 46.62, p<0.001), LWC (❑2 =
256.99, p<0.001), London zoo (❑2= 301.50, p<0.001) and Chessington ( ❑2 = 24.75,
p<0.001).
Crowd Chessington Colchester Battersea London
Behaviour size zoo zoo zoo zoo LWC
High activity L 21.3 22.7 17.5 21.5 21.2
M 49.2 52.3 47.9 40.9 54.6
H 61.5 100.0 54.4 51.9 73.2
Low activity L 66.6 55.8 65.9 69.8 75.9
M 32.3 47.7 27.1 51.4 19.4
H 34.6 0.0 21.1 24.2 19.0
Abnormal L 6.4 0.6 15.3 6.6 2.0
M 13.1 0.0 22.9 6.2 24.1
H 3.8 0.0 24.4 23.9 7.7
Aggressive L 0.6 0.1 0.8 1.4 0.5
M 0.0 0.0 2.1 1.0 0.0
H 0.0 0.0 0.0 0.0 0.0

3.4 Feeding

Wilcoxon test showed that there was no significant difference in activity level before
and after feeding in Chessington and Colchester zoos. Otters were exhibiting
significantly more low activity behaviours after feeding in Battersea zoo (p<0.01),
LWC (p<0.01) and London zoo (p<0.001) than before.

There were significantly less anticipatory behaviours in Battersea zoo (p<0.01), LWC
(p<0.01), London zoo (p<0.001) and Chessington zoo (p<0.01) after feeding. In
Chessington and Battersea zoos otters were often observed to run towards the
visitors closer to feeding time. Levels of aggression were not significantly different

27
before and after feeding in any of the institutions except for London zoo, where they
were significantly higher before feeding (p<0.05). However, large standard deviation
of the percent of aggression before feeding indicates that the difference may be a
result of sampling error. Since there was neither aggression, nor abnormality an hour
prior and after feeding in Colchester zoo, the data was not statistically analysed for
this zoo.

90

80 before

after
70 *
Percentage of behaviour observed

*
60

50 *

40

30

20

10

0
Chessington Colchester Battersea London LWC

Figure 2 Percentage and standard deviation of low activity observed in otters in five
institutions before (blue) and after (red) feeding. Asterisk above the bars indicates a
significant difference (p<0.01) between the groups.

28
 50

45
before
40 after
Percentage of behaviour observed

35 *

30

25

20 *
*
15 **

10

0
Chessington Colchester Battersea London LWC

Figure 3 Percentage and standard deviation of anticipatory behaviour observed in

otters in five institutions before (blue) and after (red) feeding. Asterisk above the bars
indicates a significant difference (p<0.01) between the groups. Double asterisk
indicates a significant difference with p<0.001.

29
4 Discussion
The results of this study clearly show that there are significant differences between
the institutions in the use of enclosure, time budget, reaction to the feeding and the
effect the visitors have on the behaviour of the otters. This means that the factors
which varied between the institutions such as otter management or the design and
size of the enclosure play an important role in the behaviour of otters.

4.1 Time budget

There was a high variability of “rest” between institutions with an extremely high
value in LWC. In Colchester zoo, otters were observed to rest the least in
comparison to other zoological institutions and this may be caused by a larger
enriching enclosure. Studies suggest that when captive animal devotes most of its
time in low activity behaviours such as sleeping and resting, it usually means that its
enclosure is not enriching enough which leads to boredom since other behaviours
are not motivated (Dawkins, 1998). However, these studies usually compare activity
levels of captive and wild animals. The only available data about levels of resting
behaviour in small clawed otters shows that they spent roughly same time awake and
asleep in the wild (Stephens, 1954). This would suggest that levels of activity in this
study are not very different from the ones in the wild. Nevertheless, a confirmation of
the study on wild otter activity level is required since this was the only study on Asian
small clawed otters and was conducted sixty years ago. The levels of “rest” in this
study would be considered to be normal only if they are nocturnal as reported in
some papers (Larivière, 2003) and spend roughly the same time awake and asleep
at night as well. Interestingly, inactivity levels were similar between the institutions
and very low, regardless of the design and size of the enclosure. High inactivity is
also another sign of boredom (Dawkins, 1998). This supports the theory that low
“rest” levels in this study are possibly not due to boredom but rather are normal levels
found in otters.

High activity levels do not necessarily indicate good welfare because most of the
abnormal behaviours are considered to require high activity (Mason et al., 2007;
Feeney et al., 2011). However, in this study high activity levels were expressed

30
through species-specific behaviours such as foraging, grooming, social play and
enrichment related behaviours which were low in all of the institutions. These are the
behaviours which are usually highly expressed in animals when their environment is
similar to their natural environment (Morgan and Tromborg, 2007). In London zoo,
natural behaviours in otters were often stimulated by high variety of enrichment such
as spreading blood in the enclosure to stimulate their senses; however, the study
shows that species-specific behaviours were still low in London zoo. These low levels
in this study suggest that their environments do not promote natural behaviours.

Foraging was promoted in London zoo by hiding the food and throwing feeding
enrichment such as crickets, whilst in other institutions keepers scatter food in the
presence of otters. On one of the days, otters in London zoo were observed playing
with the crickets, releasing and recapturing them for a long time. Recent studies
show that with enriched environment animals spent more time foraging and less
inactive (Ryan et al., 2012; Dishman et al., 2009; Kistler et al., 2009).Therefore it is
not surprising that otters were highly active and were shown to forage the most in
London zoo. Although foraging was the highest in London zoo, it was still not
satisfactory as other studies report foraging behaviour to take 20% of their time in
captivity (Gothard, 2007). Most of the institutions did not even reach half of that
percentage.

Although there were differences in the percentage of allogrooming and autogrooming

between the zoos, it was generally low in all of the institutions and studies show that
grooming is a common behaviour in otters (Foster-Turley, 1978). Grooming in this
study was the highest was in Colchester zoo, the institution with the largest
enclosure, and a study suggests that levels of grooming depend on the size of the
enclosure (Bartolini and Bicca-Marques, 2011). However, grooming was still low in
this zoo and the size of the enclosure was almost five times larger than the
guidelines (Heap et al., 2008). In fact, the size of the otter enclosure in all of the
institutions in this study was larger than the guidelines stated apart from Chessington
zoo. It is advisory to further research the preferable enclosure size of otters which
provides them with plenty of space to perform natural behaviours. There is no
information on the percentage of grooming in the wild and captive small clawed
otters. However, a 24 hour observation study of male sea otter activity budget

31
showed that they spent 19% of time foraging (Finerty et al., 2009) which is
approximately four times larger than the results in this study suggesting that the
grooming was very low in the institutions in this study.

Enrichment related activities were very low in London and Battersea zoos and the
highest in Colchester zoo. The results for Battersea zoo are not surprising since they
had the lowest variety and quantity of enrichment. However, in London zoo otters
were shown to spend almost as much time on the enrichment related behaviours as
otters in Battersea zoo, whilst they clearly had more enrichment provided for them.
For example, otters were shown to play and eat the nuts which were falling down
from the hazelnut tree and they also had deadfall trees and high levels of foliage. As
mentioned before, different types of enrichments have different effects on the
behaviours of the animal (Ryan et al., 2012). Therefore, it is not the quantity or
variety of enrichments that is provided for animals that induces positive behaviours; it
is the specific types of enrichment that promotes enrichment interaction. For
example, a study by Ryan et al. (2012) showed that gorillas spend more time feeding
from hanging forage-filled feeder than with scattered food.

The results of social play in otters were surprising. It was hypothesized that social
play would be the highest in London zoo since the choice of individuals to interact
with is higher. Percentage of social play was the highest in Colchester zoo which had
a more naturalistic environment and limited public access. Social play was the lowest
in Battersea zoo which had an open enclosure and low availability of shelters from
public. This demonstrates that affiliative behaviour such as social play is negatively
affected by the inability to hide from the visitors which was shown in other studies
(Jones, 2003; Hosey, 2008).

Otters in Battersea zoo expressed almost twice as much of abnormal behaviours

than expected, while levels of these behaviours were very small in Colchester zoo.
Also, the variety of abnormal behaviours expressed in groups of otters was very low.
Apart from the neck twisting that was observed in one of the otters in Chessington
zoo, begging and door manipulation were the only other abnormal behaviours

32
expressed in otters in this study. This contrasts with the results of another study of
small clawed otters where anticipatory behaviour was observed 21% of the time
budget (Gothard, 2007); most of the otters in this study had much lower percentage
of anticipatory behaviour with the exception of Battersea zoo, where the percentage
of anticipatory behaviour was approximately 16% of the time budget. This result is
possibly due to habituation to the keepers.

Overall aggression level was very low in all the otters, with extremely low percentage
in Colchester zoo and the highest in London zoo. It was noted by some keepers in
the institutions that the reason for not keeping more than two otters is because it
usually results in higher levels of aggression. This study illustrates that large number
of otters is possibly a reason for high levels of aggression. However, although levels
of aggression were the highest in London zoo, they were still only 1.3% of the time
budget which is very low. Aggression is not necessarily an undesirable behaviour,
since it is expressed in animals in the wild (Creel et al., 1993; Sands and Creel,
2004), it is the levels of aggression that is one of the issues in captivity (Morgan and
Tromborg, 2007). However, it is clearly not an issue in this study.

It was observed that there were factors that could have affected the behaviour of
otters in the institutions. It was mentioned that time budget can be affected by
conspecific (Challender et al., 2012). In this study, it was very common for an otter in
London zoo to wake up the rest of otters and attempt to play with them, eventually
waking them up. Also the female otter in Chessington zoo was more active than the
male, and when the male was resting, she often ran up to him and attempted to play
with him, resulting in him not being able to sleep. Otters spent almost all of their time
together and it was very unusual to see one otter spending time away from its
conspecific. As a result, the comparison of sociality was not used in the observations.
However, further research should concentrate on measuring the distance between
the otters as this could allow us to measure the degree of sociality.

An important result is that mating was observed many times in this study, and not
even once was it occurring in the water. This result directly opposes the findings of
Heap et al. (2008) who reported that the mating was mainly observed in shallow
water in captivity. When discussing the breeding of otters in captivity, some

33
institutions claimed that reproduction success is low. Jason Palmer (personal
knowledge), the Animal Collection Manager and IUCN Otter Specialist Group
member, suggested the reasons for unsuccessful breeding in otters: enclosure
design, group structure or high inbreeding. The first two factors are unlikely to be the
reasons for the low reproduction in institutions of this study due to a variety of
enrichments, enclosure size and group structure. A more likely reason is that due to
high levels of inbreeding in the UK, as confirmed by Jason Palmer, make them
unable to produce offspring.

Otters were observed to cooperatively build a nest in London zoo. This behaviour
was only reported in few studies (Wright, 2005). Similarly to the previous research,
otters in this study preferred to use bamboo for the construction of the nest. Instead
of carrying the bamboo inside the holt, they were building a nest on the shoreline of
the water pool. In Chessington and Battersea zoos, otters were also seen to build a
nest, however, it was always one otter that was building it, whilst in London zoo; all of
the otters were involved. This observation suggests that bamboo is an important type
of enrichment that can result in otters spending more time in high activity behaviours
expressing higher levels of natural behaviours. Cooperative bedding gathering was
reported at least once and has not been well researched (Wright, 2005). A study of
this interesting behaviour could provide some insight into social behaviour of otters.

4.2 Enclosure use

As expected, water use was the lowest in Colchester zoo where the pool was
extremely small and otters did not have ample room to swim and dive. Previous
studies show that small clawed otters spend some 25% of the time in water (Foster-
Turley and Santiapillai, 1990), which is a much higher number than observed in
Colchester zoo (2.5%). The highest levels of water use were observed in otters in
this study were in LWC (23.6%) where otters had a big pool but there was plenty of
terrestrial ground as well. Chessington zoo had the highest percentage of water in
the enclosure and yet the otters did not use water more than other institutions. In fact
they used it less than London zoo and LWC which suggests that the biggest
percentage of pool does not necessarily mean it would be used the most. In addition,

34
when the percentage of water in the enclosure is higher than required it reduces the
usable enclosure size enormously. Previous studies show that otters swim more
often in more stimulating environment (Harris, 1968), which is possibly the case in
LWC. It is required to compare the time otters spend in water in captivity and in the
wild to find out the right ratio of land to water use by otters. Further study of water
use of Asian small-clawed otters in the wild is needed since there is no data
available.

Otters were observed to spend a lot of time in the “close to visitors” zone in Battersea
zoo, whilst they used it the least in LWC and Colchester zoo. In all of the zoos, the
percentage of “hideout” use was very high in comparison to the use of the “close to
visitors” zones. This result suggests that animals were expressing avoidance
behaviour towards visitors (Birke, 2002). Battersea zoo was the only institution in
which the use of “close to visitors” and “hideout” was roughly the same. This result
confirms that otters in Battersea zoo may be habituated to visitors, and therefore, are
not avoiding them. Another theory is that, as mentioned before, the enclosure of
otters in Battersea was very open with almost no shelters from the visitors which
suggest that otters were forced to spend most of the time in close proximity. They
were often observed to sleep in very close proximity to humans, whilst otters in LWC
always chose to sleep in the shelter. However, it does not necessarily mean that
otters in LWC were avoiding the visitors, because when they were not resting they
were always in close proximity to humans and regardless of the high availability of
the zones further away from the humans, they only used them occasionally. In
Colchester zoo, otters used “close to visitors” zones when planning to use the pool or
during feeding time, otherwise they spent most of the time further from the visitors.
This result, however, does not necessarily mean that otters were avoiding the
visitors, because the enclosure was filled with the foliage which suggests that otters
would not be visible to the visitors, even when not attempting to hide from them. It is
suggested that in further studies, the method of measuring the enclosure use should
be adapted from Rose and Robert (2013) where the size of the zones was measured
and the expected percentage of use of a certain zone would depend on the size of it.
This method would allow obtaining a more accurate calculation of zone use.

35
4.3 Visitors

High activity behaviours increased with larger number of people in all of the
institutions. If visitors had a negative impact on the otter behaviour they would
express they would express it by spending less time in view and being at a greatest
distance from viewing area (Hosey et al., 2009). However, this is not the case in this
study. Although, otters in Colchester zoo spent significant time out of view, which
would suggest that they are avoiding the public, it is led to believe that the main
reason was that the otter enclosure in Colchester zoo had a lot of foliage which
covers a lot of ground and therefore to spot an otter is very difficult. Furthermore,
when otter did approach the glass wall and was close to visitors it appeared to never
look nor react to visitors. In other institutions, such as Battersea and Chessington
otters were often seen running towards the public and keepers begging and
vocalising. The result would suggest that otters increase activity due to being
habituated to humans and associate high visitor numbers with food (Margulis et al.,
2003). However, due to similar results observed in Colchester zoo where otters never
begged from visitors, nor showed any signs of reaction to them, it is believed that
high otter activity resulted in high visitor levels rather than otters being more active
with the presence of visitors as reported in some studies (Kuhar, 2008). As
mentioned, visitors prefer to see active animals expressing species-specific
behaviours (Wolf and Tymitz, 1980; Anderson et al., 2003). Visitors often came to
see otters when it was feeding time due to higher chances of observing active otters.

Chi squared test shows that levels of abnormal behaviour expressed with “high”
visitor numbers were much higher than expected in all of the zoos except Colchester
zoo where there was no significant difference. However, when looking at the
percentages of abnormal behaviour there is no correlation between abnormal
behaviour and increased number of visitors apart from Battersea zoo. The abnormal
behaviours in otters in London zoo were the highest with high visitor number but
were almost the same with low and medium visitor number. It was suggested that
animal behaviour changes only when the number of visitors, in their perception, is too
high. For example, a study showed that orangutans were stressed and reduced
social play when visitor number was more than 100 visitors (Jones, 2003).

36
Overall, as there was no high abnormality visible in otters with increased number of
visitors, it is suggested that otters in this study were adapted to proximity of humans
and suitable to be kept in captivity. Further studies should research the effect of
higher number of visitors to see whether the result would be different.

It was often observed that otters reacted differently to visitors. They were seen to run
towards some visitors but not the others. It is advisable to further investigate this
phenomenon and analyse whether otter behaviour depends on the colour or type of
the clothes that visitors were wearing. Furthermore, when visitors were leaning on
the enclosure wall, otters were also readily running towards them. This may be due
to otters expecting to be fed by visitors. Otters are never fed by the public and they
appear to know well where the food comes from and associate it with the keepers.
However, it is interesting that otters, which are considered to be animals of high
intelligence (Larivière, 2003), still beg from the public, whilst they never receive any
food from them and the clothes are not similar to the ones worn by keepers.
Investigating this phenomenon would give a better insight to the begging of otters.

The main limitation of the analysis of visitor effect on the behaviour of otters was the
fact that the maximum visitor number between the zoos varied from 15 in
Chessington and Colchester up to 42 in London, LWC and Battersea. Moreover,
otters in Battersea and Chessington zoos were observed calling to visitors who were
standing far away from the enclosure or visitors passing by who were not counted in
the study.

Future studies should concentrate on accurately measuring visitor number choosing

a different methodology. Instantaneous evaluation in conjunction with daily evaluation
would give a much more precise result. The evaluation used in this study allows us to
score animal behaviour and visitor characteristics accurately measuring crowd size in
the animal enclosure. The main disadvantage of this method is that cumulative
effects of varying visitor numbers cannot be measured and increased visitor density
may be a result of high animal activity (Kuhar, 2008). Measuring the effect of visitors
on otter activity and any other behaviour eliminating the data taken during any events
such as shows and feeding times would give a more accurate result and would show
whether otters become more active with increasing visitor number.

37
Studies show that the volume of sound made by visitors can affect the behaviour of
animals and it can result in avoidance behaviour (Birke, 2002; Choo et al., 2011).
The hearing of otters is considered to be good but nothing is definitively known about
their hearing acuity or frequency ranges heard (Reed-Smith et al., 2009). Therefore,
investigating the effect of noise on their behaviour could really improve our
understanding about the otters. Since most of the studies concentrate on the effect of
the number of visitors on animal behaviour an interesting investigation could be
focused on presence and absence of visitors and visitor behaviour (Choo et al.,
2011). For example, behaviours such as shouting, waving and tapping the glass
could cause stress in the wild animal as it was observed in this experiment.

4.4 Feeding time

Wilcoxon test showed that there was no significant difference in activity level before
and after feeding in Chessington and Colchester zoos. However, otters were
exhibiting significantly more low activity behaviours after feeding in Battersea zoo,
LWC and London zoo. Studies show that when feeding is predictable, animals often
become more active prior to the event (Mason et al., 2007; Feeney et al., 2011). This
was observed in most of the institutions in this study, apart from Chessington and
Colchester zoos.

Levels of aggression were not significantly different before and after feeding in any of
the institutions except for London zoo, where they were significantly higher before.
However, large standard deviation of the percent of aggression before feeding
indicates that the difference may be a result of sampling error. Also, since the levels
of aggression were very low in all of the zoos it is not possible to confirm whether
aggression was different before the feeding time.

There were significantly less anticipatory behaviours in Battersea zoo, LWC, London
zoo and Chessington zoo after feeding. In Chessington and Battersea zoos otters
were often observed to run towards the visitors and beg an hour prior to feeding time.
This result concurs with other studies where animals were shown to exhibit begging

38
behaviour prior to feeding time (Kistler et al., 2009; Choo et al., 2011; Tan et al.,
2013). Otters in Chessington, Battersea and London zoos emitted begging calls and
ran towards people regardless whether it was a keeper or a visitor. Presence and
sound of keepers entering off-exhibit area or just being close to the enclosure often
prompted the otters to run to the door and dig under the door with their paws or
scratch the door itself. Therefore, it appears that otters associated the keepers with
the food, as this was accompanied by feeding. Door manipulation was shown to be
associated with food anticipation (Ross, 2002). There is no doubt that anticipatory
behaviours were observed in otters in this study due to the predictable feeding.
Begging was also observed in some studies due to hunger or infrequent feeding
(Lyons et al., 1997; Mellowship, 1990; Gothard, 2007). It is possible that this was the
case in this study as some otters were observed eating whole fishes, including the
head, which according to Foster-Turley (1978) is a sign of hunger. In this study,
otters often moved closer to humans to beg. They would spend most of their time
either in front of the visitors, begging, or in front of the door from which the keeper
would enter and give the food an hour prior to feeding time. Further study on the
enclosure use before and after feeding would allow us to test this theory statistically.
Studies show that another anticipatory behaviour observed in otters is pacing (Hawke
et al., 2000; Ross, 2002). Yet, otters were never seen pacing in this study.

Otters are very vocal animals and produce a relatively complex vocal repertoire
which carries potential information concerning context and the identity of the
individual otter (McShane et al., 1995; Lemasson et al., 2014). Studies show that
otters have a specific call for hunger which is identified as long and loud sound
sometimes broken up into a series of short bursts (Foster-Turley, 1978). It was
observed in small clawed otters prior to feeding. However, it was not used in the
statistical analysis because of the complexity of call identification. Further studies
should concentrate on researching the vocal repertoire of otters as the knowledge of
it could assist in understanding otter behaviour.

39
4.5 Study limitations

The main limitation of this experiment was the lack of analysis of external factors
such as temperature and institutional management. Although these factors were
noted during the experiment, they were not used in statistical nor descriptive analysis
and yet might have interfered with the results. However, Gelatt et al. (2002) found no
influence of weather apart from rain on the behaviour of small clawed otters. Since
there was no precipitation on any of the days, it was not affecting otters in this
experiment. Also, as mentioned before, otters were sharing an enclosure with a
binturong in Colchester zoo. In this study they were never seen to interact and even
being in close proximity, therefore it is safe to assume that binturong did not have
any effect on the behaviour of otters. The effect of visitors on the otters was analysed
by using visitor number; however, the noise or difference in visitor activity was not
used in this study. This could have had a significant effect on otter behaviour as well
as any other external noise.

4.6 Recommendations

It is recommended to provide otters with various types of enrichments to allow them

to choose from. In this study it was more common for otters to play with pebbles than
any other type of enrichment. In some of the institutions otters were playing with
seeds which fell from the trees. In Chessington, the hazelnut tree was a perfect type
of enrichment, since the nuts fell on the floor randomly on the water slide and were
sliding into the pool with otter trying to catch it before it fell into the pool. Otters in
Chessington zoo were also seen playing with conifer tree seeds falling into the pool.
In both zoos, otters were chewing and playing with the seeds which suggest that a
tree with seeds the size of hazelnut are a great type of enrichment for otters,
promoting foraging as well as well as activity which was needed to retrieve the
seeds.

Abnormality is a sign of a bad welfare which needs to be dealt with regardless of the
levels and types of abnormal behaviours expressed. It is clear that most of the otters
in this study expressed anticipatory behaviours prior to the feeding time and therefore

40
this issue requires attention. One of the suggested ways of dealing with anticipatory
behaviour is to reduce predictability of feeding. For instance Ross (2002) proposed to
fill grapevine balls with food and toss them into the exhibit pool, reducing aggression
and anticipatory behaviours such as self-plucking, auto-plucking and door
manipulation. Another example is the experiment by Hawke et al. (2000) where food
was placed at random times with the use of a catapult. This reduced begging and
pacing. In addition, it is advisable that keepers see otters outside the feeding times
so that otters would not associate them with food (Heap et al., 2008). Predictable
feeding times are usually to entertain the visitors enhancing their experience.
However, this study shows that predicable schedule has negative effects on otters
and that randomising feeding times is required to reduce undesirable behaviours in
otters. To satisfy the public by allowing them to see the animals during their feeding
time, when they are most active, we suggest supplying visitors with the timetable of
feeding times on the day of their arrival.

This study clearly shows that otters in Colchester zoo performed better than in any
other institution. Due to high variability between the zoos it is hard to identify the
reason behind this result. However, the main differences between Colchester and
other institutions were the size, the visibility and the high wall of the enclosure. It is
clear that otters in Colchester zoo were much more isolated from the public than
otters in other institutions, suggesting that otter welfare can be improved by providing
them with enough space where they can perform various types of behaviour and not
being in close proximity to visitors. However, it is important to remember that animals
in the zoo are to raise awareness and to provide visitors with the good experience.
Visitors in Colchester zoo were observed to be not happy when approaching to the
enclosure and not seeing the animals as otters were mostly seen during the feeding
time. It is, therefore, advisable to provide otters with plenty of foliage and shelters to
hide from the visitors, but at the same time have a lot of open space filled with
enrichment such as pebbles, small shrubs and boulders to promote otters coming
close to visitors and being able to retrieve into hideout zones when under pressure
from the visitors. Water should take 20 to 30 % of the enclosure as mentioned in the
guidelines (Heap et al., 2008) as lower percentages result in otters not being able to
freely swim and dive, whilst higher percentages reduce the usable enclosure size
enormously.

41
5 Conclusion

There were clear differences between the institutions in this study which suggests
that the enclosure size and design, visitors and predictable schedules play a major
role in the behaviour of otters. Regardless of the fact that Asian small clawed
population is declining, there is very limited information about their behaviour both in
captivity and in the wild.

The main result of this study which requires attention was the high percentage of
“rest” behaviour in otters in all of the institutions. Since there is no reliable data on the
time budget of the small clawed otters neither in the wild nor in captivity, it is
advisable to carry out a meta-analysis on the time budget in the wild as well as in
captivity. This result could assist in determining the welfare of otters in captivity as
well as show the optimal values for the expression of other behaviours such as
grooming, object manipulation, aggression and sociality. In addition, data should be
collected for 24-hours to test whether any of the behaviours are exhibited by the
otters at different time (e.g being active during the night).

There was a high variability of water to land ratio. Although 20-30% of water is a
guideline, it is important to test whether otters express any undesirable behaviour if
the water level is over the guidelines. In Colchester zoo, for example, availability of
water was below the guidelines, however, it appeared that they expressed a lot of
positive behaviours. In addition, there was a variety in the choices between spending
more time in “close” or “hideout” zones between the institutions. However, a similar
study should be repeated measuring the size of each zone.

Visitors were shown to have a negative effect on the otters, resulting in abnormal
behaviours in almost all of the institutions. High activity was observed in conjunction
with large visitor crowds. This study suggests that high otter activity is causing the
increased visitor number and not otherwise. Further studies should perform visitor
analysis including noise and visitor behaviour.

42
As for the predictable feeding schedule, it was clear that otters were expressing high
anticipatory behaviours before the feeding time, which indicates that the welfare of
otters in the study was sub-optimal. Although predictable feeding schedule is a part
of entertainment for the visitors, it was shown to clearly have negative effects on the
otter behaviour. Therefore, to satisfy the public without compromising otter welfare it
is suggested to randomise otter feeding and inform visitors about the feeding times
on the day of their arrival. It is well known that visitors play an important role in
zoological institutions; however, it is also important to remember that animal welfare
is the main priority, especially when dealing with animals that are threatened in the
wild such as Asian small clawed otters. Therefore, institutions should improve animal
welfare by minimizing predictable events providing otters with plenty of shelters to
hide from visitors when desired.

43
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