An Empirical Case Study Examining Effectiveness of Environmental Enrichment in Two Captive Australian Sea Lions ( Neophoca cinerea )

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An Empirical Case StudyExamining Effectiveness ofEnvironmental Enrichment inTwo Captive Australian SeaLions (Neophoca cinerea)Bradley P. Smith a & Carla A. Litchfield aa School of Psychology, University of SouthAustralia , Magill, AustraliaPublished online: 25 Mar 2010.

To cite this article: Bradley P. Smith & Carla A. Litchfield (2010) An Empirical CaseStudy Examining Effectiveness of Environmental Enrichment in Two Captive AustralianSea Lions (Neophoca cinerea), Journal of Applied Animal Welfare Science, 13:2,103-122, DOI: 10.1080/10888700903371863

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JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 13:103–122, 2010

Copyright © Taylor & Francis Group, LLC

ISSN: 1088-8705 print/1532-7604 online

DOI: 10.1080/10888700903371863

ARTICLES

An Empirical Case Study ExaminingEffectiveness of Environmental

Enrichment in Two Captive AustralianSea Lions (Neophoca cinerea)

Bradley P. Smith and Carla A. LitchfieldSchool of Psychology, University of South Australia, Magill, Australia

This case study examined the effect of environmental enrichment on the activity

budgets of a male and female Australian Sea Lion (Neophoca cinerea) housed to-

gether at Adelaide Zoo. Using non-food-related (intrinsic) and food-related (extrin-

sic) enrichment objects, the study conducted an ABABA (withdrawal) experimental

design over a 30-day period (180 hr). The study expected extrinsically reinforcing

objects to be more effective than intrinsically reinforcing objects in reducing pattern

swimming. The male sea lion spent more than 45% of scans engaged in pattern

swimming during the initial baseline, which was reduced by at least 25% when

enrichment items were present. However, there was no evidence of stereotypic

behavior in the female sea lion, indicating that individual differences may exist.

When enrichment was present, the study observed more active behaviors in both

nonhuman animals. They spent more time interacting with the non-food-related

objects overall. Therefore, introducing simple enrichment devices offers a cheap,

practical, and effective method of adding complexity to the environment, which is

likely to benefit the animals’ welfare and enhance the zoo-visitor experience.

Australia’s only endemic pinniped, the Australian Sea Lion (Neophoca cinerea)

is endangered, with a severely fragmented population of <14,000 individuals

Correspondence should be sent to Bradley P. Smith, School of Psychology, University of South

Australia, St. Bernards Road, Magill, South Australia 5072, Australia. Email: bradley.smith@unisa.

edu.au

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104 SMITH AND LITCHFIELD

remaining (Goldsworthy & Gales, 2008). Aspects of Australian Sea Lion behav-

ioral ecology relevant to optimal enclosure design and captive husbandry include

the following: They are benthic (bottom) diurnal feeders and fast, powerful

swimmers “porpoising” out of the water on the surface. They can dive to depths

of 100 mC for up to 8 min at a time in search of prey and regularly regurgitate

parts of prey such as cephalopod beaks (McIntosh, Page, & Goldsworthy, 2006).

When hauled out, they spend most of their time resting, sleeping, or engaging

in social interactions (Costa & Gales, 2003; Fowler, Costa, Arnould, Gales, &

Kuhn, 2006; Orsini, 2004).

To calculate primary enclosure space requirements for pinnipeds (pool area

and dry resting area) set out by the United States Department of Agriculture

(USDA; 2007), the average adult length of the longest pinniped housed in the

enclosure is used. Adult male Australian Sea Lions reach lengths of at least

2.5 m, and females are 1.3–1.8 m in length (Goldsworthy & Gales, 2008).

AUSTRALIAN SEA LIONS AND

CAPTIVE ENVIRONMENTS

In captivity, little is known about their behavior. Coupled with lack of a com-

prehensive ethogram for free-living counterparts, this makes it more difficult to

assess captive welfare using behavioral measures—whether behavioral diversity

is maintained in captivity or whether behavior is abnormal (not common in

counterparts in the wild).

Current captive environments for sea lions include high levels of human

contact, limited access to large areas of water, lack of opportunities for social

interaction and foraging, controlled diets, and predictable feeding schedules.

Such inadequacies may lead to stereotypic behaviors, usually invariant, highly

repetitive, and with no obvious immediate functional value (Mason, 1991),

which may indicate poor welfare (Mason & Latham, 2004) and reduce the

overall visitor experience (McPhee, Foster, Sevenich, & Saunders, 1998; Tofield,

Coll, Vyle, & Bolstad, 2003). Investigating factors linked to optimal well being

in pinnipeds is vital because husbandry practices affect their survival rates in

captivity (Roberts & DeMaster, 2001).

Stereotypic Behavior in Captive Seals and Sea Lions

Stereotypies for seals and sea lions typically take the form of pattern or circu-

lar swimming, observed in captive Harbor Seals, Harp Seals, and Gray Seals

(Hunter, Bay, Martin, & Hatfield, 2002); Common Seals (Grindrod & Cleaver,

2001); Southern Fur Seals (Dow, Bode, Lailey, Gibbs, & Jenkins, 2001); Cali-

fornian Sea Lions and Atlantic Harbor Seals (Corson, Michel, & Zaks, 2004);

and Stellar Sea Lions (Kastelein & Wiepkema, 1988). Pinnipeds potentially

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CAPTIVE AUSTRALIAN SEA LIONS 105

experience more negative effects of captivity than do other mammals, with up

to 50% of their daily activity budget spent in stereotypic “fixations” (Swaisgood

& Shepherdson, 2005), leading to controversy about keeping them in captive

environments (Roberts & DeMaster, 2001). Other examples of aberrant behaviors

in captive pinnipeds include self-directed behaviors (flipper chewing, excessive

self-grooming or scratching); repetitive movements in water (“barrel rolling”

at the surface); and polydipsia or excessive drinking of pool water (personal

observations by Bradley P. Smith, June 1, 2006).

Enrichment for Captive Seals and Sea Lions

In an attempt to minimize stereotypic swimming in captive seals and sea lions,

environmental enrichment techniques providing new opportunities and choices

have been used (Swaisgood & Shepherdson, 2005). Enrichment includes pro-

vision of natural items such as driftwood, kelp, large beaches, and pools) and

artificial items such as balls, Frisbees, and food-treat balls (Wassel, McMann,

Phillips, Demark, & Kopf, 1996); training (Kastelein & Wiepkema, 1988); and

simulated prey chase (Morris, 1960). Evidence for success of enrichment objects

and techniques is largely anecdotal, often through keeper observation alone. Of

the few empirical studies that exist to date, the most effective techniques in

reducing pattern swimming in pinnipeds have been the following:

1. Frozen in blocks of ice for Californian Sea Lions and an Atlantic Harbor

Seals (Corson et al., 2004);

2. An air compressor with weighted soaker hose combined with fish “tossed

into pool” for Harbor Seals, Harp Seals, and Gray Seals (Hunter et al.,

2002; and

3. A simulated prey-chase technique involving a fish tied to a fishing rod

being quickly pulled across the pool for Common Seals (Grindrod &

Cleaver, 2001).

These empirical studies are beset with methodological limitations or weaknesses,

including the following:

1. Use of multiple observers without interobserver reliability checks (Corson

et al., 2004; Hunter et al., 2002);

2. Data collection over long periods of time, >12-month period (Hunter et al.,

2002);

3. Increasing the risk of extraneous variables intervening (Grindrod & Cleaver,

2001);

4. Brief observation sessions conducted at random times over the day, 20 min

in length (Corson et al., 2004; Hunter et al., 2002); and

5. Absence of baseline phase (Corson et al., 2004).

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In some cases, animals are housed in comparatively large exhibits >150,000 L in

volume (Grindrod & Cleaver, 2001), with multiple species (Hunter et al., 2002)

potentially enriching environments, which is not taken into account. Ideally,

empirical studies should provide detailed descriptions of the topography or

form of any stereotypic behavior observed, which has not been done for pattern

swimming. Whether pattern is circle or figure eight, direction is clockwise or

anticlockwise.

Ecological Learning Theory for Assessing Effectivenessof Enrichment

Learning Theory, taking ecological factors into account, provides a theoretical

framework for experimental design and assessment of enrichment effectiveness

(items, techniques, or mechanical devices) by measuring behavior change (Tim-

berlake, 1993; Zeiler, 1992). Relevant principles of learning theory to be consid-

ered include intrinsic and extrinsic reinforcement, habituation, and extinction.

Tarou and Bashaw (2007) cover this in detail.

Enrichment techniques utilize either intrinisic or extrinsic reinforcers or re-

wards, both of which increase the likelihood of behavior occurring again. In-

trinsic reinforcement occurs when simply performing a behavior is rewarding

(exploration, play, hunting, nest building, and even stereotypic behavior); extrin-

sic reinforcement occurs when performance of behavior results in a rewarding

consequence (food) external to the behavior (Hughes, 1997; Tarou & Bashaw,

2007). Extrinsically reinforcing enrichment techniques are often food related.

Because the reinforcer does not last indefinitely (food runs out), behavior is

maintained only when the reinforcer is present (Tarou & Bashaw, 2007).

Food-related objects are also intrinsically reinforcing initially when they are

novel. For extrinsic reinforcers, a decrease in responding is more likely to result

from extinction (reinforcement is no longer provided for a behavior that was

previously reinforced) than habituation. As a result of “spontaneous recovery,”

when the object is replenished with food, levels of response will again increase.

A need exists for development of effective enrichment items that are not food

related. A careful balance must be met between type of enrichment items and

how often they should be presented. Comprehensive analysis of behavior over

several days while an object is in the enclosure is vital to show when habituation

begins to take effect. This could potentially help determine the ultimate time to

withdraw objects, at a point before animals have become habituated to them,

thus retaining some novelty.

Aims of This Study

In summary, this empirical case study aimed to do the following:

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1. Provide an in-depth and systematic analysis of the behavior (activity

budget) of two Australian Sea Lions, housed together in a small zoo

exhibit, including description of topography or form of stereotypic pattern

swimming;

2. Evaluate effectiveness of enrichment objects by testing whether provision

of these objects resulted in increases in active “healthy” behaviors and de-

creases in stereotypic pattern swimming compared with baseline sessions;

and

3. Investigate effect of time of day and day of introduction of object on

object-directed behavior (habituation and/or extinction effects).

METHODS

Data were collected on a breeding pair of Australian Sea Lions (Neophoca

cinerea) housed together when on display at Adelaide Zoo, Australia. The male,

Birri, was 9 years old and 220 kg in weight. He was wild-born, rescued from

Goolwa at 3–6 months of age, and hand-reared at Adelaide Zoo (Ling & Guy,

2007). The female, Shara, was 9 years old and 75 kg in weight. She was captive-

born and raised at Adelaide Zoo. Their exhibit, built in 1988, contained a 60,000-

L pool (1.05 m max depth � 12 m max length � 6.4 m max width, filled

with moderately saline water of �8,000 ppm), haul-out sites, and a beach area

(Figure 1).

FIGURE 1 Map and dimensions of the sea lion enclosure at the Adelaide Zoo (not to

scale).

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At the shallow end, the sea lions could walk around, and the small size of the

pool did not allow Birri to engage in natural swimming patterns (pushing off, full

strokes through the water, or gliding). They were fed three times daily: (a) when

they moved into their enclosure in the morning (0800 hr); (b) during a public

feeding session (1145 hr); and (c) in their separate off-exhibit night enclosures

(1630 hr). At night, Birri was housed in the Night Den area and Shara was

housed with her mother, Doc, in the Maternity area (Figure 1). Access to water

was given overnight for approximately 2 hr.

An ethogram was developed, combining behavioral categories used by Hunter

et al. (2002) and behaviors recorded during ad libitum observation sessions at

Adelaide Zoo (Table 1). Never-observed behaviors were discarded from the

ethogram (aggression, breeding displays or breeding behavior, out-of-sight).

Individual behavioral categories considered inactive (resting in water, resting

hauled out, maintenance) were grouped together for analysis as were behavioral

categories considered active (random swimming, interaction with conspecific,

interaction with keeper, exploration, play, locomotion on land, and enrichment-

object-directed behaviors). Only pattern swimming was considered stereotypic

behavior.

The enrichment objects used were designed specifically for, and tested for

use with, sea lions and were commercially available (Figure 2) and novel to

Birri and Shara. A scratchy “bristle brush” was permanently fixed to a wall. The

non-food-related object or intrinsic reinforcer (Seal Thong Ball) was a small

rubber ball with rubber spikes (150-mm diameter) with an attached thong. The

food-related object or extrinsic reinforcer (Seal Tucker Ball) was a hard, plastic,

hollow ball (250-mm diameter) with a hole in it (5-cm diameter). Sea lions

could retrieve fish from the Seal Tucker Ball by nosing at the ball and rolling

it around until the fish fell through the hole or enough of a fish poked out of

FIGURE 2 The Seal Thong Ball (non-food-related) and Seal Tucker Ball (food-related)

enrichment objects.

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TABLE 1

Ethogram and Operational Definitions for Australian Sea Lion Behavior

Behavior

Category Description

Pattern

swimming

Swimming in a repetitive tight circle pattern (clockwise or anticlockwise),

never including figure eight pattern but sometimes including full rotations

or twists of the body.

Random

swimming

Swimming other than pattern swimming and also excluding swimming that

forms part of the other behavioral categories as listed later.

Interaction

with

conspecific

Any contact between the sea lions or any behavior directed toward another

sea lion. Includes holding any part of the other sea lion’s body using

mouth or fore flippers, nosing (touching other sea lion with the nose),

following, mouthing (open-mouth biting or “gumming” each other

simultaneously), and synchronized swimming.

Resting in

water

Inactive while in the water; includes lying under rocks, floating/drifting/

bobbing, and lying on bottom of pool.

Resting hauled

out

Any inactivity on land; includes sitting upright on fore flippers with the

neck or head pointed vertically, and also includes sitting or lying down

on stomach or side while looking around.

Locomotion

on land

Walking or running on land.

Maintenance Grooming activities directed at self (e.g., rubbing on rocks and scratching

body with fore flippers).

Exploration/Play Exploration or investigation of parts of the enclosure (in or out of water),

such as the rock wall, under rocks and pool filter. Also includes behavior

(play or exploratory) directed at objects that are not enrichment items,

such as bark or small stones.

Interaction

with

keeper

Includes looking at keeper, following keeper, being spoken to or touched by

keeper, being fed by keeper or eating while keeper is in enclosure, having

body inspected by keeper and waiting at enclosure door (prior to door

being opened by keeper trying to leave enclosure). This category

excludes any behavior directed at enrichment objects even if keeper is

present (see “enrichment interaction” category).

Enrichment-

object-

directed

behaviors

Touching and interacting with object using any part of the body but in

particular, mouth, nose, neck, and flippers. For the non-food-related

object, this includes tossing or throwing of the ball. For the food-related

object, this includes pulling fish out of the object and consuming fish

taken out of the enrichment ball. Also includes behavior directed at the

objects by both sea lions simultaneously.

the hole for the sea lions to pull it out. Two identical objects were placed in the

enclosure to prevent competition for the objects and possible aggression.

Birri and Shara were observed by a single researcher (Bradley P. Smith) over a

continuous 30-day period using a single-subject ABABA (reversal) experimental

design (Saudargas & Drummer, 1996; Sealander, 2004) as shown in Table 2.

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TABLE 2

Summary of the Experimental Design Used and Total Hours of Observation

Condition Procedure Time Total Hours of Observation

Initial baseline (A1) Observation only; noenrichment objects

14 days 14 � 6 hr per day D 84 hr

Experimental

treatment 1(B1)

Experimental condition 1;

2 non-food-relatedenrichment objects presentin enclosure


Baseline (A2) Observation only; noenrichment objects


Experimental

treatment 2(B2)

Experimental condition 2;

2 food-related enrichmentobjects present in enclosure


Baseline (A3) Observation only; noenrichment objects


Observations were made during three 2-hr sessions per day (0830–1030,

1100–1300, 1430–1630 hr) to investigate possible time-of-day effects (incorpo-

rating husbandry activities such as feeding or placing animals in/out of night

enclosure). Observations were recorded using instantaneous scan sampling of

behavior and location at 2-min intervals. A total of 180 hr of observations was

recorded.

Apart from keepers introducing experimental enrichment objects, no changes

were made to the sea lions’ routine, and no other enrichment objects were

provided during the study. Seal Thong Balls were introduced at the start of each

day and withdrawn when Birri and Shara were moved into off-exhibit night

areas. Seal Tucker Balls were three quarters filled with 1 kg of fish (from daily

food allowance) and placed in the enclosure at the start of each day. They were

refilled with a further 1 kg of fish during the public feeding session (1145 hr).

On Day 1, pieces of fish were used, but Birri showed little interest, and water

quality was negatively affected (oily film on pool surface and fish remains on

pool floor). On subsequent days, whole fish (�15 cm in length) were placed in

the balls. Tommy Roughs (Arripus georgianus) and Trumpeter Whiting (Sillago

maculata) were used in a ratio of 3:1, reflecting the sea lions’ food preferences.

Mindful of methodological issues associated with single-case designs (low

power, low degrees of freedom, and increased possibility of making Type II

errors), this study used percentage of total scans spent engaged in each behavior

to identify behavior change (Kuhar, 2006; Saudargas & Drummer, 1996). Be-

havioral analysis was made primarily by visual inspection of graphs, a technique

used to assess the effectiveness of behavioral intervention, often used for single-

case experiments (Brossart, Parker, Olson, & Mahadevan, 2006; Kazdin, 1982;

Martin & Pear, 2003; Saudargas & Drummer, 1996).

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RESULTS

Activity Budget Prior to Enrichment (Initial Baseline)

During the initial baseline phase, pattern swimming was identified in Birri’s

behavioral repertoire, with about 45% of total scans spent engaged in this

stereotypic behavior (Table 3). Shara, by contrast, displayed negligible amounts

of stereotypic behavior, instead spending a comparable amount of time (45%)

engaged in random swimming. Birri spent far less time random swimming

(about 19%). Birri and Shara spent about 15% of their time interacting with

each other. Shara also spent about 20% of her time resting on land, whereas

Birri spent less time resting on land (5.5%) and more time resting in the water

(8.4%).

Topography or Form of Stereotypic Pattern Swimming

Throughout the study, Birri’s pattern swimming followed a circular pattern in

an anticlockwise direction (Figure 3). During baseline sessions, he spent about

a third of his time engaged in this behavior during the morning (33%; <10%

during treatment conditions) and midday sessions (38%; <15% during treatment

conditions), typically in the southern end of the pool (right side). At this, the

deeper end of the pool, his pattern often included two full rotations or twists

of his body at the western side of the pool. In the afternoon baseline sessions,

he spent about 58% of his time pattern swimming (<30% during treatment

conditions) with individual bout durations of up to 90 min. For these sessions,

his pattern swimming tended to take place in the northern end of the pool (left

side), following a much tighter circle. Shara engaged in negligible amounts of

pattern swimming.

Effects of Enrichment Objects on Individual Categories

of Behavior

The introduction of enrichment objects appeared to have a large effect on Birri’s

pattern swimming (Table 3), decreasing noticeably by almost 30% (B1 compared

with A1 & B2 compared with A2). For both Birri and Shara, level of random

swimming was highest during initial baseline, slightly lower when objects were

present, and lowest after non-food-related objects were removed (A2).

More than a third of their time (>37% for both) was spent interacting with the

non-food object. The figure was much lower for the food-related object (about

23% for Birri and 5% for Shara), which Birri monopolized and Shara only used

when he was not nearby. Although more behavior was directed toward the non-

food-related objects than food-related objects, levels of pattern swimming were

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TABLE 3

Mean Percentage of Scans Spent Engaged in Each Behavioral Category

for Each Phase of the Study for Birri and Shara

Experimental Condition

Animal Behavior

Baseline

A1

Treatment 1

(B1;

Non-Food

Object)

Baseline

A2

Treatment 2

(B2;

Food

Object)

Baseline

A3

Birri Individual categories

Stereotypic

Pattern swimming 45.17 17.24 37.17 9.49 40.33

Active

Swimming (random) 19.21 16.09 9.83 14.61 12.11

Interacting (conspecific) 16.39 3.83a 25.57 23.72a 22.26

Locomotion (land) 0.16 — — — —

Exploration/Play 1.84 2.30 1.40 0.76 1.03

Keeper interaction 2.67 3.64 2.95 3.61 2.65

Enrichment-object-

directed behavior

— 42.72 — 23.34 —

Inactive

Resting (water) 8.40 8.24 6.17 12.33 9.96

Resting (hauled out) 5.54 5.36 16.60 11.20 11.64

Maintenance 0.60 0.57 0.28 0.96 —

Combined categories

Stereotypic 45.17 17.24 37.17 9.49 40.33

Active 40.27 68.58 39.75 66.04 38.05

Inactive 14.54 14.17 23.05 24.49 21.60

Shara Individual categories

Stereotypic

Pattern swimming 1.41 — 0.55 — 0.28

Active

Swimming (random) 45.55 37.19 30.38 36.38 36.04

Interacting (conspecific) 15.06 3.80a 25.32 22.94a 22.15

Locomotion (land) 0.20 — — — —

Exploration/Play 7.28 3.22 7.12 5.43 3.87

Keeper interaction 2.60 2.28 2.09 3.82 1.79

Enrichment-object-

directed behavior

— 37.34 — 5.39 —

Inactive

Resting (water) 2.28 1.33 0.97 2.99 3.02

Resting (hauled out) 25.35 14.82 33.12 23.03 32.60

Maintenance 0.24 — 0.41 — 0.28

Combined categories

Stereotypic 1.41 — 0.55 — 0.28

Active 70.69 83.83 64.91 73.96 63.85

Inactive 27.87 16.15 34.50 26.02 35.90

aWhen both animals were interacting with enrichment object, behavior was coded as interaction

with object, thus, this number is artificially low.

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FIGURE 3 Locations and direction of pattern swimming in main pool for Birri during all

phases of the study, including a diagrammatic representation of Birri that is roughly to scale.

also higher when non-food objects were present. Shara used the non-food-related

object only when interacting with Birri, whereas Birri also engaged in solitary

play with the object.

Birri and Shara spent substantially fewer scans interacting with each other

when non-food-related objects were present and more when food-related objects

were present compared with baseline sessions. Because conspecific interaction

involving use of objects was recorded as enrichment-directed behavior, this figure

is likely to be an underestimate. Indeed, Shara only used the non-food-related

object with Birri during social play. Interacting with conspecific (>20% for

both sea lions) and resting on land (>11% for Birri & >23% for Shara) were

higher following withdrawal of non-food-related objects and remained high for

subsequent phases (Table 3).

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Effects of Enrichment on Combined Behavioral Categories

(Active, Inactive, and Stereotypic)

By condensing individual behaviors into three categories (active, inactive, &

stereotypic), more obvious behavioral effects of enrichment emerge. For Birri,

introduction of enrichment objects increased active behavior by almost 30% and

concurrently decreased stereotypic behavior by a similar amount (Figure 4).

Whereas during baseline sessions, stereotypic behavior occurred in amounts

similar to active behavior (around 40%), when objects were present, active be-

havior prevailed. For these two behavioral categories, withdrawal of enrichment

objects resulted in a return to baseline levels, indicating that introduction of

objects alone caused observed changes in these behaviors. That is, behavior

change can be attributed to experimental treatment (introduction of enrichment

objects). The same cannot be said for inactive behavior, which for Birri remained

relatively unchanged when non-food objects were present, increased by about 9%

when they were withdrawn, and then remained at a similar level for subsequent

phases of the study.

For Shara, negligible amounts of stereotypic behavior were recorded during

any baseline phase and absent when objects were present (Figure 4). Introduction

of enrichment objects increased active behavior (about 10%), which was already

high for her in baseline phases (>64%). Inactive behavior decreased when

enrichment objects were present but remained slightly higher than initial baseline

level when objects were withdrawn. Thus, although behavior change was not

as dramatic as for Birri, changes in stereotypic behavior, active behavior, and

inactive behavior for Shara can also be attributed to experimental treatment

(introduction of enrichment objects).

Friedman’s test was used to evaluate differences in activity, inactivity, and

stereotypic pattern swimming over the five phases of the study (three baselines,

Treatment 1 and Treatment 2) for both sea lions. Although visual trends

exist (Figure 4), no significant differences were detected using a statistical

significance criterion of p < .05. For example, active behavior increased and

stereotypic pattern swimming decreased noticeably; however, this difference

was not statistically significant (p D .166 and p D .166, respectively).

Nonetheless, visual inspection of Figure 4 highlights the trends, providing useful

information.

Effects of Day of Introduction of Object and Time of Day

on Object-Directed Behavior

Both non-food-related and food-related objects were present in the enclosure for

3 full days, during all three observation sessions for each of these days.

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FIGURE 4 Percentage of scans spent engaged in three “combined” behavioral categories

(active, inactive, & stereotypic) for Birri (top) and Shara (bottom) for each phase of the

study.

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FIGURE 5 Percentage of scans spent engaged in behavior directed at non-food-related

objects and food-related objects over the 3 days when objects were present (Birri, left &

Shara, right).

Day of introduction of object. Birri spent almost 60% of scans interacting

with non-food objects on Day 1, with a steady decline in this behavior (>15%

per day) over the following 2 days (Figure 5). Although Birri spent more than

40% of scans interacting with food objects on Day 1, this was noticeably less

time than he spent interacting with the non-food-related items for the same day.

For the food-related object, there was a marked decline in use after Day 1, with

less than 10% of scans spent interacting with food-related objects on Day 3.

These trends were similar for Shara, but she directed noticeably more behavior

at the non-food-related objects than the food-related objects on any day, barely

interacting with the food-related objects after Day 1. Birri monopolized the

food-related object on all days, whereas both sea lions spent similar amounts of

time interacting with the non-food-related objects after Day 1.

Time of day. When objects were first encountered, in Session 1 on Day 1,

Birri spent most of his time interacting with them—twice as much time as

Shara (Figure 6). By Session 3 of Day 1, both sea lions directed about 80%

of their time toward the non-food-related objects, whereas the food-related item

was essentially ignored. With respect to the non-food-related objects, both sea

lions continued to interact with them for considerable amounts of time (>30%)

during the first two sessions of Day 2 and Day 3. Interest in these objects dropped

noticeably later in the day on Day 2, and the objects were completely ignored by

the final session of Day 3. With respect to the food-related objects, after the 1st

day, Shara spent negligible amounts of time interacting with the objects. Birri

continued to spend time engaged in object-directed behavior during Session 1

and Session 2 (between 9% & 23%) on the final 2 days but largely ignored them

in the final session on these days.

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DISCUSSION

This case study provides a comprehensive analysis of captive Australian Sea

Lion behavior during baseline and subsequent enrichment-object phases. Overall,

the introduction of enrichment objects had a positive impact on behavior. Both

intrinsic and extrinsic objects decreased Birri’s stereotypic pattern swimming,

increased active behavior for both Birri and Shara, and decreased Shara’s inactive

behavior.

Activity Budget Prior to Enrichment (Initial Baseline)

The activity budgets of the two sea lions differed greatly prior to enrichment.

Birri spent the majority of his time pattern swimming (>45%), resembling

circular pattern swimming described by Grindrod and Cleaver (2001). He also

showed a directional preference (lateralized swimming behavior) like captive

California sea lions (Wells, Irwin, & Hepper, 2006).

With a dive depth of less than 1 m, too shallow according to depth re-

quirements set by the USDA (2007), the pool was spatially restrictive for an

adult male Australian Sea Lion. The kidney-shaped pool was approximately

four times his length at the longest point and twice his length at the widest

point (Figure 3). Birri was unable to perform natural swimming patterns that

include pushing off, full strokes through the water, or gliding. Future studies

are needed to determine whether circular swimming in sea lions occurs only

in smaller pools, and figure eight or other patterns in larger pools (personal

observation) or whether differences reflect preferences of individual sea lions.

Improved reporting of pattern swimming or of any stereotypic behavior observed,

including details of topography or form of the behavior (not just percentage of

time spent engaged in the behavior), may contribute to understanding these

potential behavioral indicators of stress.

Shara seemed less affected by captivity, exhibiting greater behavioral diversity

(random swimming, resting on land, and interacting with Birri), with no evidence

of stereotypic behavior. Shara was smaller than Birri, mother-reared (Birri was

hand-reared from the age of 3–6 months), and had never known any environment

other than this enclosure (Birri was wild-born). Future studies are required

to address potential gender differences and rearing history or other individual

differences in responses to captivity.

Free-living Australian Sea Lions (a) gather in large groups at breeding colonies

and haul-out sites (McKenzie, Goldsworthy, Shaughnessy, & McIntosh, 2005);

(b) exert great effort in foraging at depths of more than 40 m; and (c) haul

out in complex and varied terrestrial habitats, none of which were possible

in this enclosure. Despite this, no other forms of stereotypic behavior were

observed. Therefore, if stereotypic behavior alone is used as a measure of

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stress or compromised welfare, it cannot be concluded that the small size of

the primary enclosure (pool area and dry resting area) is necessarily suboptimal

for all Australian Sea Lions. The findings suggest that this enclosure was less

than optimal for Birri but adequate for Shara, which may reflect inadequate

space requirements for the pool area for housing adult male Australian Sea

Lions (based on standards set by the USDA, 2007).

Effects of Enrichment Objects on Individual and Combined

Categories of Behavior

This study shows that simply providing objects effectively reduces pattern swim-

ming and increases active behavior. The non-food-related object appeared to

act as both an intrinsic reinforcer, its motivation explained by the “optimal

arousal theory” (Hughes, 1997), and as an extrinsic reinforcer (created affiliative

interactions between the sea lions). Non-food-related objects therefore act as

effective low-cost, low-maintenance enrichment devices.

As predicted, the food-related object reduced Birri’s pattern swimming and

contributed to an increase in Shara’s active behavior. However, Birri monopo-

lized use of both balls when they contained fish and rarely shared them with

Shara. Thus, provision of two identical enrichment objects does not necessarily

allow a submissive sea lion access to either of the objects. The submissive animal

may need to receive enrichment objects separately (off exhibit after hours), or

more than two objects should be provided.

Effects of Day of Introduction and Time of Day on

Object-Directed Behavior

Use of the food-related objects decreased rapidly over both days and sessions

within days, not, however, as a result of habituation to the objects, because the

Seal Tucker balls were highly effective when they contained food. The balls

were emptied more rapidly over time, indicating an effect of learning, as Birri

in particular became more proficient at removing fish. These balls were utilized

as food dispensers rather than play items with short-term extinction taking place

once the balls were emptied of fish. The balls provided a short-term predictable

source of food for the sea lions with little resistance to extinction; it was obvious

by looking through the large holes when the balls were empty of food. Tarou

and Bashaw (2007) provide a summary of learning theory and enrichment.

For Birri, the balls were both extrinsically reinforcing (when full of fish) and

intrinsically reinforcing (when empty). Occasionally, he removed and dropped

fish; Shara was able to eat them. For Shara, however, these balls were largely

intrinsically reinforcing and reduction in behaviors directed toward them reflects

habituation.

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Unlike the food-related objects, the percentage of time spent interacting with

the non-food-related objects showed only a slight decline in use over the 3 days

and a decline in use over sessions for the last 2 days. However, Birri and Shara

ignored the Seal Thong balls during Session 3 of Day 3. This may indicate

a habituation effect, suggesting that, to retain novelty, these non-food-related

objects should not receive a full 3 days of use. In order for enrichment to be

most effective (decrease habituation effect), a large number of objects should be

continually rotated or used for short periods (thereby allowing objects to regain

novelty).

CONCLUSION

To generalize these findings, similar studies of other captive Australian Sea

Lions are needed. Empirical case studies of enrichment for captive pinnipeds

should be encouraged. Many zoos and aquaria house low numbers of any one

species, publish little information on enrichment, and are financially unable to

provide enclosures approaching the space and complexity of natural pinniped

aquatic and terrestrial environments.

This article highlights the importance of evaluating other intrinsic non-food-

related enrichment objects as well as different methods of food delivery. The

effects of husbandry routines, enclosure and pool size, water quality, and level

of interaction with humans on anticipatory or stereotypic behavior of captive

Australian Sea Lions is still to be determined. The findings of this article

also highlight the need for legislated minimum standards for primary enclosure

space requirements for pinnipeds, particularly large adult males. In countries

such as Australia, where no such legislated national standards exist, the readily

accessible standards set out by the USDA (2007) could be used.

ACKNOWLEDGMENTS

We thank the staff at ZoosSA, particularly at Adelaide Zoo, for their enthusiastic

support of the project, as well as Joe Parsons at AussieDog for providing

enrichment objects. Thanks also to Professor Tony Winefield and Joanne Davis

for critical comments on the article. This experiment received animal ethics

approval from the Institute of Medical and Veterinary Sciences (South Australia;

Project 60/06) and complies with the current laws of Australia. This article is

dedicated to Birri, Shara, and Doc, who have all died since this study was

completed.

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Documents

An Empirical Case Study Examining Effectiveness of Environmental Enrichment in Two Captive Australian Sea Lions ( Neophoca cinerea )