Contribution to the welfare of captive wolves (Canis lupus lupus): A behavioral comparison of six wolf packs

Contribution to the Welfare ofCaptive Wolves (Canis lupus lupus):A Behavioral Comparisonof Six Wolf PacksAnne Frezard1* and Gilles Le Pape2

1Parc Animalier de Ste Croix, Rhodes, France2Laboratoire d’Ethologie, Faculte des Sciences et Techniques, Parc de Grandmont,Tours, France

An interesting way to understand and eventually improve the well-being ofcaptive animals is to compare different living and social conditions, in order toanalyze the behavioral differences between animals living in very restrictiveconditions and animals enjoying more permissive ones. In the present study weperformed 10 observations of six wolf enclosures with quite different living andsocial conditions. The rest/activity balance, behavioral diversity, and use ofavailable space were used as welfare criteria. Results show that the proportion oftime resting was higher in large, comfortable enclosures. In each park, animalsused only a part of the available space, the proportion being lower in largeenclosures. The behavioral diversity was little affected by the size of the enclosure,but highly related to the composition of the pack. The results underline theimportance of spatial choice and social group management. Zoo Biol 22:33–44,2003 �c 2003 Wiley-Liss, Inc.

Key words: activity; space use; psychoethology

INTRODUCTION

Humans account for a large part of the environment of zoo animals [Robinson,1998]. Even if they are born in captivity, these animals are not domesticated.Although animal keepers enter the enclosures to supply food, catch animals, or cleancages, nondomestic animals are generally afraid of humans. In addition, enclosurescan be too small and unsuitable for the animals’ needs. Increasingly, enrichment

nCorrespondence to: Anne Frezard, Parc Animalier de Ste Croix, 57810 Rhodes, France. E-mail:

[email protected]

Received for publication March 19, 2002; Accepted July 16, 2002.

DOI: 10.1002/zoo.10070

Published online in Wiley InterScience (www.interscience.wiley.com).

Zoo Biology 22:33–44 (2003)

�c 2003 Wiley-Liss, Inc.

programs are being established to make the animals’ environment more attractive,and to improve animal welfare and the education of visitors. Different types ofenrichment have been implemented, including hidden food in litter or boxes[Forthman et al., 1992; Hartmann, 1998; Kelly, 1993; Rehling, 2000; Winslow, 1992];introduction of objects [Steele and Charley-Johnson, 2000; Malone, 2000; Hediger,1954; de Monte et al., 1997; Gewalt, 1992; Korhonen and Niemela, 1994; Carlstead,1991; Hannier, 1995]; and management of groups and social relationships [Warrick,2000; O’Neill, 1997]. Different criteria are used to measure animal welfare, such asrest/activity balance, amount of stereotypic and other abnormal behaviors, andbehavioral diversity [Dawkins, 1990; O’Neill, 1994; Mason, 1991; Veasey et al., 1996;Wemelsfelder, 1993; Wiepkema, 1983].

The functionalist approach analyzes behavior in terms of adaptive function. Inthis approach, environment is considered as objective and is built without much regardfor the animal. In a constructivist approach, as suggested by Von Uexkull [1956], weassume that the animal lives in a subjective world (Umwelt). This point of view hasbeen developed and enhanced by Varela et al. [1993], who suggested that animals livein a world of significations: the different parts of an animal’s territory are matched tosignifications related to the actions expressed at these places. An affordance, theexpectation of what can be done at a given place, can be associated to each part of theterritory. More recently, Dubois et al. [2000], Gallo and de Gaulejac [1999], and deGaulejac et al. [1997] illustrated the efficiency of this theory. They showed a strong linkbetween the different parts of the enclosure of captive animals and the animals’performance in exploration tasks at different places. Moreover, an object can take ondifferent meanings depending on where it is discovered by the animal. This way oflooking at animals as subjects giving meaning to their environment by their actionswas termed ‘‘psychoethology’’ by de Gaulejac et al. [1997].

Generally, the subjective perceptual world of the animals is not studied beforeenrichment. Most previous studies of zoo animal welfare were performed onprimates [e.g., Marriner and Drickamer, 1994], and on carnivores such as bears[Forthman et al., 1992; Van Keulen-Kromhout, 1978; Wechsler, 1991; Winslow,1992], fennec foxes [Carlstead, 1991], European wildcats [Hartmann, 1998], andspecies with reproductive problems. The animal’s perception of its subjectiveenvironment was not of concern in any of these studies. The wolf is very attractivefor visitors in Europe and has a very good reproduction rate in captivity, which isprobably why it is a very common species in European zoos. Nevertheless, itsconditions in captivity are very heterogeneous. Various studies have been performedon the social behavior of captive wolves [Fentress et al., 1987; Fox et al., 1974;Lockwood, 1979; Rabb et al., 1967; Schenkel, 1967; Zimen, 1982] and theirphysiology [Asa et al., 1990; Asa, 1997]. Mech [1970, 1999] studied the socialbehavior of wolves in the wild. No studies were concerned with improving thewelfare of captive wolves. The aim of this study was to understand the needs of acaptive wolf pack, using a psychoethological approach.

ANIMALS AND METHODS

Wolves were observed in six French parks: la Bisonnerie (Bi), la Bourbansais(Bo), la Haute Touche (Ht), le Refuge de l’Arche (Ra), Pescheray (Pe), and Rhodes(Rh). The characteristics of the enclosures are described in Table 1.

34 Frezard and Le Pape

Two packs were studied several times:

1. Pescheray: One observation (Pe1) with only three females, two observations(Pe2 and Pe3) after the introduction of two males, and one observation(Pe4) 1 year after the introduction, with two remaining females and bothmales.

2. Rhodes: Two observations (Rh1 and Rh2) at a 3-month interval, with thesame number of animals. In the second session, wolves were notindividualized.

Observation Method

A scan was realized every 2 min during several hours per day for several days.The details of each observation period are given in Table 1. Activity and location ofthe activity were recorded at each scan for each subject.

Most observations were made by the same person. When a different personwas required, because of the large number of wolves in a pack, he or she was trainedby the principal observer until a 95% correlation between them was reached.

Behavioral Items

Seventeen groups of activities were observed (see descriptions in Table 2).

Regions

In each park, virtual regions were established before the beginning of the firstobservation, before the habits of the wolves were known. The different regions of agiven park were of approximately the same size.

Data Analysis

Because only six parks were studied, only descriptive statistics were used. Inorder to classify the different regions of the enclosure according to the total amountof activity, thresholds of low and high occupation were determined using the w2

probability distribution. Cross tables of parks and frequencies of activities weredescribed by multifactorial correspondence analysis (MCA). This technique is a kind

TABLE 1. Description of the enclosures and periods of observation

Parks

Surfacearea(m2) Vegetation Soil

No.of

wolvesObservationduration

Observationdates

Bi 1,000 Poor Earth+grass 7 4 h per day 3 days in FebruaryBo 160 No Concrete 3 4 h per day 3 days in NovemberHt 1,000 Good Earth+grass 11 6 h per day 2 days in MayRa 2,800 Good Earth 12 4 h per day 3 days in JanuaryPe1 2,500 Good Earth+grass 3 4 h per day 2 days in MarchPe2 2,500 Good Earth+grass 5 4 h per day 2 days in AprilPe3 2,500 Good Earth+grass 5 4 h per day 2 days in AprilPe4 2,500 Good Earth+grass 4 4 h per day 2 days in MarchRh1 10,000 Good Earth+grass 15 4 h per day 3 days in MarchRh2 10,000 Good Earth+grass 15 2 h per day 18 days in May/June

Comparison of Six Wolf Packs 35

of principal component analysis (PCA), but uses a relative w2 criterion to showdifferences and similarities between qualitative variables [Lebart et al., 1984]. Thisavoids possible artifacts due to differences related to the duration of observationsand to the size of the packs. Before the analysis was performed, the overallheterogeneity of the table was checked by a w2 test. In the same way, in a given park,cross tables of activities and regions allowed the analysis of relationships betweenactivities and regions.

Activities and regions can be linked in two ways: either a given activity occursin most cases at the same place, or a given region is highly specialized for a particularactivity. For the first case, the percentage of each activity concentrated in less than20% of the available area was calculated. For the second case, a region is calledspecialized if only one particular activity represents more than 75% of all activitiesoccurring in this region. Both cutoff percentages were arbitrary.

RESULTS

Rest/Activity Balance

Seasonal effects

The amount of ‘‘resting’’ was the sum of time spent sleeping and lying. Allother behaviors were classified as ‘‘activity.’’ The proportion of time spent resting

TABLE 2. Description of the behavioral items

Behavioral item Description

Sitting The animal is sitting motionless or looking aroundMotionless The animal is standing motionlessLying Lying, lying on the back, lying on an other individual with open

eyesSleeping Lying motionless with closed eyesLocomotion Straighting up on a tree, straighting up on the fence, straighting

up on a stump, galloping, walking, toddling, carrying a branch,carrying a piece of meat

Self directed Rubbing against a tree, the ground, licking paws, stretching,licking its own body

Sniffing the groundSocialþ Positive social behavior: straighting up on an individual, ano-

genital sniffing, ano-genital licking, sniffing another wolf, playing,licking another wolf, rubbing the muzzle against a wolf, rubbingthe muzzle one another, mating, nibbling ears, walk on a lyingwolf, leg on a wolf, wag its tail, head on a wolf

Social� Negative social behavior: agonistic behavior, biting, avoiding,flying, growling, chasing, showing one’s teeth, submission

Vocalization Barking, moaning, howlingStereotyped behavior Stereotyped walkDigging Digging, burying meatNutrition Sniffing meat, eating, biting vegetation, taking a piece of foodDrinkingDefecationUrination Urination with raised leg, urinationInvisible The observer can’t see the wolf


was less during the cold months (Fig. 1). However, a given park can show differentscores at the same season, and the lower scores were not characteristic of a particularpark. The smallest variability was obtained for Pescheray during the first period(Pe1), with only three females in the pack. Extremes values could not be calculatedfor the second observation at Rhodes (Rh2) because the wolves were notindividualized at this session.

Quality of the enclosures and resting

The six enclosures were ranked according to: 1) the surface area (ranging from1 (smallest) to 6 (largest); 2) vegetation (3¼good [trees and grass], 2¼poor [onlygrass], 1¼no vegetation); and 3) soil quality (3¼earth and grass, 2¼only earth,1¼concrete).

Visitor access to the enclosures and holding areas was the same in all parks,and this criterion was not used to rank the enclosures. Sun and shade were related tothe vegetation criteria.

The six enclosures were ranked according to the sum of ranks. For enclosureswith several observations, the different scores are indicated in Fig. 2. The twoenclosures with the best environment showed the highest proportions of resting.

Composition of the pack and resting

This could be studied only at Pescheray, where the composition changed twice(Table 3). No systematic effect was observed, perhaps because of interaction withseasonal effects.

Fig. 1. Seasonal effects on the rest/activity balance. For each observation period, thepercentage of total activity spent resting by the median wolf and the extreme subjects areindicated (except for the Rhodes pack in June). Observations with the same pattern are fromthe same parks.


Behavioral Diversity

Differences between parks

All categories of behavioral items were expressed in all parks. Differencesbetween parks were studied by removing very common items: eating, drinking,standing, resting, and locomotion in order to retain only items showing differencesbetween the packs. The table crossing parks in rows and activities in columns, withthe frequency of each activity in the cells, was described by MCA (Figure 3). Therelationship between rows and columns of the table was highly significant (w2¼2456,Po0.001).

The principal opposition was between ‘‘social+’’ and ‘‘social�’’, that is to say,between packs characterized by a ‘‘good’’ atmosphere (on the right in Fig. 3) andpacks with a ‘‘bad’’ atmosphere (on the left). Packs with a ‘‘bad’’ atmosphere were

Fig. 2. Quality of the enclosures and rest/activity balance. The percentage of total activityspent resting is noted. The six enclosures are ranked according to the sum of the ranks for thearea, the vegetation, and the ground quality, indicated in parentheses. For the enclosures withseveral observations, all scores are indicated.

TABLE 3. Effect of the pack composition on the percentage of ‘‘resting’’ observations at

Pescheray

Pack composition Resting percentage

3 adult females 47%3 adult females+2 adult males 68%3 adult females+2 adult males 53%2 adult females+2 adult males 24%


characterized by introductions of adult wolves from other packs (Ra) or wolves bredby humans (Ra and Bi). Because the three females of the Pe1 observation had a verypoor behavioral repertoire, only urination characterized this case. Vocalizationwas associated with ‘‘social+.’’ Sitting, sniffing the ground, and self-directedbehaviors did not contribute to the differentiation of the packs and the differentobservations. The biggest dots have the main responsibility for distances along eachfactor.

Seasonal effect on behavioral diversity

No seasonal effect was seen in connection with behavioral diversity (Fig. 3).

Effects of enclosure quality on behavioral diversity

There was no relationship between the quality of the enclosures and behavioraldiversity: the ‘‘worst’’ park (Bo¼rank 1) and the ‘‘best’’ one (Rh¼rank 6) are veryclose in Fig. 3.

Effects of pack composition on behavioral diversity (Pescheray, Fig. 4)

The same analysis was performed with only the four observations at Pescheray,the only park in which composition changed during the observations. Therelationship between rows and columns of the table was again highly significant(w2¼310, Po0.001).

The first observation (Pe1), with only three females that had lived together foryears, was characterized by a lack of social behaviors. Observations Pe2 and Pe3

Fig. 3. Behavioral differences between parks. Description by MCA of the table crossing allobservation sessions and the frequencies of activities. The different sessions are represented bydots. Three types of information are given for each dot: the name of the park, season ofobservation, and rank of the enclosure. The sizes of the dots are proportional to thecontributions at the two factors. The biggest dots have the main responsibility for distancesalong each factor.


were associated with ‘‘social�,’’ with a lot of aggressive behavior being directedtoward a ‘‘pariah’’ female. The many urinations observed were probably due to therecent introduction of the two males. One year later (Pe4), the ‘‘pariah’’ female died,and more playing and friendship behaviors were observed (‘‘social+’’).

Spatial Distribution of Activity

Quantitative study of spatial occupation (Table 4)

In most cases, at least half of the surface was under-occupied. The lowest scorefor poor occupation was observed in the smallest park (Bo). When the surfaceincreased, activity took place in a decreasing proportion of the total surface.The Spearman rank correlation between the proportion of under-occupied surfaceand surface available per wolf was nearly significant (r¼0.552, P¼0.051). Duringthe first period at Pescheray, the three females used only 22% of the surface.The introduction of two adult males resulted in an important increase ofoccupation.

Activities linked to a given region (Table 5)

Only activities occurring with at least an expected frequency per region of 45were included in this analysis.

No relationship was observed between localization of activities and season.The most highly localized activities were lying and sleeping. The two smallest parks

Fig. 4. Behavioral differences between the four observation sessions at Pescheray.Description by MCA of the table crossing the four observation sessions at Pescheray andthe frequencies of activities. The different observations are represented by dots. Two types ofinformation are given for each dot: the number of observations and composition of the pack.The sizes of the dots are proportional to the contributions at the two factors.


with poor soil and vegetation (Bi and Bo) showed the lowest level of localizedactivities.

At the Pescheray park, during the first observation period (Pe1) with only threefemales, activities were highly localized. The introduction of two males (Pe2 to Pe4)resulted in a differentiation of occupations.

During the first observation period (Ro1) at the Rhodes park, just afterintroduction of the wolves into the enclosure, almost all activities, including socialencounters, were highly localized. This localization was essentially far away fromwhere humans passed. During the second period, 3 months later, this importantassociation between activity and regions decreased. Although some activities,including social behaviors, were highly localized in some parks, this was not the casefor a given activity in every park. In those cases with an important link betweenactivity and place, it can be supposed that places have particular significations forthe animals. Experimental designs could be implemented to demonstrate this point.

TABLE 4. Occupation of space

Enclosure % under-occ % med-occ % over-occ Surface/wolf

Bi 50% 0% 50% 143Bo 38% 38% 24% 53Ht 63% 25% 12% 91Pe1 78% 0% 22% 833Pe2 44% 33% 33% 500Pe3 67% 0% 33% 500Pe4 56% 22% 22% 625Ra 67% 0% 33% 233Rh1 75% 17% 8% 667Rh2 50% 17% 33% 667

For each observation period, the different virtual regions of each park were classified asunder-, medium- or over-occupied, using the Chi-square law with a P¼0.001 threshold. Thepercentage of the available surface belonging to each category was calculated for eachobservation period.

TABLE 5. Activities linked to a small proportion of the available surface

Percentage of activity highly localized

Bi Bo H.T. Pe1 Pe2 Pe3 Pe4 R.A. Rh1 Rh2

Lying 44% 47% 80% 86% 64% 64% 60% 68% 79% 42%Sleeping 52% 54% 94% 80% 78% 67% 68% 74% 94% 51%Sitting 63% 79% – – – – – – – –Motionless 36% 31% 35% 67% 30% 40% 59% 68% 56% 65%Locomotion 44% 27% 26% 69% 34% 40% 50% 66% 42% 51%Sniffing the ground 35% – 27% – – 37% 68% – – 42%Socialþ 40% 31% 33% – 30% 50% 77% 41% 83% 45%Social� 45% – 43% – 32% 51% – 32% 78% –Vocalization 42% – – – – – – – 84% 72%Stereotypic behavior – 50% – – – – – – – –

The percentage of each activity concentrated in less than 20% of the available surface wascalculated. Percentages in bold are 475%; –: the total amount of activity was not sufficientfor valuable evaluation.


Specialization of some areas

Except in regions with very low attendance, the threshold of 75% of totalattendance due to only one particular activity was never reached.

DISCUSSION

Behavioral criteria, such as the number of abnormal behaviors exhibited, therest/activity balance, and behavioral diversity, are generally used to measure animalwelfare. The animals’ welfare is optimal when there are no stereotypic behaviors, andthe rest/activity balance and the behavioral diversity are similar to those observed inthe wild [Veasey et al., 1996]. It is generally hypothesized that animals in a bigenclosure have many things to do, and resting animals are considered as being bored.To the contrary, our results suggest that wolves spend more time resting in bigenclosures than they do in small ones. This suggests a reappraisal of the pertinence ofthe rest/activity balance as a welfare criterion. In a large enclosure, animals havemore opportunities to choose their resting periods because they are less disturbed byvisitors and keepers. Our observations suggest that, when they can, wolves choose tospent a lot of time resting. Observations during the night are planned in order toevaluate nocturnal activity.

The range of the behavioral repertoire was greatly reduced in the pack thatcontained only females, but it did not appear to be strongly influenced by the qualityof the enclosure. There was no link found between the quality of the enclosure andthe range of the behavioral repertoire. In agreement with Veasey et al. [1996], weconclude that the total diversity of behavior observed in the wild is not essential tothe welfare of wolves in captivity. The packs were mostly characterized by a ‘‘bad’’or ‘‘good’’ atmosphere. The management of the pack (breeding, and introduction ofunknown adult individuals) appears to influence the behavioral repertoire.

Most of the agonistic behaviors observed were related to aggression directedtoward a pariah animal. These attacks were highly localized in a corner of theenclosure where the victim was confined, generally near fences or visitors. It is likelythat in the wild these repeated aggressions cause the hurt wolf to leave the pack, or todie [Mech, 1970]. In the enclosures, the welfare of these wolves was improved byproviding narrow shelters at these particular places, in which the wolves couldprotect themselves from attacks.

Contrary to previous results [De Gaulejac and Gallo, 1997], no systematicassociations between regions of enclosures and activities were found. There were nospecialized zones for given activities, and few localized activities. This could berelated to differences in the size of the regions studied, which were larger in thepresent study than in the previous one. Additional experimental studies could clarifythis point. It is important to evaluate these associations between activities andregions before an enclosure is modified.

CONCLUSIONS

It can be concluded that it is important for the welfare of captive wolves to givethem opportunities for spatial choice. In order to satisfy the visitors, some zookeepers may be tempted to force animals to move at times. This is probably not the


best way to contribute to the animals’ welfare. The enclosure must be large enoughto allow a choice among different regions, to allow animals to be visually separatedfrom the visitors, and to give them control over their activities. Choice and controlare probably the two most significant criteria for improving animal welfare.

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Contribution to the welfare of captive wolves (Canis lupus lupus): A behavioral comparison of six wolf packs