View of Effect of the environment inside and outside the cage on the activity and behaviour test performance of silver foxes

Vol. 7(19981:13-19.

Effect of the environment inside and outside the cage ^on the activity ^{and behaviour test} performance

of silver foxes

TeppoRekilä,LeenaAhola, JaakkoMononen, Mikko Harri

UniversityofKuopio, DepartmentofApplied Zoologyand VeterinaryMedicine,POBox1627, FIN-70211Kuopio, Finland,e-mail:rekila@uku.fi

Onthe hasis ofdaily activity inthe home cage and the open field test the effect of the internaldesign and location of cages onthe behaviour of silver foxes(Vulpes vulpes) duringagrowth period was evaluated. The inclusion ofplatforms incages increased thedaytime activity of silver foxes intheir home cage, but the inclusion of nest boxes did not. Silver foxes housed at the front of the animal barn wereless active duringtheworking dayandmore^activeintheevening thanwere animals housed at therear.The results of the open field test did not differsignificantlybetween animalshousedincages differing in design.This study demonstrates that the behaviour of silver foxeswas only minimally affected bythe interior environment of the cage, and that attempts toimprove housing designshould also take the environment outside the cage into account.

Key words: cageenvironment, circadianrhythm,farm foxes, open field behaviour

ntroduction

It is generally believed that the environment in which confined farm animals live comprises only the space limited by the enclosure walls. Accord- ingly, recommendations and suggestions for im- proved housing systems usually focus on the cage interior. This holdstruefor farmed foxes too(European Convention 1991).

As abasic improvement, the European Con- vention(1991)requires the housing systemsused in fox farming tobe furnished withnestboxes and platforms. The useof these furnishingsvar- ies greatly, dependingon their design, the^spe-

cies offox and the preference shown by individ- ual animals(Mononen 1996).Silver butnotblue foxes,have_aclear-cut preference for cages with nestboxes (Mononen et al. 1996).Silver foxes housed in double fox cages (2.0

m x

m x ^0.8

with three different nestboxes and a platform hadalower base level of blood cortisol andwere fastertoproceed in the open field thanwere an- imals housed in traditionalcages.Moreover,few- eranimals in the enriched environmentwerefear- ful towards humans andmorereacted defensively towards them (Jeppesen and Pedersen 1991).

Another study, in ^contrast, failed ^to show any effect ofnestboxorplatform (Harri etal. 1995).

Moreover,Harrietal. (1995)found that age and

©Agriculturaland Food Science inFinland Manuscriptreceived May 1997

season had a greater effecton the reaction to- wards humans and on open field behaviourin both blue and silver foxes than had accesstoa platform ornestbox throughout the year. In ad- dition, ourprevious study with blue foxes dem- onstrated that the actual environment in which the farmed foxes livedwas far larger thanmere- ly the cage interior (Rekilä etal. 1996). The in- clusion ofnest boxes or platforms in the cage affected the behaviour of the animal toalesser extentthan did the location of the animal’s cage within the row of cages, i.e. the environment outside the cage itself. The animals housed in the front section of the barnwerenearestthe door and thus exposed tomore interaction with peo- ple coming in. This emphasizes the fact that, under normal farm conditions, animals in dif- ferentpartsof the farm may experience consid- erable differences in sensory input. This effect has notusually been taken intoaccount.

Red foxes aresaidtobe nocturnal and crep- uscular in the wild (Harris and Lloyd 1991).

Under farm conditions, however, over50% of the daily activity of blue foxes occurred during daylight (Rekilä ^etal. 1996). One wouldexpect that farmed silver foxes too, would be active during the photophase, when people are active onthe farm.

In our study, juvenile silver foxes were housed during theautumnin three_typesof cage:

astandard cage without any structural^additions, a cage with aplatform and a cage with a nest box. We evaluated the effects of the structural additions and the location of the cageonthe be- haviour of the foxes(seeRekiläetal. 1996).

Material and methods

Animal housing and management

The experimentwasconducted between Septem- ber and Decemberat the Fur Animal Research Station of the University of Kuopio. All the be- havioural tests were carried out in November.

Silver fox cubs (43) of both sexes from 14 lit- ters were housed singly in standard fox cages (1.15

m x ^1.05 m x

^m,

ed animal barn with eightrows of cages. Arow of windows (I x 1.2

m,

2.4 m

long sides exposed the foxestothe natural pho- toperiod. In addition, electric lightswere auto- matically switchedonatsunrise and offatsun- set.Siblingswere randomly allocated into three groups. Fifteen(8males,7females)cages were provided with a wooden platform (1.05

m x

0.24

0.25 m ^below

cageceiling, and 15 (7 males,8 females) cages wereprovided withastandard breeding box with a main chamber(0.41

m x

m x

^m,

WxH)andasmalleranteroom.Thirteen(7males, 6 females) control animals had neither boxes nor platforms. The groupswerepositioned in thetwo middle cagerows of thebarn, eachrow consist- ing of22 cages.^Ineach of thetworows,the dif- ferentcagetypes were in the sequence:nestbox cage,platform cage,emptycage,^nestbox cage, etc. (see Rekilä etal. 1996).The animals were hand-fed twice daily; between 0900 and 1000 and between 1300 and 1400.

Open field test

The open field arenaconsisted ofaclosed wire- mesh runway (5.0

m x 1.05 m x

^m,

shieldedby opaque walls. Before thetest, about

300 g of

runway. Animals were deprived of food for 24 hours before the^test.

Foxes in their home cagewerecaptured with neck tongs and carried in an opaque startbox (0.55

m x 0.29 m x

^m,

field arena.The boxwas then connected_tothe end of the runway opposite the feed. After the foxes had undergonea calming period of1min, the sliding door of the box was opened by re-

mote control. If afox was still inside the ^start box 1 min after the sliding doorwas opened, it wasgently forced into the runway. The observer then left the shed. Each foxwas video-recorded for the whole5 min experimental period(video

Vol. 7(1998): 13-19.

Table 1.^{Effect ofanestboxorplatformon}behavioural parametersinsilver foxes.

Nest box Platform Control P1

Openfield^test

Out(yes/no) 5/10 4/9 NS

NS NS NS NS NS 4/10

End(yes/no) 15/0 ^14/0 13/0

Smell (yes/no) 2/13 2/12 2/11

Eat (yes/no) 2/13 1/13 ^2/11

Rearings, counts/5 min 2.1^±2.2 4.0^±5.0 163^±72

3.2 ±4.3 156±B9 Totalactivity,counts/5 min 140^±43

In-cage tests

Activetime, ^%/24h 38" ±5 42^b±3 38“ ±4 <0.05

1

x

,bGroupswithcommonsuperscriptdo not differ.

camera: Philips LDH 460, video-recorder: Ike- gamiTVR-625).

The open field arena wasdivided into 9 sub- fields of equal sizeonthe video screen.Weana- lysed the activity(number ofvisits) of the ani- mal spatially for each of the 9 subfields andtem- porally for each of the 5 min in the open field.

As the spatial and temporal distribution of the activity didnotprovideanyadditional informa- tion,only dataonthe total number of visits(ac- tivity)(9fields x 5 min) arepresented. The oc- currence of the following behaviours was also recorded: animal exits start box (out), animal enters last field (end), animal smells food (smell), animal ^eatsfood(eat), animal rearsup totouch the cage wall (rearings).

In-cage tests

The behaviour of each individual in its home cagewasvideo-recorded duringonerandom 24- hour periodat the beginning of October with a systemdescribed by Mononenetal.(1996).The behaviour of the animals_was analysed from the videotapes using the instantaneous sampling method witha5 min sampling interval(Martin and Bateson 1993).The variables measured in the home cage were: activity onthe wire mesh floor,restingonthe wire meshfloor,activityon the roof of thenestbox_{or on} the platform,rest-

ing on the roof of the ^nest box or on the plat- form,and in thenestbox. Activity in the home cage(Table 1 and 2) included all activities: ac- tivity_onthe wire meshfloor,activity_onthe roof of thenestbox and activityonthe platform. All activities are expressed as a percentage of the 24-hour period.

Statistics

The results are presented as mean^± standard deviation, median (MD) or as numbers of indi- viduals. When differences between housingcon- ditionswere tested,the%2testwasemployed for non-parametric data. Differences in open field activity and activity in the home cage between housing conditions and betweensexes weretest- ed by ANCOVA (cage locationascovariate).The Spearman correlation coefficient was used ^to measure the effect of cage locations on the number of rearings,on the activity of the foxes in the open fieldtestandonactivity in the home cage. Associations between other open field pa- rameters and cage locations _were measured by logistic regression. Differences in activity in the home cage for each hour of the day between the front and the_rear cages and between housing conditionswere measured by the Mann-Whit- ney U-test andKruskal-Wallis one-way ANO- VA,respectively. To test for the effect of cage

locationonthe circadian rhythm of activity, the first 11 cages in therow wereclassifiedasfront cages and theremaining 11as rear cages. The Pearson correlation coefficientwascalculatedto testfor an association between the timespent inside the nest box or on the platform and the behaviour in the home cage orin the open field

test.

Results

The sexof the animals had noinfluenceon be- haviour either in the open fieldtestorin the home cage(P>0.05). Moreover, therewas nointerac- tion between the effects of sex and inclusions on behaviour (P>0.05). The dataonbothsexes aretherefore pooled in all results shown.

Circadian activity

The silver foxes showedaclear circadian rhythm, withtwo major activity peaks (Figs 1 and^2),one

startingat sunrise and the other at sunset. The dark(1900-0800) and light(0800-1900) phas- es of the day lasted 11 and 13hours, and con- sisted of45.5 ^± 13.5% and 54.5^± 13.5% of dai- ly activity, respectively.

Effect of nest box and platform

Animals with platforms displayed a higher ac- tivity level in their home cages than did control animals or animals withnest boxes (Table 1), when adjusted for the effect of cage location by ANCOVA. This differencewasevident only dur- ing the working day(0800-1600). No difference in activity levelwasfound between thenestbox and control groups. Neither ^nest box norplat- form had any other effect on the behaviour of the foxes in the open fieldtest.

Effect of cage location

A positive correlation was found between cage location and activity in the home cage during the whole day (Spearman r=0.32, ^P<0.05) and dur- Fig. 1.^Intensityand circadian rhythm of activityinthe home

cage of silver foxes housedincages with different furnish- ings.^Sunriseand sunsetaremarked witharrows.No dif- ferences wereobserved inhourly activitybetween differ- ent cage designs (Kruskal-Wallis one-way ANOVA, P>0.05).

Fig.2.Intensityand circadian rhythm of activityinthe home cages of silver foxes housedin the front andrearof the barn. Sunrise and sunsetaremarked with arrows.Differ- encesbetween front cages andrearcageswereobserved at 0900and 1200and at 1300, 1400, 2100and^2200.(Mann- Whitney U-test,P<0.05).

ing the working day (0800-1600, Spearman r=0.53, PcO.OOl). Incontrast, anegative _corre- lation was observed between cage location and activity in the home cage during evening hours (1600-2400, Spearman r=-0.36, P<0.05). The same wasobserved in hourly activity. No effects of cage locationson number of rearings or ac- tivity in the open fieldwerefound.

Use of _nest box and platform

Foxes living in cages with^nestboxes used the roofs of the boxes for active behaviour for 16^± 7%(MD⁼ 19)and for resting for 33^±23%(MD

=44) of the day. In^addition,theyspent9+11%

(MD ⁼6)of the time inside the^nest boxes. The foxes living in cages with platforms used the platforms for activity anaverage of 13^±6%(MD

= 14) and for resting 18^± 19%(MD ⁼7)of the day. Therewas no correlation between the time spentin thenestboxor onthe platform and ac- tivity either in the home cage (P>0.05)orin the open fieldtest(P>0.05).

Discussion

The silver foxes displayed a clear circadian rhythm, with_twoactivity peaks: atsunrise and at sunset.The activity of the foxeswasnotthere- fore synchronized with the natural photoperiod, asthe morning peak coincided withanincrease in illumination and the evening peak withade- crease.As a result, about half of the foxes’ total daily activity occurred during the photophase and half during the scotophase, as was also found for blue foxes^{(Rekilä et}al. 1996). Wild red fox- es aresaid_tobe nocturnal and crepuscular(Har- ris and Lloyd 1991); so are captive red foxes (Tembrock 1957) and farmed silver foxes (Ka- leta 1991).The second activity peak inourstudy, which wasmostprobably caused bysunset, fits this nocturnal activity pattern. In nocturnal spe- cies,suchaslaboratoryrats (Kersten etal. 1980),

the morning activity typicallyoccurs atthe end of the scotophase,notafter it. At the time of year thatwemeasured activity, sunrise coincided with the start of the working day. It is possible that farmed foxes postponed thestartof theirmorn- ing activity peak, with human activity actingas the zeitgeber. The main activity in the morning was feeding, which took place ^at the time the highest activitywas observed. The second meal wasdeliveredat 1400, when the activity of the foxes in therear partof the_rowincreased slight- ly. Possibly the animals in the rear were less exposedtohumans andso were moreexcited by the afternoon feeding than were the animals in the front, who were continuously exposed to human activity. Increased activity during feed deliverycanbe consideredas food anticipatory activity.

Our findings show that the circadian rhythm of silver foxes is probably synchronized with both the photophase and human activity. Incom- parison, the circadian rhythm of farmed blue foxeswas not strictly synchronized with either human activityor the photophase (Rekilä^etal.

1996).These results emphasize thegreatflexi- bility of the natural circadian rhythm in both fox species.

TheEuropean Convention(1991)recommen- dations assume that nest boxes and platforms enrichabarren cage. Recent studies have shown that silver foxes do prefer cages withnestboxes (Mononen etal. 1996).Inaddition,silver foxes housed in cages furnished with three different nestboxes andaplatform hadalower base level of eosinophils, a higher base level of lym- phocytes, andalower base level of cortisol than had animals housed in traditional cages (Jeppesen and Pedersen 1991).They werealso moreactive in the open field and less fearfulto- wards humans in two tests involving human proximity. However, in the present study the behaviour of silver foxes _was only marginally affected by the recommended enrichments of the cage interior. The inclusion of platforms in- creased the activity of animals in their home cages, in comparison with animals living in standard wire mesh cagesorcagesprovidedwith

Vol. 7(1998): 13-19.

nestboxes. However,this was seen only during the working day. This result confirms the differ- ent role of nest boxes and platforms found by Mononen (1996). Nest boxes functionasbotha hiding and _a resting place for foxes, whereas platforms _actas an observation place, and ob- servation is active behaviour withahigh arousal level. Furnishing cages withnestboxes orplat- forms didnotincrease the activity of silver fox- es in the open field as it did in the study of Jeppesen and Pedersen (1991), possibly because the foxes in Jeppesen and Pedersen’s (1991) studyspent2 years in enriched cages before the testswere carriedoutasagainst2 months inour study. On the otherhand, the provision of both nestboxes and platforms increased the activity of blue foxes in the home cage during evening hours_{(Rekilä et}al. 1996).

Ourpresentfindings, together with those of previous studies (Mononen et al. 1993, Peder- sen and Jeppesen 1993, Korhonen and Niemelä

1994

a,

However, as shown by Harri etal. (1995), the furnishing didnotresult in any changes in fox- es’temperament that might be revealed in open field orhomecagebehaviour.

We found earlier that the location of the cage in therow inducedgreater changes in the be- haviour of blue foxes than did the furnishings inside the cage(Rekilä etal. 1996).The animals nearestthe doorwere moreactive in both their home cages and in the open field^testthanwere those towards therear of the barn. The _present study demonstrated that the environment outside the cage also hadaneffectonthe activity offoxes in their home cage.Animals housed in the front of barnwere least active in their home cage dur- ing the afternoon hours. In the eveningand,toa

lesser extent, in the morning, the situation was reversed, and animals housed in the frontwere themostactive. The high activity of foxes inrear cagesduring the working day could be explained by the fact that the furnishings of the foxes’_own and/or neighbouring cages partially obstructed their view of the surroundings, the more so in therearsection of the barn. It has previously been shown that both silver and blue foxes prefer an unobstructed view from their cages (Mononen etal. 1996).

In Rekiläetal.(1996), weattributed the dif- ference in behaviour between blue foxes living

in the front and in therear of the cagerowtothe different amounts of sensory stimuli to which theywereexposed. The animals that lived in the front of the animal barn _were nearest the door and thus subjectedtogreaterinteraction with the people moving around on the farm. The same explanationcanbe appliedtoour presentresults.

Farmed foxesare mostly housed in open 2-row sheds and so can seefurther than would be pos- sible inside a closed barn. On the other hand, the amountof stimuli may also vary greatly be- tween differentparts ofatraditional farm with sheds.

Thepresentstudy with silver foxessupports the conclusions of a previous study with blue foxes (Rekilä etal. 1996),namely, that (i) the actual environment in which the farmed fox lives is larger than the cage interior itself and (ii) at- tempts to improve housing design should also take the environment outside the cage into ac- count.

Acknowledgements.We thank Matti Tengvall for takingcare of the animals and Harri Nurmela for technical assistance.

The studywasfinancedbythe Research Council forAgri- culture and Forestry(Academyof Finland).

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SELOSTUS

Kasvatushäkin ympäristön vaikutus hopeakettujen käyttäytymiseen

TeppoRekilä, LeenaAhola,JaakkoMononenja Mikko Harri Kuopion yliopisto

Tutkimuksessa selvitettiin kasvatushäkin ympäristön vaikutusta hopeakettujen käyttäytymiseen niiden omassahäkissä jaavokenttätestissä. Hyllyn lisäämi- nenhäkin sisälle lisäsi hopeakettujen vuorokausiak- tiivisuutta. Sensijaan pesäkopin tarjoaminen ei lisän- nyt aktiivisuutta. Eläinhallin ulko-ovenläheisyyteen sijoitetut hopeaketut olivat työpäivän aikaanpassii- visempia jaillan aikanaaktiivisempiakuin hallin ta-

kaosaan sijoitetut. Avokenttäkäyttäytyminen eiriip- punut häkin sijainnista hallissa, eikä myöskään hä- kin sisällöstä. Tulosten perusteella voidaan todeta, ettähäkki tai häkin sisältö vaikuttivat hopeakettujen käyttäytymiseen hyvinvähän. Häkinympäristötulee ottaanykyistä enemmän huomioon,kun hopeakettu- jen kasvatusympäristöä pyritäänparantamaan.