ANIMAL BEHAVIOUR, 2004, 67, 11e19doi:10.1016/j.anbehav.2003.01.002

Developmental and hair-coat determinants of

grooming behaviour in goats and sheep

BENJAMIN L. HART & PATRICIA A. PRYOR

Department of Anatomy, Physiology and Cell Biology, School of Veterinary Medicine,

University of California, Davis

(Received 11 June 2001; initial acceptance 16 October 2001;

final acceptance 16 January 2003; MS. number: A9086)

Self-grooming is a common behaviour among many species of ungulates, as it is among several othermammalian taxonomic groups. In goats, as in rodents and small felids, self-grooming appears to reflect anunderlying endogenous timing mechanism, resulting in what has been referred to as programmedgrooming. We tested the prediction from the programmed grooming model that newborn and younggoats, Capra hircus, would groom more frequently than similarly maintained conspecific adults. Thisprediction was upheld in that goat kids, from 2 weeks of age, orally groomed and scratch-groomedsignificantly more frequently than adult females. When the body surface-to-mass ratio of young goats,which was initially about 230% that of adults, declined to about 150%, the difference in grooming rate ofthe young was no longer significantly elevated over that of adults recorded at the same time of year. Wealso tested the predictions that oral grooming in wool sheep, Ovis aries, is inherently programmed and willoccur in adults after shearing and in lambs with undeveloped fleece at levels similar to those of ancestralhair sheep and lambs. When fully fleeced adult wool sheep were shorn, they engaged in grooming ina pattern and frequency not different from that of hair sheep with a pelage representative of ancestralsheep. Wool lambs also groomed at a rate similar to that of hair lambs. Therefore, the elevated rate ofprogrammed grooming of newborn and young ungulates appears to reflect their developmentalprecociousness and consequent exposure, in nature, to ectoparasites.

� 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Self-grooming is a frequently performed behaviour amongrodents, small felids, wild and domestic bovids, cervidsand various species of primates. Grooming serves a num-ber of functions, the most notable and widespread beingthe removal of ectoparasites and cleaning and condition-ing the pelage. The effectiveness of self-grooming inremoving ectoparasites has been experimentally docu-mented in rodents (Wiesbroth et al. 1974; Murray 1987),domestic cats, Felis domestica (Eckstein & Hart 2000b),cattle, Bos tarus (Little 1963; Sutherst et al. 1983), goats,Capra hircus (Koch 1988) and in the African antelope(impala, Aepyceros melampus: Mooring et al. 1996).Opportunistic observations provide evidence for the roleof self-grooming in primates in removing ectoparasites(Spruijt et al. 1992; Tanaka 1995).Self-grooming takes markedly different species-specific

forms. In primates, digital combing and scratching ischaracteristic. In nonprimate species, grooming cangenerally be divided between scratch grooming of the

Correspondence: B. L. Hart, Department of Anatomy, Physiology andCell Biology, School of Veterinary Medicine, University of California,Davis, CA 95616, U.S.A. (email: blhart@ucdavis.edu).

110003e3472/03/$30.00/0 � 2003 The Association

head and neck with the hind feet, claws or hooves andoral grooming with the tongue or teeth. In rodents andcats, in addition to face washing using the front paws, thetongue is used to comb through different areas of thepelage, often in a rostralecaudal progression (Richmond &Sachs 1980; Eckstein & Hart 2000a). In cattle, grooming isperformed with the tongue in bouts of licking applied toone area, and in goats and antelope, oral grooming takesthe form of scraping the lower incisors through the pelagein bouts of upward motions directed to a single area (Hartet al. 1992; Mooring et al. 1998).The occurrence of self-grooming among several mam-

malian species appears to reflect an underlying endoge-nous timing or programming mechanism. In rodents,where this concept has been explored extensively (Fen-tress 1988; Sachs 1988), recent behavioural analyses ofmice with a Hoxb8mutant gene revealed the occurrence ofexcessive initiation of grooming as well as overallgrooming (Greer & Capecchi 2002), further reinforcingthe concept of an endogenous generator for bouts ofgrooming. Observations on the initiation of grooming incats are consistent with an innate programming mecha-nism in this species (Eckstein & Hart 2000a). All of the

for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

ANIMAL BEHAVIOUR, 67, 112

behavioural studies conducted so far, both in nature andin captive ectoparasite-free environments, on antelope(reviewed in Hart 1997, 2000), elk, Cervus elaphus(Mooring & Samuel 1998a), bison, Bison bison (Mooring& Samuel 1998b) and goats (Mooring et al. 1998)are consistent with the concept of innate program-ming, rather than cutaneous stimulation, as the primarymechanism controlling the initiation of grooming bouts.In work on ungulates, where discrete bouts of groomingare delivered to single areas of the body, the term‘programmed grooming’ has been used to representthe behavioural manifestation of an innate timingmechanism.Among the derivations or predictions of the pro-

grammed grooming model is the body size principle,which predicts that species of smaller body size, witha larger body surface-to-mass ratio than taxonomicallyrelated species of larger size, groom more frequently thanspecies of larger body size (Hart et al. 1992; Mooring et al.2000). The adaptive value of this principle is that bygrooming more frequently, animals of smaller size havea lower density of ectoparasites on the body surface thananimals of larger size. This protects them from sustaininggreater blood volume loss per unit of body mass than theyotherwise would with an equivalent density of ectopar-asites. Consistent with this programmed grooming model,antelope species of smaller size groom more frequentlyand carry fewer ectoparasites (ticks) per unit of bodysurface area than large-bodied antelope species in thesame environment (Olubayo et al. 1993). Grooming inresponse to cutaneous stimulation does, of course, occur;so in reality, such stimulus-driven grooming is super-imposed upon programmed grooming.The body size principle also predicts that in species with

precocial young that are capable of moving about in anectoparasite-ridden environment, the young shouldgroom more frequently than adults that have a lowerbody surface-to-mass ratio. In nature, the more frequentoccurrence of grooming would help defend precocialnewborns and young against the blood loss fromectoparasites acquired while moving about, which couldotherwise impair growth rate and development of theimmune system. In keeping with this intraspecific pre-diction, observations on young impala (Mooring & Hart1997), elk (Mooring & Samuel 1998a) and bison (Mooring& Samuel 1998b) of a single developmental age found thatyoung animals engaged in oral grooming more frequentlythan their adult counterparts.A study of the grooming behaviour of small domestic

ruminants offers an opportunity to continue to exploresome determinants of grooming and predictions of theprogrammed grooming model that are applicable to wildas well as domestic ungulates. To test the importantintraspecific prediction of the body size principle further,we conducted weekly observations on newborn andyoung goats to determine the threshold surface-to-massratio where grooming is no longer significantly elevatedover that of adults. We sampled blood plasma of goat kidsat various stages of growth to explore a possible correla-tion in secretion of growth hormone as a mediator of thepredicted more frequent grooming in newborns and

young. In wool sheep, Ovis aries, (Klindt et al. 1987) andcattle (Plouzek & Trenkle 1991; McAndrews et al. 1993)there are age-dependent decreases in baseline and pulse-amplitude concentrations of growth hormone. However,secretion patterns of this hormone in newborn and younggoats have not been systematically explored.

A second set of predictions involved wool sheep, wherethe dense interwoven pelage prevents oral grooming(preliminary observations). Assuming that ancestral hairsheep engaged in oral grooming of all parts of the body,a prediction of the programmed grooming model is thatshearing would allow programmed grooming to occur ata rate similar to that of ancestral sheep. The wild ancestorsof domestic sheep, namely the West Asiatic mouflon, Ovisorientalis, were historically widely distributed in southwestAsia (Uerpmann 1987). Some extant breeds of sheep,referred to here as hair sheep, have retained much of theancestral pelage of shorter hairs (Zohary et al. 1998).

EXPERIMENT 1: DEVELOPMENTAL ASPECTS OF

GROOMING IN GOATS

We monitored developmental changes in grooming ratesin male and female goat kids during 1e24 weeks of age.

Methods

These studies were conducted at the University ofCalifornia, Davis, dairy goat facility. Goat kid subjects,comprising eight males and eight females, were observedat 2e7 weeks of age in inside pens and at 8e24 weeks ofage in outside pens. The goat kids had been removed fromtheir mothers just after colostrum feeding (1e2 days afterbirth). For comparison with the kids, six adult femalelactating does of the Alpine breed or Alpine-cross wereobserved. Does were maintained in pens containing a shedfor shade and inclement weather, and were provisionedwith oat hay and water. Also for comparison, four kidsthat were left with their dams were observed at 2e8 weeksof age. All goats were free of ectoparasites.

We scored oral bouts and episodes in 20-min focalobservations only when the subjects were standing.Grooming in goats is performed as a series of upwardsscraping movements of the lower incisors directed to onebody area. Each grooming movement was referred to as anepisode with a series of connected episodes to the samebody part referred to as a bout (Hart et al. 1992). Boutswere considered to be terminated when a differentbehaviour ensued or no grooming occurred for 5 s. Boutsof oral grooming, number of grooming episodes compris-ing each bout and the part of the body groomed (e.g. frontlegs, shoulders or rib cage) were recorded during focalobservations. Scratch grooming of the head and neck bythe hind hooves were scored in bouts; the scratch episodesin young animals were sometimes so rapid that they weredifficult to tabulate, so only scratch bouts were scored. Allsubjects were individually recognized by eartags. For goatkids, two observations were conducted per week, atintervals of at least 2 days, for weeks 2e6, and one

HART & PRYOR: DETERMINANTS OF GROOMING 13

observation per week for weeks 7e24. We conducted twoobservations per week on kids with dams through week 8.Weekly means were determined for each goat kid per weekand the data were then expressed as mean grooming boutsand episodes per hour.Observations were conducted in midmorning and

midafternoon on alternative tests. The first kids wereobserved in mid-February and the last observationoccurred in August. For does, we conducted four to sixfocal observations per month during AprileAugust,alternating between midmorning and midafternoonobservations. Observations on does covered the time spanof most observations on young goats. A recent study ondwarf Shiba goats revealed an increase in grooming indoes in the autumn compared with the summer (Kakumaet al. 2003). Consequently, monthly means of groomingrates, extrapolated to grooming bouts and episodes perhour, were derived for each doe not only for comparisonwith young goats but to detect seasonal changes ingrooming in does.To estimate the relative body surface-to-mass ratio

threshold at which oral and scratch grooming no longersignificantly exceeded that of adults, we used theallometric exponent of 0.67 to convert body mass torelative surface area (Schmidt-Neilsen 1984) for variousstages in development. The equation for calculatingsurface area from body mass uses a constant (Meehcoefficient, k) for differences in body shape to allowbetween-species comparisons. Although body shape un-doubtedly differs between young and adult goats, weconsidered differences in the Meeh coefficient to beinsignificant in our analysis, because the coefficient isabout the same (k ¼ 10) for a wide variety of species,including those as diverse as dogs and horses (Schmidt-Neilsen 1984, page 81). We calculated body surface-to-mass ratios for kids on even-numbered weeks throughweek 24. From these data, we calculated the surface-to-mass ratio of kids relative to that of adults during weeks2e24 (surface-to-mass ratio of kids/surface-to-mass ratioof adults).For growth hormone analyses, we took 2 ml of blood

from the jugular vein of goat kids weekly when the kidswere 2e6 weeks of age, then biweekly during weeks 7e24.These blood samples, taken on days when there were nobehavioural observations, were treated with heparin andcentrifuged, and the plasma was stored at �20 (C untilgrowth hormone assays could be conducted on allsamples. Plasma growth hormone concentrations weredetermined by radioimmunoassay as detailed elsewherefor the bovine (Joke 1978). The parallel between caprineand bovine growth hormone characteristics has beenreported elsewhere (Hashizume & Kanematsu 1991).For most statistical analyses, we used the SAS GENMOD

Procedure, with logarithmic transformations of data asnecessary to achieve normality, and with P values set at0.05, two tailed. We used a nonparametric Wilcoxonmatched-pairs signed-ranks test, two tailed, to compareseasonal differences in grooming in does after a prelimi-nary review of the data revealed an increase in groomingin JulyeAugust compared with AprileJune, and theManneWhitney test, two tailed, to compare dam-reared

kids with kids reared without dams (Siegel & Castellan1988).

Results

Tests for differences between male and female kids wereconducted on a week-by-week basis for weeks 2e24. Adifference (P!0:05) between sexes for oral bouts wasfound only on weeks 15 and 19 (ANOVA: F1;15 ¼ 6:9 and11.7, respectively). A difference in oral episodes was foundonly on weeks 4, 15 and 19 (F1;15 ¼ 5:5, 4.9 and 6.0,respectively) and a difference in scratch grooming boutsonly on weeks 3, 12, 13 and 19 (F1;15 ¼ 7:7, 6.5, 10.9 and9.4, respectively). Taking into account the absence of anysystematic difference and the likelihood of type I errorswith comparisons across each of the 23 weeks, weconcluded that there was no difference between maleand female kids in any aspect of grooming. In allsubsequent analyses, male and female kids were com-bined.For comparison with adults, and to avoid a confound of

seasonal differences in grooming, we compared thegrooming data of kids with those of adult females atapproximately the same time of year. For statisticalpurposes, we compared grooming in kids at 2e5 weeks,6e10 weeks, 11e14 weeks, 15e19 weeks and 20e24 weeksof age with grooming in adults during April, May, June,July and August, respectively.Kids at 2e14 weeks of age engaged in significantly more

oral grooming bouts in April, May and June (ANOVA:F1;20 ¼ 59:6, 18.7 and 10.7, P!0:001, 0.001 and 0.01,respectively) and oral grooming episodes (F1;20 ¼ 105:6,22.1 and 16.5, P!0:0001, 0.0001 and 0.001, respectively)than did adult females, but did not differ from adultfemales in these measures when they were 15e24 weeks ofage (JulyeAugust). Kids at 2e10 weeks of age alsoperformed significantly more scratch bouts than did adultfemales in April and May (F1;20 ¼ 32:4 and 4.4, P!0:0001and 0.05, respectively), but did not differ from adultfemales in the number of scratch bouts performed whenthey were 11e24 weeks of age (JuneeAugust). At 2e3weeks of age, kids oral-groomed at about 10 times the rateof adult females and scratch-groomed at about eight timesthe rate of adult females (Fig. 1).When observations began, kids at 2 weeks of age had

a 228% (0.57/0.25) greater surface-to-mass ratio thanadults (Fig. 1). When scratch grooming in kids was nolonger significantly different from that of adults (June),kids had a 152% (0.38/0.25) greater surface-to-mass ratiothan adults, and when oral grooming in kids was nolonger significantly different from that of adults ( July),this ratio dropped to 140% (0.35/0.25).Grooming in does increased between June and July,

but was relatively stable before and after this period.For statistical analysis, we compared the mean groomingrates for each doe in April, May and June with those ob-tained for July and August. Oral grooming bouts andepisodes were significantly higher for JulyeAugust thanAprileJune (Wilcoxon matched-pairs signed-ranks test:T ¼ 21,N ¼ 6, P ¼ 0:03); scratch grooming rates, although

ANIMAL BEHAVIOUR, 67, 114

Figure 1. Weekly changes in mean grooming rates of goat kids during weeks 2e24 after birth (�) shown as oral bouts, oral episodes and

scratch bouts extrapolated to bouts or episodes per hour. Weekly changes in body surface-to-mass ratios of goat kids during weeks 2e24 after

birth (B) as a function of development and age. Bars represent the means of six adults sampled in the months indicated and used forcomparison with goat kids. The vertical lines represent the point where measures of grooming in goat kids were no longer significantly greater

than those of adults during the comparison month.

higher in JulyeAugust, did not reach significance (T ¼ 15,N ¼ 6, NS).Because there may be a physiological reason for the

lower rate of grooming in does in AprileJune than inJulyeAugust (see Discussion) that would not apply to kids,the grooming of adults in August may be a better referencelevel for comparisons with kids than the monthly

comparisons used above. To address this possibility, wecompared the grooming rates of kids with those of adultsusing August as a baseline for adults, because adult femalesshowed the highest rate of grooming during this time.During week 2, kids oral-groomed and scratch-groomedabout two to three times more than adults (Fig. 1). Withthis comparison, kids differed from adults on oral bouts

HART & PRYOR: DETERMINANTS OF GROOMING 15

only for weeks 2e11 (F1;20 ¼ 42:7, 35.7, 33.6, 38.5, 21.9,12.1, 15.1, 12.5, 10.6 and 4.9, P!0:0001, 0.0001, 0.0001,0.0001, 0.0001, 0.01, 0.001, 0.01, 0.01 and 0.05, re-spectively). For oral episodes, kids differed from adults inAugust only for weeks 2e6 (F1;20 ¼ 11:3, 12.9, 9.9, 13.0and 7.6, P!0:01, 0.01, 0.01, 0.01 and 0.05, respectively),reflecting a decline in oral episodes per bout over thedevelopmental period. Kids differed from adults in Auguston scratch grooming only for weeks 2e5 (F1;20 ¼ 16:6,27.8, 9.2 and 8.0, P!0:001, 0.0001, 0.01 and 0.01,respectively). Using the comparison when scratch groom-ing was no longer elevated over adults, kids had a 180%greater surface-to-mass ratio than adults, and when oralgrooming (bouts) was no longer significantly different, theratio dropped to about 150%.To compare the grooming behaviour of the four kids

reared with dams with the grooming behaviour of kidsreared without dams, we calculated the mean number oforal bouts, oral episodes and scratch bouts for allgrooming observations for weeks 2e8 for each kid.Extrapolated to hourly rates, dam-reared kids delivereda mean of 17.0 oral bouts, 229 oral episodes and 7.3scratch bouts compared with 20.7, 281 and 11.7, re-spectively, for the 16 kids reared without dams. Thesedifferences were not significant for oral bouts, oralepisodes or scratch bouts (ManneWhitney U tests:Z ¼ 1:5, 1.6 and 0.7, P ¼ 0:13, 0.11 and 0.7, respectively).Growth hormone assays revealed extreme variability

within and between subjects. On sequential weeks, levelsof 18.8, 57.6, 3.1, 2.8 and 3.1 ng/ml were typical forsamples from the same kid. Samples taken every 15 minfrom an indwelling venous cannula of a goat, which wasnot part of this study, showed spikes of 50e60 ng/ml ofgrowth hormone about every 4 h compared withbackground levels of 1e10 ng/ml. Despite the impracti-cality of accurately portraying growth hormone secretionpatterns or levels with weekly and biweekly sampling,a Pearson correlation conducted between the log ofgrowth hormone and log of oral bouts over the 23observations revealed a significant positive correlation,although the degree of correlation was low (r21 ¼ 0:15,P ¼ 0:03). The correlation with oral episodes was also lowbut significant (r21 ¼ 0:14, P ¼ 0:04), and the correlationwith scratch bouts was not significant (r21 ¼ 0:013,P ¼ 0:07).

EXPERIMENT 2: GROOMING IN WOOL

AND HAIR SHEEP

We tested the prediction that oral grooming in woolsheep, which is prevented by a dense fleece, is inherentlyprogrammed and will occur after shearing at a level similarto that of the ancestral hair sheep. We allowed 2 weeksafter shearing for habituation to the shearing process tooccur and for the immediate postshearing change incutaneous sensory stimulation. The second prediction,related to the first, was that oral grooming in wool sheeplambs, with a short undeveloped fleece, would occur ata level similar to that of ancestral hair sheep lambs, againreflecting an inherently programmed grooming rate.

Methods

Wool sheepThe wool sheep were of the Suffolk breed maintained in

ectoparasite-free facilities at the University of California,Davis. Adult subjects were five ewes maintained in a barn.Lamb subjects were five males and five females studied2e8 weeks after birth. Preliminary observations of hairsheep and lambs revealed that the pattern of oralgrooming in sheep was the same as in goats, with boutsof upward scraping motions of the lower incisors againstthe pelage. In preliminary observations, to verify theabsence of grooming (or grooming attempts) to fleecedareas, we noticed occasional oral bouts delivered to a partof the front or back legs not covered with wool.We conducted focal observations on grooming, consist-

ing of recording oral bouts, oral episodes and scratchbouts, in the same manner as with goats. The head ofSuffolk sheep is not covered fully with wool and was notexpected to interfere with scratch grooming of the head.For wool ewes, we conducted two 20-min focal observa-tions on each ewe 2 weeks before shearing and six 20-minobservations per ewe during weeks 2e4 after shearing ata minimum of 2-day intervals. For wool lambs, weconducted two 20-min observations each week on eachlamb for weeks 2e8. Means were determined for ewesbefore and after shearing and for lambs for weeks 2e8combined. The data were then expressed as the meannumber of grooming bouts and episodes per hour. Allobservations were conducted with the sheep standing andwere equally divided between morning and afternoonobservations. We focused on the distribution of groomingbouts to the legs and areas other than the legs in the woolsheep.

Hair sheepWe observed hair sheep in a pasture on a private farm

194 km north of the University of California, Davis. Thesesheep were part of a flock of approximately 150 breedingewes. The flock consisted of purebred St Croix along withSt Croix crossbred sheep (0.75e0.9% St Croix). Thesesheep had a hair-type pelage on most of the body withsome individual variability in degree of wool pelageranging between 0 and 50%. The degree of wool coveragein these sheep varies depending upon individual, age,physiological status and season (E. Bradford, personalcommunication). Because the flock size precluded thelikelihood of finding the same animal for replicateobservations, we conducted only a single focal observa-tion on each subject. The adults in the study comprised 31ewes that had been eartagged and could be individuallyidentified to avoid repeated observations on the sameewes. Observations took place during the lambing season,allowing single focal observations on 30 lambs 2e7 weeksafter birth. To avoid replicate observations, we identifiedthe lambs by association with their dams.Observations on hair sheep were the same as those with

wool sheep and consisted of identifying a subject andattempting a focal observation of 20 min. For partialobservations of 10 min, and for those of 20 min, all data

ANIMAL BEHAVIOUR, 67, 116

were extrapolated to grooming bouts and episodes perhour. Observations were made at midmorning or earlyafternoon while the sheep were foraging and standing ormoving. Observations were made at 100e150 m, usingbinoculars, so as not to disturb normal behaviour. Maleand female lambs could not be distinguished in the field.

Statistical analysesBased on an obvious physical prevention of grooming

by a dense wool fleece, we predicted that shorn woolsheep would orally groom more than unshorn woolsheep. In light of the fact that oral grooming could onlyincrease for wool ewes, and not decrease, after shearing,we used one-tailed nonparametric Fisher’s exact tests, witheach subject serving as its own control and P values set at0.05. For all other tests, we used the SAS GENMODprocedure, logit model with ANOVA tests and t tests, withtwo-tailed P values set at 0.05. Logarithmic and square-root transformations were performed as necessary toachieve normality. Because we conducted only oneobservation per subject for hair sheep, we expected thevariance in grooming rates to be much higher than thatfor the replicate observations on wool ewes and lambs.Therefore, although direct statistical comparison betweenhair and wool sheep was not possible, we were able tomake general comparisons.

Results

Confirming preliminary observations, the pattern oforal grooming in sheep was the same as that observed ingoats, with bouts of upward scraping movements of thelower incisors against the pelage. Usually it was notevident whether primarily the tongue or the lower incisorswere used in grooming, but when the observation angleallowed, it was clear that grooming was with the lowerincisors.As expected, wool ewes, prior to shearing, did not

engage in oral grooming and displayed no ‘groomingintention movements’ towards fleeced areas (Fig. 2).Following shearing, all ewes delivered oral groomingbouts to previously fleeced areas at rates that were signi-ficantly higher than those prior to shearing (Wilcoxonmatched-pairs signed-ranks test: T ¼ 15, N ¼ 5, P ¼ 0:03,one tailed). Analyses of body areas groomed revealed thatthe sheared wool ewes devoted a mean of 48% of oralgrooming bouts to areas that were previously covered withwool. The relative rates of scratch grooming in wool ewes(to nonfleeced head and neck) did not differ before andafter shearing (Fig. 2). Also as predicted, the mean rates oforal and scratch grooming in shorn wool ewes were atleast as high as those in hair sheep and may have beeneven higher (Fig. 2).Analysis of grooming rates of wool lambs revealed no

difference between males and females in oral bouts orepisodes (ANOVA: F1;62 ¼ 1:05 and 1.22, P ¼ 0:3 and 0.3,respectively). There was a significant difference in scratchbouts (F1;62 ¼ 9:63, P ¼ 0:03), with females deliveringmore bouts than males. This difference between sexeswas considered relatively minor, and for comparison with

ewes, sexes of lambs were combined. Lambs deliveredsignificantly more oral bouts (F1;13 ¼ 5:45, P ¼ 0:036)than did adult shorn ewes. However, the number of oralepisodes and scratch bouts of lambs did not significantlyexceed that of adults (F ¼ 3:41, P ¼ 0:1 and F ¼ 1:18,P ¼ 0:3, respectively). Wool lambs devoted a mean of 34%of oral grooming bouts to nonleg areas. As with thecomparison of shorn ewes with hair ewes, the meangrooming rates of wool lambs were similar to those of hairlambs (Fig. 2), although, as with ewes, no statisticalcomparison was made.

The statistical analysis for comparing grooming in hairlambs with grooming in hair ewes took into account thatthe single focal animal procedure resulted in 25/32 (78%)samples of ewes and 24/37 (64%) lambs with no oralgrooming and 23/32 (72%) ewes and 27/37 (73%) lambswith no scratch grooming. A chi-square analysis revealedno difference between lambs and ewes in number ofobservations with zero for oral bouts and scratch bouts(P ¼ 0:40 and 0.51, respectively). Comparison of justthe 13 lambs with the seven ewes that displayed someoral grooming revealed that lambs showed significantlymore oral episodes (t18 ¼ �3:26, P ¼ 0:004) but not moreoral bouts (t18 ¼ �2:00, P ¼ 0:06) or scratch bouts(t14 ¼ �0:57, P ¼ 0:58) than hair ewes.

DISCUSSION

The prediction that oral grooming in newborn goat kidswould exceed that of conspecific adults was confirmed ingoats, where oral grooming in kids was about 10 times,and scratch grooming eight times, greater than that seenin female adults recorded during the same time of year.These findings are consistent with an intrinsic timingmechanism for grooming that changes with developmen-tal stage. The more frequent grooming of newborn goatswas significant during the second week and declinedgradually to the adult rate. Two-week-old goats hada 230% greater surface-to-mass ratio than adults. Whenthis ratio declined to about 150%, the scratch groomingrate in kids no longer exceeded that of adults, and at 15weeks of age, when the surface-to-mass ratio in kidsdropped to 140%, oral grooming was no longer signifi-cantly elevated over adults. In impala, when the surface-to-mass ratio of the young reaches 130e160% that ofadults, their rates of oral grooming do not differ (Mooring& Hart 1997). A similar surface-to-mass threshold fora development effect on oral grooming between species asdiverse as wild impala and domesticated goats suggeststhat a threshold ratio difference of about 150% (or whenyoung are about 30% the mass of adults) may be a generalbiological variable that would be predictive for otherungulates.

This developmental effect on grooming rate is hypoth-esized to be a reflection of some underlying hormonal orneuropeptide change (Hart 1997). A precedent exists forhormonal alteration of the oral grooming rate from a studyof the effects of castration in adult male goats in which thegrooming rate is accelerated by removal of the suppressiveeffects of testosterone (Mooring et al. 1998) and is in turn

HART & PRYOR: DETERMINANTS OF GROOMING 17

down-regulated by testosterone supplementation (Kakumaet al. 2003). Although there is a sexually dimorphicdifference in grooming rate in adult domestic goats relatedto the secretion of testosterone (Mooring et al. 1998;Kakuma et al. 2003), the absence of a gender differencein goat kids in the present study between the ages of 2and 24 weeks could reflect complex interactions betweenboth developmental and seasonal effects on hormonesecretion.One candidate for a developmental change is growth

hormone secretion. The decline in plasma concentrationof growth hormone in kids was significantly correlatedwith the decline in oral grooming rate, although thecorrelation was rather weak. With the pulsatile pattern ofgrowth hormone secretions, blood samples taken oncea week do not capture the secretory pattern and poorlyestimate developmental patterns. In domestic cattle, thedecline in circulating growth hormone during the transi-tion from newborn to the juvenile stage is initially due toa reduction in the baseline concentration and latera reduction of pulse amplitude of growth hormone

Figure 2. Grooming rates, shown as oral bouts, oral episodes and

scratch episodes extrapolated to mean G SE bouts or episodes per

hour, for unshorn and shorn adult wool sheep and lambs and foradult hair sheep and lambs.

(McAndrews et al. 1993). Other possibilities for themediation of a decline in grooming frequency could beneuropeptides such as vasopressin (Meisenberg 1988).The increase in oral grooming in does in JulyeAugust,

which was more than double that in AprileJune, is similarto an increase in grooming in the autumn of adult femaleJapanese Shiba goats, where the increase is also aboutdouble that in summer (Kakuma et al. 2003). BecauseAlpine goats are seasonal in reproduction, the increasecould reflect the effects of changing patterns of secretionof ovarian hormones. However, Shiba goats are notseasonal breeders, so the increase in these goats couldnot be attributed to ovarian hormones. It was suggestedthat the increase may reflect a ‘release’ from a depressiveeffect of prolactin, which decreases as days become shorter(Mori et al. 1985; Maeda et al. 1986). Alpine does typical ofthose in the present study begin to come into oestrus inJuly and August when one would expect prolactin levelsto be declining. In nature, an increase in grooming wouldcut down on blood protein loss to ectoparasites duringgestation, optimizing birth weight of the newborn.During the spring when kids are born, there is an increasein prolactin related to lactation, which might be re-sponsible for the lower grooming rate seen in the presentstudy during AprileJune, allowing for greater vigilanceover potential predators of the newborn.It is difficult to say whether the best comparison of

grooming rate in kids is with female adults observedduring the same month or with female adults observedonly during the month when their grooming was mostfrequent and perhaps occurring at a baseline rate. If thelatter comparison were to be used, newborn goats wouldonly be grooming two to three times more frequentlythan adults, a difference more comparable to that seen inwild impala and North American cervids (see Introduc-tion). Furthermore, the difference between kids and adultsin oral grooming would no longer be significant beyondabout week 11 when the surface-to-mass ratio of kidsreached about 150% that of adults.In the wool sheep, as expected, unshorn ewes did not

groom areas covered with fleece or perform ‘groomingintention movements’, but in the 2e4 weeks aftershearing, all ewes groomed areas previously covered withwool; 48% of oral grooming bouts were delivered to areaspreviously covered with wool. Immediately followingshearing, the skin undoubtedly presents a different set ofcutaneous stimuli than that in the fully fleeced conditionand possibly evokes some grooming or rubbing. Thus, wewaited until 2 weeks had elapsed before conductinggrooming observations. A change in grooming behaviourdue to the novelty of having the fleece removed, or a brief‘catch-up effect’ of having grooming prevented, as seen incats (Eckstein & Hart 2000a), would not be expected to lastas late as 2e4 weeks after shearing when observationswere made.Consistent with the concept of an underlying intrinsic

generator of grooming bouts, our observations revealedthat the grooming rate of shorn wool sheep was similar tothat of ancestral hair sheep. Furthermore, the groomingrate of wool lambs (prior to fleece development) wassimilar to that of hair lambs. The difference in grooming

ANIMAL BEHAVIOUR, 67, 118

rates between lambs and ewes, so evident in thecomparison of goat kids with adult females, was not sopronounced and reached significance only for oral bouts(wool sheep) or oral episodes (hair sheep). The absence ofa clear statistically significant developmental effect mayreflect limitations of the number of subjects available forobservations and/or the extent of observations.All the predictions of the programmed grooming model

outlined in Introduction were upheld: (1) newborn andyoung goats groomed significantly more than adults andthe difference gradually declined; (2) adult wool sheepthat did not orally groom fleeced areas groomed theseareas when sheared and at a rate similar to hair sheep withan ancestral type of pelage; and (3) wool lambs orallygroomed at a rate similar to that of hair lambs.The elevated grooming rate in newborn and young

ungulates, demonstrated in systematic observations onthe goats of the present study, and in the more time-limited observations on impala, elk and bison, undoubt-edly reflects the adaptive value of such a developmentaleffect in precocial newborn that are vulnerable toectoparasite bites and the associated blood loss. In impala,young groom more frequently than do adults (Mooring &Hart 1997) and severe tick infestations in young are foundonly one-half to one-fifth as often as in adults (Gallivan etal. 1995). This developmental effect undoubtedly contrib-utes to the growth and survival of young animals innature in those species where the young are precociousand freely move about in an environment infested withectoparasites almost as soon as they are born. One wouldnot necessarily expect to see such developmental effects inother mammalian taxa, such as felids and rodents, wherethe young are altricial and do not move about inectoparasite-infested environments until they are older.While in the nest, they are presumably protected fromectoparasites by intensive grooming from their mothers(Hart 1990). A study of such species differences indevelopmental effects of grooming would contribute toa further understanding of the role of grooming in parasitecontrol of animals in nature.

Acknowledgments

We kindly acknowledge the assistance of Erik Bradford ofthe University of California, Davis, Department of AnimalScience, for advice on breeds of sheep, and Kathy Lewis forpermission to conduct behavioural observations on herflock of St Croix sheep. Marcie Linet, Debbie Kress andKevin Eslinger contributed to behavioural observations.Yukari Takeuchi and Yuji Mori of the University providedguidance on growth hormone analyses, which wereconducted by K. Mogi. Kelly Cliff provided data manage-ment assistance and Mitch Watnik, of the University ofCalifornia, Davis Statistical Laboratory, provided statisticalassistance.

References

Eckstein, R. A. & Hart, B. L. 2000a. The organization of control of

grooming in cats. Applied Animal Behaviour Science, 68, 131e140.

Eckstein, R. A. & Hart, B. L. 2000b. Grooming and control of fleas

in cats. Applied Animal Behaviour Science, 68, 141e150.

Fentress, J. S. 1988. Expressive contexts, fine structure, and central

mediation of rodent grooming. Annals of the New York Academy of

Sciences, 525, 18e26.

Gallivan, G. J., Culverwell, J., Girdwood, R. & Surgearer, G. A.1995. Ixodid ticks of impala (Aepyceros melampus) in Swaziland:effect of age class, sex, body condition and management. South

African Journal of Zoology, 30, 178e186.

Greer, J. M. & Capecchi, M. R. 2002. Hoxb8 is required for normal

grooming behavior in mice. Neuron, 33, 23e34.

Hart, B. L. 1990. Behavioral adaptations to pathogens and parasites:

five strategies. Neuroscience and Biobehavioral Reviews, 14,273e294.

Hart, B. L. 1997. Effects of hormones on behavioral defenses against

parasites. In: Parasites and Pathogens: Effects on Host Hormones and

Behavior (Ed. by N. Beckage), pp. 210e230. New York: Chapman& Hall.

Hart, B. L. 2000. Role of grooming in biological control of ticks.Annals of the New York Academy of Sciences, 916, 565e569.

Hart, B. L., Hart, L. A., Mooring, M. S. & Olubayo, R. 1992.Biological basis of grooming behaviour in antelope: the body size,

vigilance and habitat principles. Animal Behaviour, 44, 615e631.

Hashizume, T. & Kanematsu, S. 1991. Effects of cholecystokinin

octapeptide on the release of growth hormone in perifused

pituitary and hypothalamus of goat. Animal Science Technology,

62, 343e350.

Joke, T. 1978. Effect of TRH on circulating growth hormone, prolactin

and triiodothyronine levels in the bovine. Endocrinology,25, 19e26.

Kakuma, Y., Takeuchi, Y., Mori, Y. & Hart, B. L. 2003. Hormonal

control of grooming behavior in domestic goats. Physiology &Behavior, 78, 61e66.

Klindt, J., Jenkins, T. G. & Ford, J. J. 1987. Prenatal androgen

exposure and growth and secretion of growth hormone andprolactin in ewes postweaning. Proceedings of the Society for

Experimental Biology and Medicine, 185, 201e205.

Koch, H. G. 1988. Suitability of white-tailed deer, cattle, and goats as

hosts for the lone star tick, Amblyomma americanum (Acari:

Ixodidae). Journal of the Kansas Entomological Society, 61, 251e257.

Little, D. A. 1963. The effects of cattle tick infestation on the growth

rate of cattle. Australian Veterinary Journal, 39, 6e10.

McAndrews, J. M., Stroud, C. M., MacDonald, R. D., Hymer, W. C.& Deaver, D. R. 1993. Age-related changes in the secretion of

growth hormone in vivo and in vitro in infantile and prepubertalHolstein bull calves. Journal of Endocrinology, 139, 307e315.

Maeda, K. I., Mori, Y. & Kano, Y. 1986. Superior cervical ganglio-nectomy prevents gonadal regression and increased plasma

prolactin concentrations induced by long days in goats. Journal

of Endocrinology, 110, 137e144.

Meisenberg, G. 1988. Vasopressin-induced grooming and scratch-

ing behavior in mice. Annals of the New York Academy of Sciences,

525, 257e269.

Mooring, M. S. & Hart, B. L. 1997. Self-grooming in impala

mothers and lambs: testing the body size and tick challengeprinciples. Animal Behaviour, 53, 925e934.

Mooring, M. S. & Samuel, W. M. 1998a. Tick-removal grooming byelk (Cervus elaphus): testing principles from the programmed-

grooming hypothesis. Canadian Journal of Zoology, 76, 740e750.

Mooring, M. S. & Samuel, W. M. 1998b. Tick defense strategies in

bison: the role of grooming and hair coat. Behaviour, 135,693e718.

Mooring, M. S., McKenzie, A. A. & Hart, B. L. 1996. Grooming in

impala: role of oral grooming in removal of ticks and effects of

ticks in increasing grooming rate. Physiology & Behavior, 59,965e971.

HART & PRYOR: DETERMINANTS OF GROOMING 19

Mooring,M. S., Gavazzi, A. J. &Hart, B. L. 1998. Effects of castrationon grooming of goats. Physiology & Behavior, 64, 707e713.

Mooring, M. S., Benjamin, J. E., Harte, C. R. & Herzog, N. B. 2000.Testing the interspecific body size principle in ungulates: the

smaller they come, the harder they groom. Animal Behaviour, 60,35e45.

Mori, Y., Maeda, K., Sawasaki, T. & Kano, Y. 1985. Photoperiodiccontrol of prolactin secretion in the goat. Japan Journal of Animal

Reproduction, 31, 9e15.

Murray, M. O. 1987. Effects of host grooming on louse populations.

Parasitology Today, 3, 276e278.

Olubayo, R. O., Jono, J., Orinda, G., Groothenius, J. G. & Hart, B. L.1993. Comparative differences in densities of adult ticks as a func-

tion of body size on some East African antelopes. African Journal

of Ecology, 31, 26e34.

Plouzek, C. A. & Trenkle, A. 1991. Growth hormone parameters at

four ages in intact and castrated male and female cattle. DomesticAnimal Endrocrinology, 8, 63e72.

Richmond, G. & Sachs, B. D. 1980. Grooming in Norway rats: thedevelopment and adult expression of a complex motor pattern.

Behaviour, 75, 82e95.

Sachs, B. D. 1988. The development of grooming and its expression

in adult animals. Annals of the New York Academy of Sciences, 525,1e17.

Schmidt-Neilsen, K. 1984. Scaling: Why Is Animal Size So Important?

New York: Cambridge University Press.

Siegel, S. & Castellan, N. J. 1988. Nonparametric Statistics for the

Behavioral Sciences. 2nd edn. Boston: McGraweHill.

Spruijt, B. M., Van Hoof, J. A. R. A. M. & Gispen, W. H. 1992.Ethology and neurobiology of grooming behavior. Physiological

Review, 72, 825e852.

Sutherst, R. W., Maywald, G. F., Kerr, J. D. & Stegeman, D. A.1983. The effect of cattle tick (Boophilus microplus) on the growthof Bos indicus ! B. Taurus steers. Australian Journal of Agricultural

Research, 34, 317e327.

Tanaka, I. 1995. Matrilineal distribution of louse egg-handling

techniques during grooming in free-ranging Japanese macaques.

American Journal of Physiological Anthropology, 98, 197e201.

Uerpmann, H.-P. 1987. The Ancient Distribution of Ungulate

Mammals in the Middle East. Fauna and Archaeological Sites in

Southwest Asia and Northeast Africa. Supplement to the TubingerAtlas of the Front Orients. Wiesbaden: Ludwig Reichert Verlag.

Wiesbroth, S. H., Friedman, S. & Powell, M. 1974. The parasiticecology of the rodent mite Myobia mulculi. I. Grooming factors.

Laboratory Animal Science, 24, 510e516.

Zohary, D., Tchernov, E. & Horwitz, L. K. 1998. The role of

unconscious selection in the domestication of sheep and goats.

Journal of the Biological Society, 245, 129e135.