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Developmental and hair-coat determinants of grooming behaviour in goats and sheep
ANIMAL BEHAVIOUR, 2004, 67, 11e19 doi:10.1016/j.anbehav.2003.01.002
Developmental and hair-coat determinants of grooming behaviour in goats and sheep BENJAMI N L. HART & PATRI CI A A. P RYOR
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 other mammalian taxonomic groups. In goats, as in rodents and small felids, self-grooming appears to reflect an underlying endogenous timing mechanism, resulting in what has been referred to as programmed grooming. We tested the prediction from the programmed grooming model that newborn and young goats, Capra hircus, would groom more frequently than similarly maintained conspecific adults. This prediction was upheld in that goat kids, from 2 weeks of age, orally groomed and scratch-groomed significantly 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 of the young was no longer significantly elevated over that of adults recorded at the same time of year. We also tested the predictions that oral grooming in wool sheep, Ovis aries, is inherently programmed and will occur in adults after shearing and in lambs with undeveloped fleece at levels similar to those of ancestral hair sheep and lambs. When fully fleeced adult wool sheep were shorn, they engaged in grooming in a pattern and frequency not different from that of hair sheep with a pelage representative of ancestral sheep. Wool lambs also groomed at a rate similar to that of hair lambs. Therefore, the elevated rate of programmed grooming of newborn and young ungulates appears to reflect their developmental precociousness and consequent exposure, in nature, to ectoparasites. Ó 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Self-grooming is a frequently performed behaviour among rodents, small felids, wild and domestic bovids, cervids and various species of primates. Grooming serves a number of functions, the most notable and widespread being the removal of ectoparasites and cleaning and conditioning the pelage. The effectiveness of self-grooming in removing ectoparasites has been experimentally documented 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 role of 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 is characteristic. In nonprimate species, grooming can generally be divided between scratch grooming of the Correspondence: B. L. Hart, Department of Anatomy, Physiology and Cell Biology, School of Veterinary Medicine, University of California, Davis, CA 95616, U.S.A. (email: [email protected]). 0003e3472/03/$30.00/0
head and neck with the hind feet, claws or hooves and oral grooming with the tongue or teeth. In rodents and cats, in addition to face washing using the front paws, the tongue is used to comb through different areas of the pelage, often in a rostralecaudal progression (Richmond & Sachs 1980; Eckstein & Hart 2000a). In cattle, grooming is performed with the tongue in bouts of licking applied to one area, and in goats and antelope, oral grooming takes the form of scraping the lower incisors through the pelage in bouts of upward motions directed to a single area (Hart et al. 1992; Mooring et al. 1998). The occurrence of self-grooming among several mammalian species appears to reflect an underlying endogenous timing or programming mechanism. In rodents, where this concept has been explored extensively (Fentress 1988; Sachs 1988), recent behavioural analyses of mice with a Hoxb8 mutant gene revealed the occurrence of excessive initiation of grooming as well as overall grooming (Greer & Capecchi 2002), further reinforcing the concept of an endogenous generator for bouts of grooming. Observations on the initiation of grooming in cats are consistent with an innate programming mechanism in this species (Eckstein & Hart 2000a). All of the
11 Ó 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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behavioural studies conducted so far, both in nature and in 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 programming, rather than cutaneous stimulation, as the primary mechanism controlling the initiation of grooming bouts. In work on ungulates, where discrete bouts of grooming are delivered to single areas of the body, the term ‘programmed grooming’ has been used to represent the behavioural manifestation of an innate timing mechanism. Among the derivations or predictions of the programmed grooming model is the body size principle, which predicts that species of smaller body size, with a larger body surface-to-mass ratio than taxonomically related species of larger size, groom more frequently than species of larger body size (Hart et al. 1992; Mooring et al. 2000). The adaptive value of this principle is that by grooming more frequently, animals of smaller size have a lower density of ectoparasites on the body surface than animals of larger size. This protects them from sustaining greater blood volume loss per unit of body mass than they otherwise would with an equivalent density of ectoparasites. Consistent with this programmed grooming model, antelope species of smaller size groom more frequently and carry fewer ectoparasites (ticks) per unit of body surface area than large-bodied antelope species in the same environment (Olubayo et al. 1993). Grooming in response to cutaneous stimulation does, of course, occur; so in reality, such stimulus-driven grooming is superimposed upon programmed grooming. The body size principle also predicts that in species with precocial young that are capable of moving about in an ectoparasite-ridden environment, the young should groom more frequently than adults that have a lower body surface-to-mass ratio. In nature, the more frequent occurrence of grooming would help defend precocial newborns and young against the blood loss from ectoparasites acquired while moving about, which could otherwise impair growth rate and development of the immune system. In keeping with this intraspecific prediction, observations on young impala (Mooring & Hart 1997), elk (Mooring & Samuel 1998a) and bison (Mooring & Samuel 1998b) of a single developmental age found that young animals engaged in oral grooming more frequently than their adult counterparts. A study of the grooming behaviour of small domestic ruminants offers an opportunity to continue to explore some determinants of grooming and predictions of the programmed grooming model that are applicable to wild as well as domestic ungulates. To test the important intraspecific prediction of the body size principle further, we conducted weekly observations on newborn and young goats to determine the threshold surface-to-mass ratio where grooming is no longer significantly elevated over that of adults. We sampled blood plasma of goat kids at various stages of growth to explore a possible correlation in secretion of growth hormone as a mediator of the predicted more frequent grooming in newborns and
young. In wool sheep, Ovis aries, (Klindt et al. 1987) and cattle (Plouzek & Trenkle 1991; McAndrews et al. 1993) there are age-dependent decreases in baseline and pulseamplitude concentrations of growth hormone. However, secretion patterns of this hormone in newborn and young goats have not been systematically explored. A second set of predictions involved wool sheep, where the dense interwoven pelage prevents oral grooming (preliminary observations). Assuming that ancestral hair sheep engaged in oral grooming of all parts of the body, a prediction of the programmed grooming model is that shearing would allow programmed grooming to occur at a rate similar to that of ancestral sheep. The wild ancestors of domestic sheep, namely the West Asiatic mouflon, Ovis orientalis, were historically widely distributed in southwest Asia (Uerpmann 1987). Some extant breeds of sheep, referred to here as hair sheep, have retained much of the ancestral pelage of shorter hairs (Zohary et al. 1998).
EXPERIMENT 1: DEVELOPMENTAL ASPECTS OF GROOMING IN GOATS We monitored developmental changes in grooming rates in male and female goat kids during 1e24 weeks of age.
Methods These studies were conducted at the University of California, Davis, dairy goat facility. Goat kid subjects, comprising eight males and eight females, were observed at 2e7 weeks of age in inside pens and at 8e24 weeks of age in outside pens. The goat kids had been removed from their mothers just after colostrum feeding (1e2 days after birth). For comparison with the kids, six adult female lactating does of the Alpine breed or Alpine-cross were observed. Does were maintained in pens containing a shed for shade and inclement weather, and were provisioned with oat hay and water. Also for comparison, four kids that were left with their dams were observed at 2e8 weeks of age. All goats were free of ectoparasites. We scored oral bouts and episodes in 20-min focal observations only when the subjects were standing. Grooming in goats is performed as a series of upwards scraping movements of the lower incisors directed to one body area. Each grooming movement was referred to as an episode with a series of connected episodes to the same body part referred to as a bout (Hart et al. 1992). Bouts were considered to be terminated when a different behaviour ensued or no grooming occurred for 5 s. Bouts of oral grooming, number of grooming episodes comprising each bout and the part of the body groomed (e.g. front legs, shoulders or rib cage) were recorded during focal observations. Scratch grooming of the head and neck by the hind hooves were scored in bouts; the scratch episodes in young animals were sometimes so rapid that they were difficult to tabulate, so only scratch bouts were scored. All subjects were individually recognized by eartags. For goat kids, two observations were conducted per week, at intervals of at least 2 days, for weeks 2e6, and one
HART & PRYOR: DETERMINANTS OF GROOMING
observation per week for weeks 7e24. We conducted two observations per week on kids with dams through week 8. Weekly means were determined for each goat kid per week and the data were then expressed as mean grooming bouts and episodes per hour. Observations were conducted in midmorning and midafternoon on alternative tests. The first kids were observed in mid-February and the last observation occurred in August. For does, we conducted four to six focal observations per month during AprileAugust, alternating between midmorning and midafternoon observations. Observations on does covered the time span of most observations on young goats. A recent study on dwarf Shiba goats revealed an increase in grooming in does in the autumn compared with the summer (Kakuma et al. 2003). Consequently, monthly means of grooming rates, extrapolated to grooming bouts and episodes per hour, were derived for each doe not only for comparison with young goats but to detect seasonal changes in grooming in does. To estimate the relative body surface-to-mass ratio threshold at which oral and scratch grooming no longer significantly exceeded that of adults, we used the allometric exponent of 0.67 to convert body mass to relative surface area (Schmidt-Neilsen 1984) for various stages in development. The equation for calculating surface area from body mass uses a constant (Meeh coefficient, k) for differences in body shape to allow between-species comparisons. Although body shape undoubtedly differs between young and adult goats, we considered differences in the Meeh coefficient to be insignificant in our analysis, because the coefficient is about the same (k ¼ 10) for a wide variety of species, including those as diverse as dogs and horses (SchmidtNeilsen 1984, page 81). We calculated body surface-tomass ratios for kids on even-numbered weeks through week 24. From these data, we calculated the surface-tomass ratio of kids relative to that of adults during weeks 2e24 (surface-to-mass ratio of kids/surface-to-mass ratio of adults). For growth hormone analyses, we took 2 ml of blood from the jugular vein of goat kids weekly when the kids were 2e6 weeks of age, then biweekly during weeks 7e24. These blood samples, taken on days when there were no behavioural observations, were treated with heparin and centrifuged, and the plasma was stored at 20 (C until growth hormone assays could be conducted on all samples. Plasma growth hormone concentrations were determined by radioimmunoassay as detailed elsewhere for the bovine ( Joke 1978). The parallel between caprine and bovine growth hormone characteristics has been reported elsewhere (Hashizume & Kanematsu 1991). For most statistical analyses, we used the SAS GENMOD Procedure, with logarithmic transformations of data as necessary to achieve normality, and with P values set at 0.05, two tailed. We used a nonparametric Wilcoxon matched-pairs signed-ranks test, two tailed, to compare seasonal differences in grooming in does after a preliminary review of the data revealed an increase in grooming in JulyeAugust compared with AprileJune, and the ManneWhitney test, two tailed, to compare dam-reared
kids with kids reared without dams (Siegel & Castellan 1988).
Results Tests for differences between male and female kids were conducted on a week-by-week basis for weeks 2e24. A difference (P!0:05) between sexes for oral bouts was found only on weeks 15 and 19 (ANOVA: F1;15 ¼ 6:9 and 11.7, respectively). A difference in oral episodes was found only on weeks 4, 15 and 19 (F1;15 ¼ 5:5, 4.9 and 6.0, respectively) and a difference in scratch grooming bouts only on weeks 3, 12, 13 and 19 (F1;15 ¼ 7:7, 6.5, 10.9 and 9.4, respectively). Taking into account the absence of any systematic difference and the likelihood of type I errors with comparisons across each of the 23 weeks, we concluded that there was no difference between male and female kids in any aspect of grooming. In all subsequent analyses, male and female kids were combined. For comparison with adults, and to avoid a confound of seasonal differences in grooming, we compared the grooming data of kids with those of adult females at approximately the same time of year. For statistical purposes, we compared grooming in kids at 2e5 weeks, 6e10 weeks, 11e14 weeks, 15e19 weeks and 20e24 weeks of 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 adult females in these measures when they were 15e24 weeks of age (JulyeAugust). Kids at 2e10 weeks of age also performed significantly more scratch bouts than did adult females in April and May (F1;20 ¼ 32:4 and 4.4, P!0:0001 and 0.05, respectively), but did not differ from adult females in the number of scratch bouts performed when they were 11e24 weeks of age (JuneeAugust). At 2e3 weeks of age, kids oral-groomed at about 10 times the rate of adult females and scratch-groomed at about eight times the 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 than adults (Fig. 1). When scratch grooming in kids was no longer significantly different from that of adults ( June), kids had a 152% (0.38/0.25) greater surface-to-mass ratio than adults, and when oral grooming in kids was no longer 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 grooming rates for each doe in April, May and June with those obtained for July and August. Oral grooming bouts and episodes were significantly higher for JulyeAugust than AprileJune (Wilcoxon matched-pairs signed-ranks test: T ¼ 21, N ¼ 6, P ¼ 0:03); scratch grooming rates, although
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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 for comparison 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 in JulyeAugust (see Discussion) that would not apply to kids, the grooming of adults in August may be a better reference level for comparisons with kids than the monthly
comparisons used above. To address this possibility, we compared the grooming rates of kids with those of adults using August as a baseline for adults, because adult females showed the highest rate of grooming during this time. During week 2, kids oral-groomed and scratch-groomed about two to three times more than adults (Fig. 1). With this comparison, kids differed from adults on oral bouts
HART & PRYOR: DETERMINANTS OF GROOMING
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, respectively). For oral episodes, kids differed from adults in August only for weeks 2e6 (F1;20 ¼ 11:3, 12.9, 9.9, 13.0 and 7.6, P!0:01, 0.01, 0.01, 0.01 and 0.05, respectively), reflecting a decline in oral episodes per bout over the developmental period. Kids differed from adults in August on 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 grooming was no longer elevated over adults, kids had a 180% greater surface-to-mass ratio than adults, and when oral grooming (bouts) was no longer significantly different, the ratio dropped to about 150%. To compare the grooming behaviour of the four kids reared with dams with the grooming behaviour of kids reared without dams, we calculated the mean number of oral bouts, oral episodes and scratch bouts for all grooming observations for weeks 2e8 for each kid. Extrapolated to hourly rates, dam-reared kids delivered a mean of 17.0 oral bouts, 229 oral episodes and 7.3 scratch bouts compared with 20.7, 281 and 11.7, respectively, for the 16 kids reared without dams. These differences were not significant for oral bouts, oral episodes 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, levels of 18.8, 57.6, 3.1, 2.8 and 3.1 ng/ml were typical for samples from the same kid. Samples taken every 15 min from an indwelling venous cannula of a goat, which was not part of this study, showed spikes of 50e60 ng/ml of growth hormone about every 4 h compared with background levels of 1e10 ng/ml. Despite the impracticality of accurately portraying growth hormone secretion patterns or levels with weekly and biweekly sampling, a Pearson correlation conducted between the log of growth hormone and log of oral bouts over the 23 observations 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 low but significant (r21 ¼ 0:14, P ¼ 0:04), and the correlation with 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 wool sheep, which is prevented by a dense fleece, is inherently programmed and will occur after shearing at a level similar to that of the ancestral hair sheep. We allowed 2 weeks after shearing for habituation to the shearing process to occur and for the immediate postshearing change in cutaneous sensory stimulation. The second prediction, related to the first, was that oral grooming in wool sheep lambs, with a short undeveloped fleece, would occur at a level similar to that of ancestral hair sheep lambs, again reflecting an inherently programmed grooming rate.
Methods Wool sheep The 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 studied 2e8 weeks after birth. Preliminary observations of hair sheep and lambs revealed that the pattern of oral grooming in sheep was the same as in goats, with bouts of upward scraping motions of the lower incisors against the pelage. In preliminary observations, to verify the absence of grooming (or grooming attempts) to fleeced areas, we noticed occasional oral bouts delivered to a part of the front or back legs not covered with wool. We conducted focal observations on grooming, consisting of recording oral bouts, oral episodes and scratch bouts, in the same manner as with goats. The head of Suffolk sheep is not covered fully with wool and was not expected to interfere with scratch grooming of the head. For wool ewes, we conducted two 20-min focal observations on each ewe 2 weeks before shearing and six 20-min observations per ewe during weeks 2e4 after shearing at a minimum of 2-day intervals. For wool lambs, we conducted two 20-min observations each week on each lamb for weeks 2e8. Means were determined for ewes before and after shearing and for lambs for weeks 2e8 combined. The data were then expressed as the mean number of grooming bouts and episodes per hour. All observations were conducted with the sheep standing and were equally divided between morning and afternoon observations. We focused on the distribution of grooming bouts to the legs and areas other than the legs in the wool sheep.
Hair sheep We observed hair sheep in a pasture on a private farm 194 km north of the University of California, Davis. These sheep were part of a flock of approximately 150 breeding ewes. The flock consisted of purebred St Croix along with St Croix crossbred sheep (0.75e0.9% St Croix). These sheep had a hair-type pelage on most of the body with some individual variability in degree of wool pelage ranging between 0 and 50%. The degree of wool coverage in these sheep varies depending upon individual, age, physiological status and season (E. Bradford, personal communication). Because the flock size precluded the likelihood of finding the same animal for replicate observations, we conducted only a single focal observation on each subject. The adults in the study comprised 31 ewes that had been eartagged and could be individually identified to avoid repeated observations on the same ewes. Observations took place during the lambing season, allowing single focal observations on 30 lambs 2e7 weeks after birth. To avoid replicate observations, we identified the lambs by association with their dams. Observations on hair sheep were the same as those with wool sheep and consisted of identifying a subject and attempting a focal observation of 20 min. For partial observations of 10 min, and for those of 20 min, all data
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were extrapolated to grooming bouts and episodes per hour. Observations were made at midmorning or early afternoon while the sheep were foraging and standing or moving. Observations were made at 100e150 m, using binoculars, so as not to disturb normal behaviour. Male and female lambs could not be distinguished in the field.
Statistical analyses Based on an obvious physical prevention of grooming by a dense wool fleece, we predicted that shorn wool sheep would orally groom more than unshorn wool sheep. In light of the fact that oral grooming could only increase for wool ewes, and not decrease, after shearing, we used one-tailed nonparametric Fisher’s exact tests, with each subject serving as its own control and P values set at 0.05. For all other tests, we used the SAS GENMOD procedure, logit model with ANOVA tests and t tests, with two-tailed P values set at 0.05. Logarithmic and squareroot transformations were performed as necessary to achieve normality. Because we conducted only one observation per subject for hair sheep, we expected the variance in grooming rates to be much higher than that for the replicate observations on wool ewes and lambs. Therefore, although direct statistical comparison between hair and wool sheep was not possible, we were able to make general comparisons.
ewes, sexes of lambs were combined. Lambs delivered significantly more oral bouts (F1;13 ¼ 5:45, P ¼ 0:036) than did adult shorn ewes. However, the number of oral episodes and scratch bouts of lambs did not significantly exceed 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 the comparison of shorn ewes with hair ewes, the mean grooming rates of wool lambs were similar to those of hair lambs (Fig. 2), although, as with ewes, no statistical comparison was made. The statistical analysis for comparing grooming in hair lambs with grooming in hair ewes took into account that the single focal animal procedure resulted in 25/32 (78%) samples of ewes and 24/37 (64%) lambs with no oral grooming and 23/32 (72%) ewes and 27/37 (73%) lambs with no scratch grooming. A chi-square analysis revealed no difference between lambs and ewes in number of observations with zero for oral bouts and scratch bouts (P ¼ 0:40 and 0.51, respectively). Comparison of just the 13 lambs with the seven ewes that displayed some oral grooming revealed that lambs showed significantly more oral episodes (t18 ¼ 3:26, P ¼ 0:004) but not more oral bouts (t18 ¼ 2:00, P ¼ 0:06) or scratch bouts (t14 ¼ 0:57, P ¼ 0:58) than hair ewes.
DISCUSSION
Results Confirming preliminary observations, the pattern of oral grooming in sheep was the same as that observed in goats, with bouts of upward scraping movements of the lower incisors against the pelage. Usually it was not evident whether primarily the tongue or the lower incisors were used in grooming, but when the observation angle allowed, it was clear that grooming was with the lower incisors. As expected, wool ewes, prior to shearing, did not engage in oral grooming and displayed no ‘grooming intention movements’ towards fleeced areas (Fig. 2). Following shearing, all ewes delivered oral grooming bouts to previously fleeced areas at rates that were significantly higher than those prior to shearing (Wilcoxon matched-pairs signed-ranks test: T ¼ 15, N ¼ 5, P ¼ 0:03, one tailed). Analyses of body areas groomed revealed that the sheared wool ewes devoted a mean of 48% of oral grooming bouts to areas that were previously covered with wool. The relative rates of scratch grooming in wool ewes (to nonfleeced head and neck) did not differ before and after shearing (Fig. 2). Also as predicted, the mean rates of oral and scratch grooming in shorn wool ewes were at least as high as those in hair sheep and may have been even higher (Fig. 2). Analysis of grooming rates of wool lambs revealed no difference between males and females in oral bouts or episodes (ANOVA: F1;62 ¼ 1:05 and 1.22, P ¼ 0:3 and 0.3, respectively). There was a significant difference in scratch bouts (F1;62 ¼ 9:63, P ¼ 0:03), with females delivering more bouts than males. This difference between sexes was considered relatively minor, and for comparison with
The prediction that oral grooming in newborn goat kids would exceed that of conspecific adults was confirmed in goats, where oral grooming in kids was about 10 times, and scratch grooming eight times, greater than that seen in female adults recorded during the same time of year. These findings are consistent with an intrinsic timing mechanism for grooming that changes with developmental stage. The more frequent grooming of newborn goats was significant during the second week and declined gradually to the adult rate. Two-week-old goats had a 230% greater surface-to-mass ratio than adults. When this ratio declined to about 150%, the scratch grooming rate in kids no longer exceeded that of adults, and at 15 weeks of age, when the surface-to-mass ratio in kids dropped to 140%, oral grooming was no longer significantly elevated over adults. In impala, when the surfaceto-mass ratio of the young reaches 130e160% that of adults, their rates of oral grooming do not differ (Mooring & Hart 1997). A similar surface-to-mass threshold for a development effect on oral grooming between species as diverse as wild impala and domesticated goats suggests that a threshold ratio difference of about 150% (or when young are about 30% the mass of adults) may be a general biological variable that would be predictive for other ungulates. This developmental effect on grooming rate is hypothesized to be a reflection of some underlying hormonal or neuropeptide change (Hart 1997). A precedent exists for hormonal alteration of the oral grooming rate from a study of the effects of castration in adult male goats in which the grooming rate is accelerated by removal of the suppressive effects of testosterone (Mooring et al. 1998) and is in turn
HART & PRYOR: DETERMINANTS OF GROOMING
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 for adult hair sheep and lambs.
down-regulated by testosterone supplementation (Kakuma et al. 2003). Although there is a sexually dimorphic difference in grooming rate in adult domestic goats related to the secretion of testosterone (Mooring et al. 1998; Kakuma et al. 2003), the absence of a gender difference in goat kids in the present study between the ages of 2 and 24 weeks could reflect complex interactions between both developmental and seasonal effects on hormone secretion. One candidate for a developmental change is growth hormone secretion. The decline in plasma concentration of growth hormone in kids was significantly correlated with the decline in oral grooming rate, although the correlation was rather weak. With the pulsatile pattern of growth hormone secretions, blood samples taken once a week do not capture the secretory pattern and poorly estimate developmental patterns. In domestic cattle, the decline in circulating growth hormone during the transition from newborn to the juvenile stage is initially due to a reduction in the baseline concentration and later a reduction of pulse amplitude of growth hormone
(McAndrews et al. 1993). Other possibilities for the mediation of a decline in grooming frequency could be neuropeptides such as vasopressin (Meisenberg 1988). The increase in oral grooming in does in JulyeAugust, which was more than double that in AprileJune, is similar to an increase in grooming in the autumn of adult female Japanese Shiba goats, where the increase is also about double that in summer (Kakuma et al. 2003). Because Alpine goats are seasonal in reproduction, the increase could reflect the effects of changing patterns of secretion of ovarian hormones. However, Shiba goats are not seasonal breeders, so the increase in these goats could not be attributed to ovarian hormones. It was suggested that the increase may reflect a ‘release’ from a depressive effect of prolactin, which decreases as days become shorter (Mori et al. 1985; Maeda et al. 1986). Alpine does typical of those in the present study begin to come into oestrus in July and August when one would expect prolactin levels to be declining. In nature, an increase in grooming would cut down on blood protein loss to ectoparasites during gestation, optimizing birth weight of the newborn. During the spring when kids are born, there is an increase in prolactin related to lactation, which might be responsible for the lower grooming rate seen in the present study during AprileJune, allowing for greater vigilance over potential predators of the newborn. It is difficult to say whether the best comparison of grooming rate in kids is with female adults observed during the same month or with female adults observed only during the month when their grooming was most frequent and perhaps occurring at a baseline rate. If the latter comparison were to be used, newborn goats would only be grooming two to three times more frequently than adults, a difference more comparable to that seen in wild impala and North American cervids (see Introduction). Furthermore, the difference between kids and adults in oral grooming would no longer be significant beyond about week 11 when the surface-to-mass ratio of kids reached about 150% that of adults. In the wool sheep, as expected, unshorn ewes did not groom areas covered with fleece or perform ‘grooming intention movements’, but in the 2e4 weeks after shearing, all ewes groomed areas previously covered with wool; 48% of oral grooming bouts were delivered to areas previously covered with wool. Immediately following shearing, the skin undoubtedly presents a different set of cutaneous stimuli than that in the fully fleeced condition and possibly evokes some grooming or rubbing. Thus, we waited until 2 weeks had elapsed before conducting grooming observations. A change in grooming behaviour due to the novelty of having the fleece removed, or a brief ‘catch-up effect’ of having grooming prevented, as seen in cats (Eckstein & Hart 2000a), would not be expected to last as late as 2e4 weeks after shearing when observations were made. Consistent with the concept of an underlying intrinsic generator of grooming bouts, our observations revealed that the grooming rate of shorn wool sheep was similar to that of ancestral hair sheep. Furthermore, the grooming rate of wool lambs (prior to fleece development) was similar to that of hair lambs. The difference in grooming
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rates between lambs and ewes, so evident in the comparison of goat kids with adult females, was not so pronounced and reached significance only for oral bouts (wool sheep) or oral episodes (hair sheep). The absence of a clear statistically significant developmental effect may reflect limitations of the number of subjects available for observations and/or the extent of observations. All the predictions of the programmed grooming model outlined in Introduction were upheld: (1) newborn and young goats groomed significantly more than adults and the difference gradually declined; (2) adult wool sheep that did not orally groom fleeced areas groomed these areas when sheared and at a rate similar to hair sheep with an ancestral type of pelage; and (3) wool lambs orally groomed at a rate similar to that of hair lambs. The elevated grooming rate in newborn and young ungulates, demonstrated in systematic observations on the goats of the present study, and in the more timelimited observations on impala, elk and bison, undoubtedly reflects the adaptive value of such a developmental effect in precocial newborn that are vulnerable to ectoparasite 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 found only one-half to one-fifth as often as in adults (Gallivan et al. 1995). This developmental effect undoubtedly contributes to the growth and survival of young animals in nature in those species where the young are precocious and freely move about in an environment infested with ectoparasites almost as soon as they are born. One would not necessarily expect to see such developmental effects in other mammalian taxa, such as felids and rodents, where the young are altricial and do not move about in ectoparasite-infested environments until they are older. While in the nest, they are presumably protected from ectoparasites by intensive grooming from their mothers (Hart 1990). A study of such species differences in developmental effects of grooming would contribute to a further understanding of the role of grooming in parasite control of animals in nature. Acknowledgments We kindly acknowledge the assistance of Erik Bradford of the University of California, Davis, Department of Animal Science, for advice on breeds of sheep, and Kathy Lewis for permission to conduct behavioural observations on her flock of St Croix sheep. Marcie Linet, Debbie Kress and Kevin Eslinger contributed to behavioural observations. Yukari Takeuchi and Yuji Mori of the University provided guidance on growth hormone analyses, which were conducted by K. Mogi. Kelly Cliff provided data management assistance and Mitch Watnik, of the University of California, Davis Statistical Laboratory, provided statistical assistance.
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 and prolactin 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 prepubertal Holstein bull calves. Journal of Endocrinology, 139, 307e315. Maeda, K. I., Mori, Y. & Kano, Y. 1986. Superior cervical ganglionectomy 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 scratching 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 challenge principles. Animal Behaviour, 53, 925e934. Mooring, M. S. & Samuel, W. M. 1998a. Tick-removal grooming by elk (Cervus elaphus): testing principles from the programmedgrooming 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.
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Mooring, M. S., Gavazzi, A. J. & Hart, B. L. 1998. Effects of castration on 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. Photoperiodic control 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 function 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. Domestic Animal Endrocrinology, 8, 63e72. Richmond, G. & Sachs, B. D. 1980. Grooming in Norway rats: the development 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 growth of 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 Tu¨binger Atlas of the Front Orients. Wiesbaden: Ludwig Reichert Verlag. Wiesbroth, S. H., Friedman, S. & Powell, M. 1974. The parasitic ecology 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.
19
Developmental and hair-coat determinants of grooming behaviour in goats and sheep BENJAMI N L. HART & PATRI CI A A. P RYOR
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 other mammalian taxonomic groups. In goats, as in rodents and small felids, self-grooming appears to reflect an underlying endogenous timing mechanism, resulting in what has been referred to as programmed grooming. We tested the prediction from the programmed grooming model that newborn and young goats, Capra hircus, would groom more frequently than similarly maintained conspecific adults. This prediction was upheld in that goat kids, from 2 weeks of age, orally groomed and scratch-groomed significantly 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 of the young was no longer significantly elevated over that of adults recorded at the same time of year. We also tested the predictions that oral grooming in wool sheep, Ovis aries, is inherently programmed and will occur in adults after shearing and in lambs with undeveloped fleece at levels similar to those of ancestral hair sheep and lambs. When fully fleeced adult wool sheep were shorn, they engaged in grooming in a pattern and frequency not different from that of hair sheep with a pelage representative of ancestral sheep. Wool lambs also groomed at a rate similar to that of hair lambs. Therefore, the elevated rate of programmed grooming of newborn and young ungulates appears to reflect their developmental precociousness and consequent exposure, in nature, to ectoparasites. Ó 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Self-grooming is a frequently performed behaviour among rodents, small felids, wild and domestic bovids, cervids and various species of primates. Grooming serves a number of functions, the most notable and widespread being the removal of ectoparasites and cleaning and conditioning the pelage. The effectiveness of self-grooming in removing ectoparasites has been experimentally documented 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 role of 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 is characteristic. In nonprimate species, grooming can generally be divided between scratch grooming of the Correspondence: B. L. Hart, Department of Anatomy, Physiology and Cell Biology, School of Veterinary Medicine, University of California, Davis, CA 95616, U.S.A. (email: [email protected]). 0003e3472/03/$30.00/0
head and neck with the hind feet, claws or hooves and oral grooming with the tongue or teeth. In rodents and cats, in addition to face washing using the front paws, the tongue is used to comb through different areas of the pelage, often in a rostralecaudal progression (Richmond & Sachs 1980; Eckstein & Hart 2000a). In cattle, grooming is performed with the tongue in bouts of licking applied to one area, and in goats and antelope, oral grooming takes the form of scraping the lower incisors through the pelage in bouts of upward motions directed to a single area (Hart et al. 1992; Mooring et al. 1998). The occurrence of self-grooming among several mammalian species appears to reflect an underlying endogenous timing or programming mechanism. In rodents, where this concept has been explored extensively (Fentress 1988; Sachs 1988), recent behavioural analyses of mice with a Hoxb8 mutant gene revealed the occurrence of excessive initiation of grooming as well as overall grooming (Greer & Capecchi 2002), further reinforcing the concept of an endogenous generator for bouts of grooming. Observations on the initiation of grooming in cats are consistent with an innate programming mechanism in this species (Eckstein & Hart 2000a). All of the
11 Ó 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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behavioural studies conducted so far, both in nature and in 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 programming, rather than cutaneous stimulation, as the primary mechanism controlling the initiation of grooming bouts. In work on ungulates, where discrete bouts of grooming are delivered to single areas of the body, the term ‘programmed grooming’ has been used to represent the behavioural manifestation of an innate timing mechanism. Among the derivations or predictions of the programmed grooming model is the body size principle, which predicts that species of smaller body size, with a larger body surface-to-mass ratio than taxonomically related species of larger size, groom more frequently than species of larger body size (Hart et al. 1992; Mooring et al. 2000). The adaptive value of this principle is that by grooming more frequently, animals of smaller size have a lower density of ectoparasites on the body surface than animals of larger size. This protects them from sustaining greater blood volume loss per unit of body mass than they otherwise would with an equivalent density of ectoparasites. Consistent with this programmed grooming model, antelope species of smaller size groom more frequently and carry fewer ectoparasites (ticks) per unit of body surface area than large-bodied antelope species in the same environment (Olubayo et al. 1993). Grooming in response to cutaneous stimulation does, of course, occur; so in reality, such stimulus-driven grooming is superimposed upon programmed grooming. The body size principle also predicts that in species with precocial young that are capable of moving about in an ectoparasite-ridden environment, the young should groom more frequently than adults that have a lower body surface-to-mass ratio. In nature, the more frequent occurrence of grooming would help defend precocial newborns and young against the blood loss from ectoparasites acquired while moving about, which could otherwise impair growth rate and development of the immune system. In keeping with this intraspecific prediction, observations on young impala (Mooring & Hart 1997), elk (Mooring & Samuel 1998a) and bison (Mooring & Samuel 1998b) of a single developmental age found that young animals engaged in oral grooming more frequently than their adult counterparts. A study of the grooming behaviour of small domestic ruminants offers an opportunity to continue to explore some determinants of grooming and predictions of the programmed grooming model that are applicable to wild as well as domestic ungulates. To test the important intraspecific prediction of the body size principle further, we conducted weekly observations on newborn and young goats to determine the threshold surface-to-mass ratio where grooming is no longer significantly elevated over that of adults. We sampled blood plasma of goat kids at various stages of growth to explore a possible correlation in secretion of growth hormone as a mediator of the predicted more frequent grooming in newborns and
young. In wool sheep, Ovis aries, (Klindt et al. 1987) and cattle (Plouzek & Trenkle 1991; McAndrews et al. 1993) there are age-dependent decreases in baseline and pulseamplitude concentrations of growth hormone. However, secretion patterns of this hormone in newborn and young goats have not been systematically explored. A second set of predictions involved wool sheep, where the dense interwoven pelage prevents oral grooming (preliminary observations). Assuming that ancestral hair sheep engaged in oral grooming of all parts of the body, a prediction of the programmed grooming model is that shearing would allow programmed grooming to occur at a rate similar to that of ancestral sheep. The wild ancestors of domestic sheep, namely the West Asiatic mouflon, Ovis orientalis, were historically widely distributed in southwest Asia (Uerpmann 1987). Some extant breeds of sheep, referred to here as hair sheep, have retained much of the ancestral pelage of shorter hairs (Zohary et al. 1998).
EXPERIMENT 1: DEVELOPMENTAL ASPECTS OF GROOMING IN GOATS We monitored developmental changes in grooming rates in male and female goat kids during 1e24 weeks of age.
Methods These studies were conducted at the University of California, Davis, dairy goat facility. Goat kid subjects, comprising eight males and eight females, were observed at 2e7 weeks of age in inside pens and at 8e24 weeks of age in outside pens. The goat kids had been removed from their mothers just after colostrum feeding (1e2 days after birth). For comparison with the kids, six adult female lactating does of the Alpine breed or Alpine-cross were observed. Does were maintained in pens containing a shed for shade and inclement weather, and were provisioned with oat hay and water. Also for comparison, four kids that were left with their dams were observed at 2e8 weeks of age. All goats were free of ectoparasites. We scored oral bouts and episodes in 20-min focal observations only when the subjects were standing. Grooming in goats is performed as a series of upwards scraping movements of the lower incisors directed to one body area. Each grooming movement was referred to as an episode with a series of connected episodes to the same body part referred to as a bout (Hart et al. 1992). Bouts were considered to be terminated when a different behaviour ensued or no grooming occurred for 5 s. Bouts of oral grooming, number of grooming episodes comprising each bout and the part of the body groomed (e.g. front legs, shoulders or rib cage) were recorded during focal observations. Scratch grooming of the head and neck by the hind hooves were scored in bouts; the scratch episodes in young animals were sometimes so rapid that they were difficult to tabulate, so only scratch bouts were scored. All subjects were individually recognized by eartags. For goat kids, two observations were conducted per week, at intervals of at least 2 days, for weeks 2e6, and one
HART & PRYOR: DETERMINANTS OF GROOMING
observation per week for weeks 7e24. We conducted two observations per week on kids with dams through week 8. Weekly means were determined for each goat kid per week and the data were then expressed as mean grooming bouts and episodes per hour. Observations were conducted in midmorning and midafternoon on alternative tests. The first kids were observed in mid-February and the last observation occurred in August. For does, we conducted four to six focal observations per month during AprileAugust, alternating between midmorning and midafternoon observations. Observations on does covered the time span of most observations on young goats. A recent study on dwarf Shiba goats revealed an increase in grooming in does in the autumn compared with the summer (Kakuma et al. 2003). Consequently, monthly means of grooming rates, extrapolated to grooming bouts and episodes per hour, were derived for each doe not only for comparison with young goats but to detect seasonal changes in grooming in does. To estimate the relative body surface-to-mass ratio threshold at which oral and scratch grooming no longer significantly exceeded that of adults, we used the allometric exponent of 0.67 to convert body mass to relative surface area (Schmidt-Neilsen 1984) for various stages in development. The equation for calculating surface area from body mass uses a constant (Meeh coefficient, k) for differences in body shape to allow between-species comparisons. Although body shape undoubtedly differs between young and adult goats, we considered differences in the Meeh coefficient to be insignificant in our analysis, because the coefficient is about the same (k ¼ 10) for a wide variety of species, including those as diverse as dogs and horses (SchmidtNeilsen 1984, page 81). We calculated body surface-tomass ratios for kids on even-numbered weeks through week 24. From these data, we calculated the surface-tomass ratio of kids relative to that of adults during weeks 2e24 (surface-to-mass ratio of kids/surface-to-mass ratio of adults). For growth hormone analyses, we took 2 ml of blood from the jugular vein of goat kids weekly when the kids were 2e6 weeks of age, then biweekly during weeks 7e24. These blood samples, taken on days when there were no behavioural observations, were treated with heparin and centrifuged, and the plasma was stored at 20 (C until growth hormone assays could be conducted on all samples. Plasma growth hormone concentrations were determined by radioimmunoassay as detailed elsewhere for the bovine ( Joke 1978). The parallel between caprine and bovine growth hormone characteristics has been reported elsewhere (Hashizume & Kanematsu 1991). For most statistical analyses, we used the SAS GENMOD Procedure, with logarithmic transformations of data as necessary to achieve normality, and with P values set at 0.05, two tailed. We used a nonparametric Wilcoxon matched-pairs signed-ranks test, two tailed, to compare seasonal differences in grooming in does after a preliminary review of the data revealed an increase in grooming in JulyeAugust compared with AprileJune, and the ManneWhitney test, two tailed, to compare dam-reared
kids with kids reared without dams (Siegel & Castellan 1988).
Results Tests for differences between male and female kids were conducted on a week-by-week basis for weeks 2e24. A difference (P!0:05) between sexes for oral bouts was found only on weeks 15 and 19 (ANOVA: F1;15 ¼ 6:9 and 11.7, respectively). A difference in oral episodes was found only on weeks 4, 15 and 19 (F1;15 ¼ 5:5, 4.9 and 6.0, respectively) and a difference in scratch grooming bouts only on weeks 3, 12, 13 and 19 (F1;15 ¼ 7:7, 6.5, 10.9 and 9.4, respectively). Taking into account the absence of any systematic difference and the likelihood of type I errors with comparisons across each of the 23 weeks, we concluded that there was no difference between male and female kids in any aspect of grooming. In all subsequent analyses, male and female kids were combined. For comparison with adults, and to avoid a confound of seasonal differences in grooming, we compared the grooming data of kids with those of adult females at approximately the same time of year. For statistical purposes, we compared grooming in kids at 2e5 weeks, 6e10 weeks, 11e14 weeks, 15e19 weeks and 20e24 weeks of 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 adult females in these measures when they were 15e24 weeks of age (JulyeAugust). Kids at 2e10 weeks of age also performed significantly more scratch bouts than did adult females in April and May (F1;20 ¼ 32:4 and 4.4, P!0:0001 and 0.05, respectively), but did not differ from adult females in the number of scratch bouts performed when they were 11e24 weeks of age (JuneeAugust). At 2e3 weeks of age, kids oral-groomed at about 10 times the rate of adult females and scratch-groomed at about eight times the 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 than adults (Fig. 1). When scratch grooming in kids was no longer significantly different from that of adults ( June), kids had a 152% (0.38/0.25) greater surface-to-mass ratio than adults, and when oral grooming in kids was no longer 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 grooming rates for each doe in April, May and June with those obtained for July and August. Oral grooming bouts and episodes were significantly higher for JulyeAugust than AprileJune (Wilcoxon matched-pairs signed-ranks test: T ¼ 21, N ¼ 6, P ¼ 0:03); scratch grooming rates, although
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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 for comparison 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 in JulyeAugust (see Discussion) that would not apply to kids, the grooming of adults in August may be a better reference level for comparisons with kids than the monthly
comparisons used above. To address this possibility, we compared the grooming rates of kids with those of adults using August as a baseline for adults, because adult females showed the highest rate of grooming during this time. During week 2, kids oral-groomed and scratch-groomed about two to three times more than adults (Fig. 1). With this comparison, kids differed from adults on oral bouts
HART & PRYOR: DETERMINANTS OF GROOMING
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, respectively). For oral episodes, kids differed from adults in August only for weeks 2e6 (F1;20 ¼ 11:3, 12.9, 9.9, 13.0 and 7.6, P!0:01, 0.01, 0.01, 0.01 and 0.05, respectively), reflecting a decline in oral episodes per bout over the developmental period. Kids differed from adults in August on 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 grooming was no longer elevated over adults, kids had a 180% greater surface-to-mass ratio than adults, and when oral grooming (bouts) was no longer significantly different, the ratio dropped to about 150%. To compare the grooming behaviour of the four kids reared with dams with the grooming behaviour of kids reared without dams, we calculated the mean number of oral bouts, oral episodes and scratch bouts for all grooming observations for weeks 2e8 for each kid. Extrapolated to hourly rates, dam-reared kids delivered a mean of 17.0 oral bouts, 229 oral episodes and 7.3 scratch bouts compared with 20.7, 281 and 11.7, respectively, for the 16 kids reared without dams. These differences were not significant for oral bouts, oral episodes 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, levels of 18.8, 57.6, 3.1, 2.8 and 3.1 ng/ml were typical for samples from the same kid. Samples taken every 15 min from an indwelling venous cannula of a goat, which was not part of this study, showed spikes of 50e60 ng/ml of growth hormone about every 4 h compared with background levels of 1e10 ng/ml. Despite the impracticality of accurately portraying growth hormone secretion patterns or levels with weekly and biweekly sampling, a Pearson correlation conducted between the log of growth hormone and log of oral bouts over the 23 observations 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 low but significant (r21 ¼ 0:14, P ¼ 0:04), and the correlation with 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 wool sheep, which is prevented by a dense fleece, is inherently programmed and will occur after shearing at a level similar to that of the ancestral hair sheep. We allowed 2 weeks after shearing for habituation to the shearing process to occur and for the immediate postshearing change in cutaneous sensory stimulation. The second prediction, related to the first, was that oral grooming in wool sheep lambs, with a short undeveloped fleece, would occur at a level similar to that of ancestral hair sheep lambs, again reflecting an inherently programmed grooming rate.
Methods Wool sheep The 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 studied 2e8 weeks after birth. Preliminary observations of hair sheep and lambs revealed that the pattern of oral grooming in sheep was the same as in goats, with bouts of upward scraping motions of the lower incisors against the pelage. In preliminary observations, to verify the absence of grooming (or grooming attempts) to fleeced areas, we noticed occasional oral bouts delivered to a part of the front or back legs not covered with wool. We conducted focal observations on grooming, consisting of recording oral bouts, oral episodes and scratch bouts, in the same manner as with goats. The head of Suffolk sheep is not covered fully with wool and was not expected to interfere with scratch grooming of the head. For wool ewes, we conducted two 20-min focal observations on each ewe 2 weeks before shearing and six 20-min observations per ewe during weeks 2e4 after shearing at a minimum of 2-day intervals. For wool lambs, we conducted two 20-min observations each week on each lamb for weeks 2e8. Means were determined for ewes before and after shearing and for lambs for weeks 2e8 combined. The data were then expressed as the mean number of grooming bouts and episodes per hour. All observations were conducted with the sheep standing and were equally divided between morning and afternoon observations. We focused on the distribution of grooming bouts to the legs and areas other than the legs in the wool sheep.
Hair sheep We observed hair sheep in a pasture on a private farm 194 km north of the University of California, Davis. These sheep were part of a flock of approximately 150 breeding ewes. The flock consisted of purebred St Croix along with St Croix crossbred sheep (0.75e0.9% St Croix). These sheep had a hair-type pelage on most of the body with some individual variability in degree of wool pelage ranging between 0 and 50%. The degree of wool coverage in these sheep varies depending upon individual, age, physiological status and season (E. Bradford, personal communication). Because the flock size precluded the likelihood of finding the same animal for replicate observations, we conducted only a single focal observation on each subject. The adults in the study comprised 31 ewes that had been eartagged and could be individually identified to avoid repeated observations on the same ewes. Observations took place during the lambing season, allowing single focal observations on 30 lambs 2e7 weeks after birth. To avoid replicate observations, we identified the lambs by association with their dams. Observations on hair sheep were the same as those with wool sheep and consisted of identifying a subject and attempting a focal observation of 20 min. For partial observations of 10 min, and for those of 20 min, all data
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were extrapolated to grooming bouts and episodes per hour. Observations were made at midmorning or early afternoon while the sheep were foraging and standing or moving. Observations were made at 100e150 m, using binoculars, so as not to disturb normal behaviour. Male and female lambs could not be distinguished in the field.
Statistical analyses Based on an obvious physical prevention of grooming by a dense wool fleece, we predicted that shorn wool sheep would orally groom more than unshorn wool sheep. In light of the fact that oral grooming could only increase for wool ewes, and not decrease, after shearing, we used one-tailed nonparametric Fisher’s exact tests, with each subject serving as its own control and P values set at 0.05. For all other tests, we used the SAS GENMOD procedure, logit model with ANOVA tests and t tests, with two-tailed P values set at 0.05. Logarithmic and squareroot transformations were performed as necessary to achieve normality. Because we conducted only one observation per subject for hair sheep, we expected the variance in grooming rates to be much higher than that for the replicate observations on wool ewes and lambs. Therefore, although direct statistical comparison between hair and wool sheep was not possible, we were able to make general comparisons.
ewes, sexes of lambs were combined. Lambs delivered significantly more oral bouts (F1;13 ¼ 5:45, P ¼ 0:036) than did adult shorn ewes. However, the number of oral episodes and scratch bouts of lambs did not significantly exceed 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 the comparison of shorn ewes with hair ewes, the mean grooming rates of wool lambs were similar to those of hair lambs (Fig. 2), although, as with ewes, no statistical comparison was made. The statistical analysis for comparing grooming in hair lambs with grooming in hair ewes took into account that the single focal animal procedure resulted in 25/32 (78%) samples of ewes and 24/37 (64%) lambs with no oral grooming and 23/32 (72%) ewes and 27/37 (73%) lambs with no scratch grooming. A chi-square analysis revealed no difference between lambs and ewes in number of observations with zero for oral bouts and scratch bouts (P ¼ 0:40 and 0.51, respectively). Comparison of just the 13 lambs with the seven ewes that displayed some oral grooming revealed that lambs showed significantly more oral episodes (t18 ¼ 3:26, P ¼ 0:004) but not more oral bouts (t18 ¼ 2:00, P ¼ 0:06) or scratch bouts (t14 ¼ 0:57, P ¼ 0:58) than hair ewes.
DISCUSSION
Results Confirming preliminary observations, the pattern of oral grooming in sheep was the same as that observed in goats, with bouts of upward scraping movements of the lower incisors against the pelage. Usually it was not evident whether primarily the tongue or the lower incisors were used in grooming, but when the observation angle allowed, it was clear that grooming was with the lower incisors. As expected, wool ewes, prior to shearing, did not engage in oral grooming and displayed no ‘grooming intention movements’ towards fleeced areas (Fig. 2). Following shearing, all ewes delivered oral grooming bouts to previously fleeced areas at rates that were significantly higher than those prior to shearing (Wilcoxon matched-pairs signed-ranks test: T ¼ 15, N ¼ 5, P ¼ 0:03, one tailed). Analyses of body areas groomed revealed that the sheared wool ewes devoted a mean of 48% of oral grooming bouts to areas that were previously covered with wool. The relative rates of scratch grooming in wool ewes (to nonfleeced head and neck) did not differ before and after shearing (Fig. 2). Also as predicted, the mean rates of oral and scratch grooming in shorn wool ewes were at least as high as those in hair sheep and may have been even higher (Fig. 2). Analysis of grooming rates of wool lambs revealed no difference between males and females in oral bouts or episodes (ANOVA: F1;62 ¼ 1:05 and 1.22, P ¼ 0:3 and 0.3, respectively). There was a significant difference in scratch bouts (F1;62 ¼ 9:63, P ¼ 0:03), with females delivering more bouts than males. This difference between sexes was considered relatively minor, and for comparison with
The prediction that oral grooming in newborn goat kids would exceed that of conspecific adults was confirmed in goats, where oral grooming in kids was about 10 times, and scratch grooming eight times, greater than that seen in female adults recorded during the same time of year. These findings are consistent with an intrinsic timing mechanism for grooming that changes with developmental stage. The more frequent grooming of newborn goats was significant during the second week and declined gradually to the adult rate. Two-week-old goats had a 230% greater surface-to-mass ratio than adults. When this ratio declined to about 150%, the scratch grooming rate in kids no longer exceeded that of adults, and at 15 weeks of age, when the surface-to-mass ratio in kids dropped to 140%, oral grooming was no longer significantly elevated over adults. In impala, when the surfaceto-mass ratio of the young reaches 130e160% that of adults, their rates of oral grooming do not differ (Mooring & Hart 1997). A similar surface-to-mass threshold for a development effect on oral grooming between species as diverse as wild impala and domesticated goats suggests that a threshold ratio difference of about 150% (or when young are about 30% the mass of adults) may be a general biological variable that would be predictive for other ungulates. This developmental effect on grooming rate is hypothesized to be a reflection of some underlying hormonal or neuropeptide change (Hart 1997). A precedent exists for hormonal alteration of the oral grooming rate from a study of the effects of castration in adult male goats in which the grooming rate is accelerated by removal of the suppressive effects of testosterone (Mooring et al. 1998) and is in turn
HART & PRYOR: DETERMINANTS OF GROOMING
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 for adult hair sheep and lambs.
down-regulated by testosterone supplementation (Kakuma et al. 2003). Although there is a sexually dimorphic difference in grooming rate in adult domestic goats related to the secretion of testosterone (Mooring et al. 1998; Kakuma et al. 2003), the absence of a gender difference in goat kids in the present study between the ages of 2 and 24 weeks could reflect complex interactions between both developmental and seasonal effects on hormone secretion. One candidate for a developmental change is growth hormone secretion. The decline in plasma concentration of growth hormone in kids was significantly correlated with the decline in oral grooming rate, although the correlation was rather weak. With the pulsatile pattern of growth hormone secretions, blood samples taken once a week do not capture the secretory pattern and poorly estimate developmental patterns. In domestic cattle, the decline in circulating growth hormone during the transition from newborn to the juvenile stage is initially due to a reduction in the baseline concentration and later a reduction of pulse amplitude of growth hormone
(McAndrews et al. 1993). Other possibilities for the mediation of a decline in grooming frequency could be neuropeptides such as vasopressin (Meisenberg 1988). The increase in oral grooming in does in JulyeAugust, which was more than double that in AprileJune, is similar to an increase in grooming in the autumn of adult female Japanese Shiba goats, where the increase is also about double that in summer (Kakuma et al. 2003). Because Alpine goats are seasonal in reproduction, the increase could reflect the effects of changing patterns of secretion of ovarian hormones. However, Shiba goats are not seasonal breeders, so the increase in these goats could not be attributed to ovarian hormones. It was suggested that the increase may reflect a ‘release’ from a depressive effect of prolactin, which decreases as days become shorter (Mori et al. 1985; Maeda et al. 1986). Alpine does typical of those in the present study begin to come into oestrus in July and August when one would expect prolactin levels to be declining. In nature, an increase in grooming would cut down on blood protein loss to ectoparasites during gestation, optimizing birth weight of the newborn. During the spring when kids are born, there is an increase in prolactin related to lactation, which might be responsible for the lower grooming rate seen in the present study during AprileJune, allowing for greater vigilance over potential predators of the newborn. It is difficult to say whether the best comparison of grooming rate in kids is with female adults observed during the same month or with female adults observed only during the month when their grooming was most frequent and perhaps occurring at a baseline rate. If the latter comparison were to be used, newborn goats would only be grooming two to three times more frequently than adults, a difference more comparable to that seen in wild impala and North American cervids (see Introduction). Furthermore, the difference between kids and adults in oral grooming would no longer be significant beyond about week 11 when the surface-to-mass ratio of kids reached about 150% that of adults. In the wool sheep, as expected, unshorn ewes did not groom areas covered with fleece or perform ‘grooming intention movements’, but in the 2e4 weeks after shearing, all ewes groomed areas previously covered with wool; 48% of oral grooming bouts were delivered to areas previously covered with wool. Immediately following shearing, the skin undoubtedly presents a different set of cutaneous stimuli than that in the fully fleeced condition and possibly evokes some grooming or rubbing. Thus, we waited until 2 weeks had elapsed before conducting grooming observations. A change in grooming behaviour due to the novelty of having the fleece removed, or a brief ‘catch-up effect’ of having grooming prevented, as seen in cats (Eckstein & Hart 2000a), would not be expected to last as late as 2e4 weeks after shearing when observations were made. Consistent with the concept of an underlying intrinsic generator of grooming bouts, our observations revealed that the grooming rate of shorn wool sheep was similar to that of ancestral hair sheep. Furthermore, the grooming rate of wool lambs (prior to fleece development) was similar to that of hair lambs. The difference in grooming
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ANIMAL BEHAVIOUR, 67, 1
rates between lambs and ewes, so evident in the comparison of goat kids with adult females, was not so pronounced and reached significance only for oral bouts (wool sheep) or oral episodes (hair sheep). The absence of a clear statistically significant developmental effect may reflect limitations of the number of subjects available for observations and/or the extent of observations. All the predictions of the programmed grooming model outlined in Introduction were upheld: (1) newborn and young goats groomed significantly more than adults and the difference gradually declined; (2) adult wool sheep that did not orally groom fleeced areas groomed these areas when sheared and at a rate similar to hair sheep with an ancestral type of pelage; and (3) wool lambs orally groomed at a rate similar to that of hair lambs. The elevated grooming rate in newborn and young ungulates, demonstrated in systematic observations on the goats of the present study, and in the more timelimited observations on impala, elk and bison, undoubtedly reflects the adaptive value of such a developmental effect in precocial newborn that are vulnerable to ectoparasite 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 found only one-half to one-fifth as often as in adults (Gallivan et al. 1995). This developmental effect undoubtedly contributes to the growth and survival of young animals in nature in those species where the young are precocious and freely move about in an environment infested with ectoparasites almost as soon as they are born. One would not necessarily expect to see such developmental effects in other mammalian taxa, such as felids and rodents, where the young are altricial and do not move about in ectoparasite-infested environments until they are older. While in the nest, they are presumably protected from ectoparasites by intensive grooming from their mothers (Hart 1990). A study of such species differences in developmental effects of grooming would contribute to a further understanding of the role of grooming in parasite control of animals in nature. Acknowledgments We kindly acknowledge the assistance of Erik Bradford of the University of California, Davis, Department of Animal Science, for advice on breeds of sheep, and Kathy Lewis for permission to conduct behavioural observations on her flock of St Croix sheep. Marcie Linet, Debbie Kress and Kevin Eslinger contributed to behavioural observations. Yukari Takeuchi and Yuji Mori of the University provided guidance on growth hormone analyses, which were conducted by K. Mogi. Kelly Cliff provided data management assistance and Mitch Watnik, of the University of California, Davis Statistical Laboratory, provided statistical assistance.
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