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Social preferences of domestic ewes for rams (Ovis aries)
Applied Animal Behaviour Science, 24 (1989) 287-300
287
Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands
S o c i a l P r e f e r e n c e s o f D o m e s t i c E w e s for R a m s
( Ovis aries) D.Q. E S T E P 1, E.O. P R I C E 2, S.J.R. WALLACH 2 and M.R. DALLY 2
~Department of Psychology, University of Georgia, Athens, GA 30602 (U.S.A.) 2Department of Animal Science, University of California, Davis, CA 95616 (U.S.A.) (Accepted for publication 23 June 1989)
ABSTRACT Estep, D.Q., Price, E.O., Wallach, S.J.R. and Dally, M.R., 1989. Social preferences of domestic ewes for rams ( Ovis aries). Appl. Anim. Behav. Sci., 24: 287-300. A series of four experiments was performed to investigate the social preferences of 16 domestic ewes for potential mating partners. Ewe preferences were assessed by measuring the time spent in proximity to each of 2 restrained rams a n d / o r 1 or 2 restrained ewes, in 5- or 20-min tests. In the first experiment, it was shown that oestrous ewes preferred to be in proximity to rams, while anoestrous ewes preferred other ewes. The second experiment showed that ewe preferences were strongly correlated with the rates of ram sexual solicitations and that ewes preferred older, larger rams over younger, smaller rams. The third experiment demonstrated that ewes preferred rams that had a history of higher sexual performance, independent of their rates of sexual solicitation. The fourth experiment demonstrated that the presence of other oestrous ewes interacting with rams can enhance the attractivity of some, but not all rams. Taken together, these results suggest that ewes can have strong preferences for potential mates and that these preferences may account, in part, for the findings that older, larger, more sexually active rams tend to be more reproductively successful. These findings suggest specific management practices which could improve breeding efficiency in domestic flocks.
INTRODUCTION
Oestrous ewes actively seek out rams (Hafez, 1951; Lindsay and Fletcher, 1972 ) and compete with one another to maintain proximity to males (Lindsay and Robinson, 1961a; Bourke, 1967; Mattner et al., 1967). However, there is a paucity of information on the extent to which ewes exhibit preferences for certain rams and the biological factors on which those preferences are based. Key and MacIver (1977) found ewe preferences unrelated to ram breed or rearing experience, but noted that ewes preferred specific individual rams. In contrast, Lees and Weatherhead (1970) noted that Clun Forest ewes strongly preferred rams of their own breed.
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© 1989 Elsevier Science Publishers B.V.
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Carefully controlled preference tests are needed when investigating mate choice in domestic ewes since preferences can be obscured by female-female competition and differential feedback from rams (i.e. ram mate preferences). The present research was designed to investigate the social preferences of ewes for rams in a social context which provided females with the opportunity to express their mate preferences while attempting to limit the influence of the male over those choices. Experiments were designed to address the following questions. (1) Do ewes exhibit stronger preferences for rams (than ewes) when in oestrus than when in anoestrus? (2) Do ewes prefer older, larger rams over younger, smaller rams? (3)Do ewes prefer sexually active rams over sexually inactive rams? (4) Are ewes more attracted to rams who are accompanied by other ewes than rams not accompanied by other ewes? EXPERIMENT 1. SOCIAL PREFERENCES OF EWES IN RELATION TO OESTROUS CONDITION
The purpose of this study was to determine if the social preferences of ewes varied with their oestrous condition.
Materials and methods The subjects were 16 ovariectomized Targhee crossbred ewes, housed at the University of California H o p l a n d Field Station. The ewes were 32-56 months of age at the time of testing. The stimulus ewe was an ovariectomized flock mate of the subjects who had been housed with them at pasture for 2 years. The 2 stimulus rams were of the Targhee breed from the Hopland Field Station. One ram was ~ 20 months of age, the other was aged ~ 8 months. Both were sexually mature, intact and proven sexually active (i.e. achieved numerous ejaculations) in a previous study of ram sexual behaviour (Price, unpublished data, 1987). The ewes were also used in the previous study of ram sexual behaviour and had approximately equal experience with all of the rams used in this and the following experiments. Ewe social preferences were tested in an indoor pen, illustrated in Fig. 1. The pen was constructed of plywood panels, wooden planks and corrugated sheet metal. The long side of each ram holding pen was constructed of welded steel wire-mesh with gaps (2.4X3.1 cm) large enough to allow tactile contact between rams and ewes. The stimulus ewe was tethered to a post opposite to the gate with a halter and a 0.9-m nylon line. The stimulus ewe was 3.3-4.3 m from each of the stimulus rams, while the rams were 2.6-4.9 m from each other. Each ewe was tested twice, once in hormone-induced oestrus and once in anoestrus in the absence of exogenous hormones. The order of testing was counterbalanced with half of the ewes tested first in oestrus and the other half tested first in anoestrus. The tests were conducted 1 week apart in late October
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6.1m
EWE TETHER POST
3.7m •,.,..,.
RAM
HOLDING PENS 0.5m
Fig. 1. D i a g r a m o f t h e ewe m a t e p r e f e r e n c e t e s t i n g pen.
1987. The subjects were brought into oestrus with two intramuscular injections of 25 mg of progesterone (dissolved in corn oil ), 48 h apart, followed by a single injection of 200/tg of oestradiol benzoate 48 h after the last progesterone injection and 24 h before the start of behavioural testing. On the morning of preference testing, each ewe was screened for behavioural receptivity by pairing her with a teaser ram that was allowed to mount, but not intromit or ejaculate. Receptive females stood quietly while teasers mounted; unreceptive females avoided mounting. Only receptive ewes were tested. Preference tests lasted 20 min and began with the introduction of the ewe into the pen with the 2 rams and the ewe. Ewe preferences were measured in 3 ways: (1) the total number of seconds that the ewe spent within one body length of the 3 stimulus animals; (2) the frequency of contact investigations by the subject ewe of the stimulus ewe or the stimulus rams; (3) the frequency of non-contact investigations of the stimulus animals while within one body length of them. The second measure included licking, nuzzling, kicking a n d / or pawing the stimulus animal, and the third measure included orienting the head to the stimulus animal, orienting the anogenital region to the stimulus animal while orienting the head toward the stimulus animal, sniffing a n d / o r tail wagging. Banks (1964) has defined these categories previously and has identified them as patterns of female courtship behaviour. The data for all three measures were analyzed using repeated measures analyses of variance for a switch back design (Gill, 1978). Results and discussion
The data for time in proximity showed considerable variability between conditions and were adjusted to achieve homogeneity of variance with natural log
D.Q. ESTEP ET AL.
290 TABLE 1 Results of analysis of variance for Experiment 1 Source of variance
df
F
Test order (T) Sex (S) Oestrous condition (C)
1,13 1,13 1,13 1,13 1,13 1,13 1,13
0.32 1.63 0.63 3.46 5.38* 15.45" 0.14
T×C T× S CXS
TxS×C *P < 0.05. TABLE 2
Mean and SE for the time (s) spent in proximity to rams or stimulus ewes by oestrous or anoestrous ewes Stimulus animal
Ewe condition Oestrous
Rams
303.3 _+78.9 a
Ewe
245.8 _+88.4 a'b
Anoestrous 79.9 _+27.5 b 398.6 _+78.1 a
"'bMeans not sharing a common superscript differ significantly ( P < 0.05).
transformation of the data (Gill, 1978). Data for contact and non-contact investigation needed no adjustment. Analysis of time in proximity revealed significant interaction effects for test order by sex of the stimulus animal and for oestrous condition by sex of the stimulus animal (see Table 1 ). The interaction effect of test order by sex was not readily interpretable and was not examined further. The interaction effect of oestrous condition by sex of the stimulus animal was further analyzed with Bonferroni t-statistics for planned comparisons (Gill, 1978). These showed that oestrous ewes spent more time in proximity to rams than did anoestrous ewes and that anoestrous ewes spent more time in proximity to the stimulus ewe than to the rams (Table 2). Analyses of contact and non-contact investigation by ewes to stimulus animals revealed no significant main effects or interactions for either variable. During all oestrous tests, ewes demonstrated a preference for 1 ram over the other by spending more time within one body length of the former. Thirteen of the 16 ewes (81%) showed the same preference during the first 5 min as they did for the entire 20 min. This suggests that ewe social preferences can be as reliably assessed with 5-min preference tests as with 20-min tests.
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EXPERIMENT 2. SOCIAL PREFERENCES OF EWES FOR OLDER VERSUS YOUNGER RAMS This experiment was designed to test the hypothesis that ewes would prefer older, larger rams to younger, smaller rams.
Materials and methods The subject ewes and stimulus ewe were the same animals used in Experiment 1. The stimulus rams were 4 yearling rams ( ~ 20 months of age) and 4 rams lambs ( ~ 8 months of age), all of the Targhee breed. The rams were all sexually mature, intact and proven sexually active. All ewes had had previous experience with all the rams in several tests of sexual behaviour. Testing occurred in four indoor pens, one of which was the same one used in Experiment 1. The other three pens were identical in construction to the first. Each ewe was given four preference tests, all on the same day, and each with a different pair of rams and the same stimulus ewe. In each test, 1 ram was a yearling, the other was a lamb. Subject ewes were brought into oestrus with exogenous hormone injections as described in Experiment 1. Behavioural receptivity was confirmed prior to testing as in Experiment 1 and then each ewe was rotated through the four tests in a counterbalanced order using a Latin square design (Gill, 1978). Each test lasted 5 min and preferences were measured by the total amount of time in seconds that each ewe spent within one body length of each ram. Male sexual solicitations were also recorded. These included grunting, licking the ewe, naso-nasal contact, nudging the ewe with the head, kicking and pawing the ewe with a foreleg.
Results and discussion In Experiment 1, it was suspected that ram sexual solicitations might be correlated with ewe preferences. To determine this, the frequencies of ram sexual solicitations were treated as a statistical covariate in the Latin square analysis of covariance for repeated measures (Gill, 1978). This analysis revealed significant main effects for test, the specific pair of rams and age of the ram (Table 3). The effect of the covariate was significant both for betweensubject variables and within-subject variables. Examination of the adjusted mean difference (i.e. adjusted by the covariate ) using the Bonferroni t-statistic (Neter and Wasserman, 1974; Gill, 1978) revealed that ewes spent less time with both rams in Test 4 than in either Test 1 or Test 2. Bonferroni t-tests also showed that ewes spent less time with Pair 1 rams than Pair 2 rams or Pair 3 rams (Table 4). Ewes consistently spent
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TABLE 3 Results of analysis of covariance for Experiment 2 Source of variance
df
F
Ewe ( E ) Test number ( T ) R a m Pair ( P ) Covariate between Age of ram (A) A× E A× T
15,41 3,41 3,41 1,41 1,41 15,41 3,41 3,41 1,41
0.96 3.87" 3.54* 22.03* 7.45* 1.66 0.83 0.11 83.99*
A×P Covariate within *P < 0.05.
more time with older, larger rams (128.0 s) than with younger, smaller rams (108.7 s, P < 0.05), even when ram sexual solicitations were covaried out. A Pearson's p r o d u c t - m o m e n t correlation of ram sexual solicitation with ewe proximity time to the ram revealed a large, positive and highly significant correlation (r = 0.815, P < 0.001 ). These results are consistent with previous suggestions that ram sexual "vigour" may influence ewe preferences for rams and that ewes prefer older, larger rams to younger, smaller rams.
TABLE 4 M e a n a n d SE for the time (s) spent in proximity to both rams across different tests a n d with different pairs of rams in E x p e r i m e n t 2 Test 1
2
3
130.6 _+23.8 a
140.5 _+22.5 a
110.7 + 25.7 a'b
4 74.1 _+19.5 b
a,bMeans n o t sharing a common superscript differ significantly ( P < 0.05 ). Pair 1 71.6 +_ 12.4 a
2
3
4
145.5_+ 27.3 b
127.1 _+ 18.9 b
107.8_+ 19.9 a'b
a'bMeans not sharing a common superscript differ significantly ( P < 0.05 ).
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E X P E R I M E N T 3. SOCIAL PREFERENCES OF EWES FOR RAMS OF VARYING SEXUAL PERFORMANCE
This experiment tests the hypothesis that ewes prefer sexually more "vigorous" or "efficient" rams. Ewe preferences were assessed for rams that varied in their sexual performance in prior, independent tests of sexual ability. Materials and methods The subject ewes and the stimulus ewe were the same animals used in Experiments 1 and 2. The stimulus rams were 4 high-performing and 4 low-performing males of Targhee breed bred and maintained at the Hopland Field Station. One pair of high- and low-performing rams were lambs, while the other three pairs were yearlings. High- and low-performing rams were closely matched for body weight as well as age. High-performing rams were defined as those that had a total of at least 20 ejaculations in five previous 30-min tests of copulation. Low-performing rams were defined as those having no ejaculations in five previous 30-min tests. The subject ewes of this study were the same animals used to provide the sexual experience for the stimulus rams. Testing was performed as in Experiment 2; each ewe was tested four times on the same day, each with a different pair of rams (one high performer, one low performer) and the stimulus ewe. Subject ewes were brought into oestrus and screened for behavioural receptivity as in Experiment 2. The testing sequence was counterbalanced using a Latin square design and the same dependent variables were measured as in Experiment 2. Results and discussion The data were analyzed as in Experiment 2 using an analysis of covariance for Latin square design with repeated measures (Gill, 1978). Ram sexual solicitations during the tests were the covariate. The analysis revealed a significant main effect of ewe and of the covariate for between-subject variables. The interaction of pairs of rams by male performance was also significant, as was the covariate for the within-subject variables (Table 5). Comparisons of the adjusted cell means using the Bonferroni t-statistics revealed that even when ram sexual solicitations were accounted for, ewes spent significantly more time with higher performing rams t h a n lower performing rams in all pairs except one (Table 6). The non-significant data did not come from the pair of ram lambs (Pair 1 ), but from ram yearlings. These results are consistent with the hypothesis that ewes prefer rams of' higher sexual performance, vigour or efficiency. Furthermore, these differ-
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TABLE 5 Results of analysis of covariance for Experiment 3 Source of variance
df
F
Ewe (E) Test number (T) Ram pair (P) Covariate between Ram performance (R) R× E RXT
15,41 3,41 3,41 1,41 1,41 15,41 3,41 3,41 1,41
1.94" 0.65 0.43 33.68" 3.75 1.57 0.06 3.17" 95.85
R×P Covariate within
*P < 0.05. TABLE 6 Mean and SE for the time (s) spent in proximity to high- and low-performing rams in different pairs of rams Ram pair 1 2 3 4
Type of ram High
Low
101.2 _+_24.5 105.9 ± 17.0 130.5 ± 22.6 150.5 ± 22.6
39.3 ± 27.8* 77.3 ± 15.3 58.4 ± 9.7* 52.0 ± 6.5*
*P < 0.05. e n c e s c a n n o t be a c c o u n t e d f o r s o l e l y o n t h e b a s i s of d i f f e r e n c e s a m o n g r a m s in sexual solicitation during preference tests. EXPERIMENT 4. SOCIAL PREFERENCES OF EWES FOR RAMS IN THE PRESENCE OR ABSENCE OF OTHER OESTROUS EWES This experiment was designed to test the hypothesis that the presence of o t h e r o e s t r o u s ewes a f f e c t s t h e s o c i a l p r e f e r e n c e s o f ewes for r a m s .
Materials a n d m e t h o d s T h e s u b j e c t ewes w e r e t h e s a m e a n i m a l u s e d in t h e p r e v i o u s t h r e e e x p e r i m e n t s . T w o s t i m u l u s ewes a n d 2 s t i m u l u s r a m s w e r e a l s o used. O n e o f t h e s t i m u l u s e w e s w a s t h e s a m e o n e u s e d in p r e v i o u s e x p e r i m e n t s , t h e o t h e r w a s a flock m a t e of b o t h t h e s u b j e c t ewes a n d t h e o t h e r s t i m u l u s ewe. T h e 2 r a m s
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were both yearlings, matched for weight and copulatory ability in previous tests of sexual performance. Both had been used as high-performing males in Experiment 3. Each ewe was tested four times on the same day, each test varying in the location and number of oestrous ewes present in the test pen. Ram identity and location were not varied. In one test, only 1 oestrous ewe was present and she was tethered next to the ram in the left side pen. In another test, the 1 oestrous ewe was tethered next to the right side ram. In another test, 1 oestrous ewe was tethered to the post equidistant from both rams and not in proximity to either and, in the remaining test, 2 oestrous ewes were tethered to the central post not in proximity to either ram. This last condition was implemented to control for the possibility t h a t 2 animals, regardless of sex; were more attractive t h a n 1 animal. The order of presentation of the tests was counterbalanced using a Latin square design. As in previous experiments, all ewes were brought into oestrus with injections of exogenous hormones and behavioural receptivity was confirmed prior to testing. The same dependent variables were measured as in Experiments 2 and 3.
Results and discussion As in previous experiments, the data were analyzed with an analysis of covariance for L a t i n square design with repeated measures (Gill, 1978). As in previous experiments, the covariate was the frequency of sexual solicitations made by rams to subject ewes. The analysis revealed significant main effects for the stimulus male and the covariate for between-subject variables. The ram by oestrous ewe location interaction was significant, as was the covariate for within-subject variables (Table 7). Comparisons of the adjusted cell means for the ewe location by ram interTABLE 7 Results of analysisof covariancefor Experiment 4 Source of variance
df
F
Ewe (E) Test number (T) Oestrous ewe location (L) Covariate between Ram (R) R XE RX T Rx L Covariate within
15,41 3,41 3,41 1,41 1,41 15,41 3,41 3,41 1,41
0.65 1.33 1.74 8.01" 6.40* 1.28 2.31 3.30* 43.81"
*P < 0.05.
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TABLE 8 Mean and SE for the time (s) spent in proximity to 2 different rams as a function of oestrous ewe location Ewe location
X-20 X-28 Tether post Two ewes at post
Ram X-20
X-28
145.5 _+28.1 100.9_+ 20.5 107.1 + 13.8 100.3 _+26.8
59.4 _+27.6* 117.1 _+26.6 70.5 _+20.9 67.2 Jr 23.8
*P<0.05.
action were made with the Bonferroni t-statistic. T h e y revealed that ewes preferred one ram (X-20) when the oestrous ewe was tethered next to him. However, the subject ewes did not show a significant preference for the other ram (X-28) when the oestrous ewe was tethered next to him. Subject ewes showed no preferences for either ram when 1 or 2 oestrous ewes were tethered at a central location away from both rams (Table 8). These results suggest that the presence of another oestrous ewe in proximity to and interacting with a ram may make some rams more attractive to ewes, even when differences in sexual solicitations by the rams to the subject ewes are accounted for. However, the presence of another oestrous ewe does not always enhance the attractivity of rams and may play only a minor role in the social preferences of ewes, compared with other factors. GENERAL DISCUSSION
Taken together, the results of these four experiments demonstrate that domestic ewes can show strong mate preferences and that these preferences are based on specific biological characteristics of the rams. These preferences are shown even when the behaviour of rams is restricted physically and accounted for statistically. The finding that oestrous ewes preferred the company of rams while anoestrous ewes did not, is consistent with the observations of ram-seeking behaviour reported for wild bighorn and Dall's sheep (Geist, 1971) and domestic sheep observed under both free-ranging and more controlled test conditions (Hafez, 1951; Inkster, 1957; Lindsay and Robinson, 1961a,b; Lindsay, 1966; Lindsay and Fletcher, 1972). These results also parallel the results of Tilbrook (1987a), who found that rams preferred oestrous ewes to anoestrous ewes. Results from Experiment 3 revealed that ewes may have individual preferences that are independent of male characteristics manipulated in this study. However, this effect was not found consistently across experiments, suggesting
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that individual preferences are far less important than other characteristics such as age and/or body size, sexual performance or rates of male sexual solicitation. Key and MacIver (1977) also reported individual preferences among ewes for rams, but they did not speculate as to the nature of these preferences. In Experiment 2, female preferences were found to be highly correlated with the rates of ram sexual solicitations. This is consistent with the hypothesis of Lindsay and Robinson (1961b) that the more sexually vigorous rams are preferred as mating partners. Hulet el al. (1962b) and Tilbrook et al. (1987) reported a high correlation between the rates of ram sexual solicitations and ejaculations. The present results suggest that this correlation may be due in part to female preferences for the highly solicitous rams. It is interesting to note that Tilbrook (1987a) and Tilbrook et al. (1987) found no relationship and a very weak relationship, respectively, between ewe sexual solicitations and ram mating preferences. This suggests that rams and ewes may use different criteria in determining their preferences. Hulet et al. (1962b) reported that ram social dominance and age are also correlated with ejaculation rates, making it difficult to determine the relative importance of these factors (age, dominance or sexual solicitations) independently of each other. Covariance analysis may be one way to assess the relative importance of such confounded variables. In Experiments 2 and 3, the covariance analysis demonstrated that when the variance due to sexual solicitations was accounted for, the factors of age and prior reproductive performance were still important in ewe social preferences. Ewes preferred older rams and those with a history of higher sexual performance, independent of their rates of sexual solicitation. These data are consistent with the hypotheses of Geist ( 1971 ) and Gibson and Jewell (1982) that ewes prefer older, larger rams, and the hypotheses of Lindsay and Robinson (1961b) and Gibson and Jewell (1982) that ewes prefer rams of greater sexual vigour and/or efficiency. One observation from Experiment 3 suggests that ram sexual performance may be more important to ewes than age and/or body size. In that experiment, ewes showed no differences in time spent with one pair of ram lambs vs. two other pairs of ram yearlings presented at different times. The nature of the cues used by ewes to discriminate rams that differ in sexual performance is not clear. They are not the patterns of sexual solicitation shown by the rams in the presence of the ewes, for when differences in sexual solicitations are accounted for, preferences for higher performing rams remain. One possibility is that the ewes individually recognize and remember prior sexual experience with the rams and discriminate among them based on this prior experience. All of the ewes in this experiment had experienced several tests of copulatory behaviour with the stimulus rams used here. Furthermore, Banks (1964) reports that rams can individually recognize and discriminate among ewes that they have recently copulated or not copulated with. Alternatively, ewes may have no specific memory of ram performance, but use other cues
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(e.g. odour) provided by the rams during the preference tests that were unmeasured. Finally, the results of Experiment 4 suggest that the social attractivity of some rams, but not all, may be enhanced simply by the presence of other oestrous ewes interacting with those rams. This suggests that the "harems" of oestrous ewes following rams reported for free-roaming sheep (Bourke, 1967; Mattner et al., 1967) may be one cue that ewes could use to find and discriminate among sexually active rams. If only the more socially dominant rams attract such harems, as reported by Bourke (1967), then such males should attract even more ewes for mating. It is noteworthy that two of the characteristics that were most preferred by ewes, increased age a n d / o r size and increased sexual solicitations, have been found in other studies to be correlated with ram sexual performance (e.g. higher rates of ejaculations). This suggests that ewe mate choice may be partially responsible for differences in reproductive performance among rams. This hypothesis does not negate the role of ram mate choice for specific ewe characteristics (e.g. Hafez, 1951; Key and MacIver, 1977; Tilbrook, 1987a,b; Tilbrook and Lindsay, 1987 ), success in intrasexual competition among ewes for rams (e.g. Lindsay and Robinson, 1961a; Hulet et al., 1962a; Banks, 1964; Mattner et al., 1967) or intrasexual competition among rams for ewes (e.g. Inkster, 1957; Lindsay and Robinson, 1961a; Hulet el al., 1962b; Bourke, 1967; Grubb, 1974). Halliday (1983) has pointed out that mate choice by one sex can exist even in the presence of intense intrasexual competition, both within the more choosy sex and for the less choosy sex. He cites examples in elephant seals (Mirounga angustirostris) (Cox and LeBoeuf, 1977; Cox, 1981) and mottled sculpins (Cottus bairdi) (Brown, 1981 ) where mate choice co-exists with strong intrasexual competition. It is common in multisire breeding flocks for some ewes to be mated an unnecessarily large number of times, while others may not be mated at all (see review by Tilbrook et al., 1987). Since intrasexual competition and mate choice can influence who mates with whom and how often, any breeding management scheme that reduces the significance of these factors should result in a more even distribution of matings and an increase in flock reproductive efficiency. Producers might be able to increase the breeding efficiency of their flocks by grouping females by size to reduce the impact of female-female competition and matching rams with regard to age, size, sexual activity and breed to reduce the effectiveness of female choice. ACKNOWLEDGEMENTS
The authors would like to acknowledge the assistance of John Hay and Gil Dow in maintaining the test subjects. David Lyons provided valuable advice
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in designing this experiment. Thanks are due to Susan Meier for preparing the figure.
REFERENCES Banks, E.M., 1964. Some aspects of sexual behavior in domestic sheep, Ovis aries. Behaviour, 23: 249-279. Bourke, M.E., 1967. A study of mating behaviour of Merino rams. Aust. J. Exp. Agric. Anim. Husb., 7: 203-205. Brown, L., 1981. Patterns of female choice in mottled sculpins (Cottidae, Teleostei). Anim. Behav., 29: 375-382. Cox, C.R., 1981. Agonistic encounters among male elephant seals: frequency, context and the role of female preference. Am. Zool., 21: 197-209. Cox, C.R. and LeBoeuf, B.J., 1977. Female incitation of male competition: a mechanism in sexual selection. Am. Nat., 111: 317-335. Geist, V., 1971. Mountain Sheep. A Study In Behavior and Evolution. University of Chicago Press, Chicago, IL. Gibson, R.M. and Jewell, P.A., 1982. Seman quality, female choice and multiple mating in domestic sheep: A test of Trivers' sexual competence hypothesis. Behaviour, 80:9-31. Gill, J.L., 1978. Design and Analysis of Experiments in Animal and Medical Sciences. Iowa State University Press, Ames, IA. Grubb, P., 1974. Mating activity and the social significance of rams in a feral sheep community. In: V. Geist and F. Walther (Editors), The Behaviour of Ungulates and Its Relation to Management, Vol. 1. IUCN; Morges, Switzerland, pp. 457-476. Hafez, E.S.E., 1951. Mating behaviour in sheep. Nature (London), 167: 777-778. Halliday, T.R., 1983. The study of mate choice. In: P. Bateson (Editor), Mate Choice. Cambridge University Press, Cambridge, pp. 3-32. Hulet, C.V., Blackwell, R.L., Ecranbrack, S.K., Price, D.A. and Wilson, L.-O., 1962a. Mating behavior of the ewe. J. Anim. Sci., 21: 870-874. Hulet, C.V., Ecranbrack, S.K., Blackwell, R.L., Price, D.A. and Wilson, L.-O., 1962b. Mating behavior of the ram in the multi-sire pen. J. Anim. Sci., 21: 865-869. |nkster, I.J., 1957. The mating behaviour of sheep. Sheepfarming Annual, pp. 163-169. Key, C. and MacIver, R.M., 1977. Factors affecting sexual preferences in sheep. Appl. Anim. Ethol., 3: 291. Lees, J.L. and Weatherhead, M., 1970. A note on mating preferences of Clun Forest ewes. Anim. Prod., 12: 173-175. Lindsay, D.R., 1966. Mating behaviour of ewes and its effect on mating efficiency. Anim. Bebav., 14: 419-424. Lindsay, D.R. and Fletcher, I.C., 1972. Ram-seeking activity associated with oestrous behaviour in ewes. Anim. Behav., 20: 452-456. Lindsay, D.R. and Robinson, T.J., 1961a. Studies on the efficiency of mating in the sheep. I. The effect of paddock size and number of rams. J. Agric. Sci., 57: 137-140. Lindsay, D.R. and Robinson, T.J., 1961b. Studies on the efficiency of mating in the sheep. II. The effect of freedom of rams, paddock size, and age of ewes. J. Agric. Sci., 57: 141-145. Mattner, P.E., Braden, A.W.H. and Turnbull, K.E., 1967. Studies in flock mating of sheep. I. Mating Behaviour. Aust. J. Exp. Agric. Anim. Husb., 7: 103-109. Neter, J. and Wasserman, W., 1974. Applied Linear Statistical Models. Regression, Analysis of Variance and Experimental Designs. Richard D. Irwin, Homewood, IL.
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Tilbrook, A.J., 1987a. The influence of factors associated with oestrus on the sexual "attractiveness" of ewes to rams. Appl. Anim. Behav. Sci., 17: 117-128. Tilbrook, A.J., 1987b. Physical and behavioural factors affecting the sexual "attractiveness" of the ewe. Appl. Anim. Behav. Sci., 17: 109-115. Tilbrook, A.J. and Lindsay, D.R., 1987. Differences in the sexual "attractiveness" of oestrous ewes to rams. Appl. Anim. Behav. Sci., 17: 129-138. Tilbrook, A.J., Cameron, A.W.N. and Lindsay, D.R., 1987. The influence of ram mating preferences and social interaction between rams on the proportion of ewes mated at field joining. Appl. Anim. Behav. Sci., 18: 173-184.
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S o c i a l P r e f e r e n c e s o f D o m e s t i c E w e s for R a m s
( Ovis aries) D.Q. E S T E P 1, E.O. P R I C E 2, S.J.R. WALLACH 2 and M.R. DALLY 2
~Department of Psychology, University of Georgia, Athens, GA 30602 (U.S.A.) 2Department of Animal Science, University of California, Davis, CA 95616 (U.S.A.) (Accepted for publication 23 June 1989)
ABSTRACT Estep, D.Q., Price, E.O., Wallach, S.J.R. and Dally, M.R., 1989. Social preferences of domestic ewes for rams ( Ovis aries). Appl. Anim. Behav. Sci., 24: 287-300. A series of four experiments was performed to investigate the social preferences of 16 domestic ewes for potential mating partners. Ewe preferences were assessed by measuring the time spent in proximity to each of 2 restrained rams a n d / o r 1 or 2 restrained ewes, in 5- or 20-min tests. In the first experiment, it was shown that oestrous ewes preferred to be in proximity to rams, while anoestrous ewes preferred other ewes. The second experiment showed that ewe preferences were strongly correlated with the rates of ram sexual solicitations and that ewes preferred older, larger rams over younger, smaller rams. The third experiment demonstrated that ewes preferred rams that had a history of higher sexual performance, independent of their rates of sexual solicitation. The fourth experiment demonstrated that the presence of other oestrous ewes interacting with rams can enhance the attractivity of some, but not all rams. Taken together, these results suggest that ewes can have strong preferences for potential mates and that these preferences may account, in part, for the findings that older, larger, more sexually active rams tend to be more reproductively successful. These findings suggest specific management practices which could improve breeding efficiency in domestic flocks.
INTRODUCTION
Oestrous ewes actively seek out rams (Hafez, 1951; Lindsay and Fletcher, 1972 ) and compete with one another to maintain proximity to males (Lindsay and Robinson, 1961a; Bourke, 1967; Mattner et al., 1967). However, there is a paucity of information on the extent to which ewes exhibit preferences for certain rams and the biological factors on which those preferences are based. Key and MacIver (1977) found ewe preferences unrelated to ram breed or rearing experience, but noted that ewes preferred specific individual rams. In contrast, Lees and Weatherhead (1970) noted that Clun Forest ewes strongly preferred rams of their own breed.
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Carefully controlled preference tests are needed when investigating mate choice in domestic ewes since preferences can be obscured by female-female competition and differential feedback from rams (i.e. ram mate preferences). The present research was designed to investigate the social preferences of ewes for rams in a social context which provided females with the opportunity to express their mate preferences while attempting to limit the influence of the male over those choices. Experiments were designed to address the following questions. (1) Do ewes exhibit stronger preferences for rams (than ewes) when in oestrus than when in anoestrus? (2) Do ewes prefer older, larger rams over younger, smaller rams? (3)Do ewes prefer sexually active rams over sexually inactive rams? (4) Are ewes more attracted to rams who are accompanied by other ewes than rams not accompanied by other ewes? EXPERIMENT 1. SOCIAL PREFERENCES OF EWES IN RELATION TO OESTROUS CONDITION
The purpose of this study was to determine if the social preferences of ewes varied with their oestrous condition.
Materials and methods The subjects were 16 ovariectomized Targhee crossbred ewes, housed at the University of California H o p l a n d Field Station. The ewes were 32-56 months of age at the time of testing. The stimulus ewe was an ovariectomized flock mate of the subjects who had been housed with them at pasture for 2 years. The 2 stimulus rams were of the Targhee breed from the Hopland Field Station. One ram was ~ 20 months of age, the other was aged ~ 8 months. Both were sexually mature, intact and proven sexually active (i.e. achieved numerous ejaculations) in a previous study of ram sexual behaviour (Price, unpublished data, 1987). The ewes were also used in the previous study of ram sexual behaviour and had approximately equal experience with all of the rams used in this and the following experiments. Ewe social preferences were tested in an indoor pen, illustrated in Fig. 1. The pen was constructed of plywood panels, wooden planks and corrugated sheet metal. The long side of each ram holding pen was constructed of welded steel wire-mesh with gaps (2.4X3.1 cm) large enough to allow tactile contact between rams and ewes. The stimulus ewe was tethered to a post opposite to the gate with a halter and a 0.9-m nylon line. The stimulus ewe was 3.3-4.3 m from each of the stimulus rams, while the rams were 2.6-4.9 m from each other. Each ewe was tested twice, once in hormone-induced oestrus and once in anoestrus in the absence of exogenous hormones. The order of testing was counterbalanced with half of the ewes tested first in oestrus and the other half tested first in anoestrus. The tests were conducted 1 week apart in late October
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6.1m
EWE TETHER POST
3.7m •,.,..,.
RAM
HOLDING PENS 0.5m
Fig. 1. D i a g r a m o f t h e ewe m a t e p r e f e r e n c e t e s t i n g pen.
1987. The subjects were brought into oestrus with two intramuscular injections of 25 mg of progesterone (dissolved in corn oil ), 48 h apart, followed by a single injection of 200/tg of oestradiol benzoate 48 h after the last progesterone injection and 24 h before the start of behavioural testing. On the morning of preference testing, each ewe was screened for behavioural receptivity by pairing her with a teaser ram that was allowed to mount, but not intromit or ejaculate. Receptive females stood quietly while teasers mounted; unreceptive females avoided mounting. Only receptive ewes were tested. Preference tests lasted 20 min and began with the introduction of the ewe into the pen with the 2 rams and the ewe. Ewe preferences were measured in 3 ways: (1) the total number of seconds that the ewe spent within one body length of the 3 stimulus animals; (2) the frequency of contact investigations by the subject ewe of the stimulus ewe or the stimulus rams; (3) the frequency of non-contact investigations of the stimulus animals while within one body length of them. The second measure included licking, nuzzling, kicking a n d / or pawing the stimulus animal, and the third measure included orienting the head to the stimulus animal, orienting the anogenital region to the stimulus animal while orienting the head toward the stimulus animal, sniffing a n d / o r tail wagging. Banks (1964) has defined these categories previously and has identified them as patterns of female courtship behaviour. The data for all three measures were analyzed using repeated measures analyses of variance for a switch back design (Gill, 1978). Results and discussion
The data for time in proximity showed considerable variability between conditions and were adjusted to achieve homogeneity of variance with natural log
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290 TABLE 1 Results of analysis of variance for Experiment 1 Source of variance
df
F
Test order (T) Sex (S) Oestrous condition (C)
1,13 1,13 1,13 1,13 1,13 1,13 1,13
0.32 1.63 0.63 3.46 5.38* 15.45" 0.14
T×C T× S CXS
TxS×C *P < 0.05. TABLE 2
Mean and SE for the time (s) spent in proximity to rams or stimulus ewes by oestrous or anoestrous ewes Stimulus animal
Ewe condition Oestrous
Rams
303.3 _+78.9 a
Ewe
245.8 _+88.4 a'b
Anoestrous 79.9 _+27.5 b 398.6 _+78.1 a
"'bMeans not sharing a common superscript differ significantly ( P < 0.05).
transformation of the data (Gill, 1978). Data for contact and non-contact investigation needed no adjustment. Analysis of time in proximity revealed significant interaction effects for test order by sex of the stimulus animal and for oestrous condition by sex of the stimulus animal (see Table 1 ). The interaction effect of test order by sex was not readily interpretable and was not examined further. The interaction effect of oestrous condition by sex of the stimulus animal was further analyzed with Bonferroni t-statistics for planned comparisons (Gill, 1978). These showed that oestrous ewes spent more time in proximity to rams than did anoestrous ewes and that anoestrous ewes spent more time in proximity to the stimulus ewe than to the rams (Table 2). Analyses of contact and non-contact investigation by ewes to stimulus animals revealed no significant main effects or interactions for either variable. During all oestrous tests, ewes demonstrated a preference for 1 ram over the other by spending more time within one body length of the former. Thirteen of the 16 ewes (81%) showed the same preference during the first 5 min as they did for the entire 20 min. This suggests that ewe social preferences can be as reliably assessed with 5-min preference tests as with 20-min tests.
SOCIAL PREFERENCES OF DOMESTIC EWES FOR RAMS
29 ]
EXPERIMENT 2. SOCIAL PREFERENCES OF EWES FOR OLDER VERSUS YOUNGER RAMS This experiment was designed to test the hypothesis that ewes would prefer older, larger rams to younger, smaller rams.
Materials and methods The subject ewes and stimulus ewe were the same animals used in Experiment 1. The stimulus rams were 4 yearling rams ( ~ 20 months of age) and 4 rams lambs ( ~ 8 months of age), all of the Targhee breed. The rams were all sexually mature, intact and proven sexually active. All ewes had had previous experience with all the rams in several tests of sexual behaviour. Testing occurred in four indoor pens, one of which was the same one used in Experiment 1. The other three pens were identical in construction to the first. Each ewe was given four preference tests, all on the same day, and each with a different pair of rams and the same stimulus ewe. In each test, 1 ram was a yearling, the other was a lamb. Subject ewes were brought into oestrus with exogenous hormone injections as described in Experiment 1. Behavioural receptivity was confirmed prior to testing as in Experiment 1 and then each ewe was rotated through the four tests in a counterbalanced order using a Latin square design (Gill, 1978). Each test lasted 5 min and preferences were measured by the total amount of time in seconds that each ewe spent within one body length of each ram. Male sexual solicitations were also recorded. These included grunting, licking the ewe, naso-nasal contact, nudging the ewe with the head, kicking and pawing the ewe with a foreleg.
Results and discussion In Experiment 1, it was suspected that ram sexual solicitations might be correlated with ewe preferences. To determine this, the frequencies of ram sexual solicitations were treated as a statistical covariate in the Latin square analysis of covariance for repeated measures (Gill, 1978). This analysis revealed significant main effects for test, the specific pair of rams and age of the ram (Table 3). The effect of the covariate was significant both for betweensubject variables and within-subject variables. Examination of the adjusted mean difference (i.e. adjusted by the covariate ) using the Bonferroni t-statistic (Neter and Wasserman, 1974; Gill, 1978) revealed that ewes spent less time with both rams in Test 4 than in either Test 1 or Test 2. Bonferroni t-tests also showed that ewes spent less time with Pair 1 rams than Pair 2 rams or Pair 3 rams (Table 4). Ewes consistently spent
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TABLE 3 Results of analysis of covariance for Experiment 2 Source of variance
df
F
Ewe ( E ) Test number ( T ) R a m Pair ( P ) Covariate between Age of ram (A) A× E A× T
15,41 3,41 3,41 1,41 1,41 15,41 3,41 3,41 1,41
0.96 3.87" 3.54* 22.03* 7.45* 1.66 0.83 0.11 83.99*
A×P Covariate within *P < 0.05.
more time with older, larger rams (128.0 s) than with younger, smaller rams (108.7 s, P < 0.05), even when ram sexual solicitations were covaried out. A Pearson's p r o d u c t - m o m e n t correlation of ram sexual solicitation with ewe proximity time to the ram revealed a large, positive and highly significant correlation (r = 0.815, P < 0.001 ). These results are consistent with previous suggestions that ram sexual "vigour" may influence ewe preferences for rams and that ewes prefer older, larger rams to younger, smaller rams.
TABLE 4 M e a n a n d SE for the time (s) spent in proximity to both rams across different tests a n d with different pairs of rams in E x p e r i m e n t 2 Test 1
2
3
130.6 _+23.8 a
140.5 _+22.5 a
110.7 + 25.7 a'b
4 74.1 _+19.5 b
a,bMeans n o t sharing a common superscript differ significantly ( P < 0.05 ). Pair 1 71.6 +_ 12.4 a
2
3
4
145.5_+ 27.3 b
127.1 _+ 18.9 b
107.8_+ 19.9 a'b
a'bMeans not sharing a common superscript differ significantly ( P < 0.05 ).
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E X P E R I M E N T 3. SOCIAL PREFERENCES OF EWES FOR RAMS OF VARYING SEXUAL PERFORMANCE
This experiment tests the hypothesis that ewes prefer sexually more "vigorous" or "efficient" rams. Ewe preferences were assessed for rams that varied in their sexual performance in prior, independent tests of sexual ability. Materials and methods The subject ewes and the stimulus ewe were the same animals used in Experiments 1 and 2. The stimulus rams were 4 high-performing and 4 low-performing males of Targhee breed bred and maintained at the Hopland Field Station. One pair of high- and low-performing rams were lambs, while the other three pairs were yearlings. High- and low-performing rams were closely matched for body weight as well as age. High-performing rams were defined as those that had a total of at least 20 ejaculations in five previous 30-min tests of copulation. Low-performing rams were defined as those having no ejaculations in five previous 30-min tests. The subject ewes of this study were the same animals used to provide the sexual experience for the stimulus rams. Testing was performed as in Experiment 2; each ewe was tested four times on the same day, each with a different pair of rams (one high performer, one low performer) and the stimulus ewe. Subject ewes were brought into oestrus and screened for behavioural receptivity as in Experiment 2. The testing sequence was counterbalanced using a Latin square design and the same dependent variables were measured as in Experiment 2. Results and discussion The data were analyzed as in Experiment 2 using an analysis of covariance for Latin square design with repeated measures (Gill, 1978). Ram sexual solicitations during the tests were the covariate. The analysis revealed a significant main effect of ewe and of the covariate for between-subject variables. The interaction of pairs of rams by male performance was also significant, as was the covariate for the within-subject variables (Table 5). Comparisons of the adjusted cell means using the Bonferroni t-statistics revealed that even when ram sexual solicitations were accounted for, ewes spent significantly more time with higher performing rams t h a n lower performing rams in all pairs except one (Table 6). The non-significant data did not come from the pair of ram lambs (Pair 1 ), but from ram yearlings. These results are consistent with the hypothesis that ewes prefer rams of' higher sexual performance, vigour or efficiency. Furthermore, these differ-
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TABLE 5 Results of analysis of covariance for Experiment 3 Source of variance
df
F
Ewe (E) Test number (T) Ram pair (P) Covariate between Ram performance (R) R× E RXT
15,41 3,41 3,41 1,41 1,41 15,41 3,41 3,41 1,41
1.94" 0.65 0.43 33.68" 3.75 1.57 0.06 3.17" 95.85
R×P Covariate within
*P < 0.05. TABLE 6 Mean and SE for the time (s) spent in proximity to high- and low-performing rams in different pairs of rams Ram pair 1 2 3 4
Type of ram High
Low
101.2 _+_24.5 105.9 ± 17.0 130.5 ± 22.6 150.5 ± 22.6
39.3 ± 27.8* 77.3 ± 15.3 58.4 ± 9.7* 52.0 ± 6.5*
*P < 0.05. e n c e s c a n n o t be a c c o u n t e d f o r s o l e l y o n t h e b a s i s of d i f f e r e n c e s a m o n g r a m s in sexual solicitation during preference tests. EXPERIMENT 4. SOCIAL PREFERENCES OF EWES FOR RAMS IN THE PRESENCE OR ABSENCE OF OTHER OESTROUS EWES This experiment was designed to test the hypothesis that the presence of o t h e r o e s t r o u s ewes a f f e c t s t h e s o c i a l p r e f e r e n c e s o f ewes for r a m s .
Materials a n d m e t h o d s T h e s u b j e c t ewes w e r e t h e s a m e a n i m a l u s e d in t h e p r e v i o u s t h r e e e x p e r i m e n t s . T w o s t i m u l u s ewes a n d 2 s t i m u l u s r a m s w e r e a l s o used. O n e o f t h e s t i m u l u s e w e s w a s t h e s a m e o n e u s e d in p r e v i o u s e x p e r i m e n t s , t h e o t h e r w a s a flock m a t e of b o t h t h e s u b j e c t ewes a n d t h e o t h e r s t i m u l u s ewe. T h e 2 r a m s
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were both yearlings, matched for weight and copulatory ability in previous tests of sexual performance. Both had been used as high-performing males in Experiment 3. Each ewe was tested four times on the same day, each test varying in the location and number of oestrous ewes present in the test pen. Ram identity and location were not varied. In one test, only 1 oestrous ewe was present and she was tethered next to the ram in the left side pen. In another test, the 1 oestrous ewe was tethered next to the right side ram. In another test, 1 oestrous ewe was tethered to the post equidistant from both rams and not in proximity to either and, in the remaining test, 2 oestrous ewes were tethered to the central post not in proximity to either ram. This last condition was implemented to control for the possibility t h a t 2 animals, regardless of sex; were more attractive t h a n 1 animal. The order of presentation of the tests was counterbalanced using a Latin square design. As in previous experiments, all ewes were brought into oestrus with injections of exogenous hormones and behavioural receptivity was confirmed prior to testing. The same dependent variables were measured as in Experiments 2 and 3.
Results and discussion As in previous experiments, the data were analyzed with an analysis of covariance for L a t i n square design with repeated measures (Gill, 1978). As in previous experiments, the covariate was the frequency of sexual solicitations made by rams to subject ewes. The analysis revealed significant main effects for the stimulus male and the covariate for between-subject variables. The ram by oestrous ewe location interaction was significant, as was the covariate for within-subject variables (Table 7). Comparisons of the adjusted cell means for the ewe location by ram interTABLE 7 Results of analysisof covariancefor Experiment 4 Source of variance
df
F
Ewe (E) Test number (T) Oestrous ewe location (L) Covariate between Ram (R) R XE RX T Rx L Covariate within
15,41 3,41 3,41 1,41 1,41 15,41 3,41 3,41 1,41
0.65 1.33 1.74 8.01" 6.40* 1.28 2.31 3.30* 43.81"
*P < 0.05.
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TABLE 8 Mean and SE for the time (s) spent in proximity to 2 different rams as a function of oestrous ewe location Ewe location
X-20 X-28 Tether post Two ewes at post
Ram X-20
X-28
145.5 _+28.1 100.9_+ 20.5 107.1 + 13.8 100.3 _+26.8
59.4 _+27.6* 117.1 _+26.6 70.5 _+20.9 67.2 Jr 23.8
*P<0.05.
action were made with the Bonferroni t-statistic. T h e y revealed that ewes preferred one ram (X-20) when the oestrous ewe was tethered next to him. However, the subject ewes did not show a significant preference for the other ram (X-28) when the oestrous ewe was tethered next to him. Subject ewes showed no preferences for either ram when 1 or 2 oestrous ewes were tethered at a central location away from both rams (Table 8). These results suggest that the presence of another oestrous ewe in proximity to and interacting with a ram may make some rams more attractive to ewes, even when differences in sexual solicitations by the rams to the subject ewes are accounted for. However, the presence of another oestrous ewe does not always enhance the attractivity of rams and may play only a minor role in the social preferences of ewes, compared with other factors. GENERAL DISCUSSION
Taken together, the results of these four experiments demonstrate that domestic ewes can show strong mate preferences and that these preferences are based on specific biological characteristics of the rams. These preferences are shown even when the behaviour of rams is restricted physically and accounted for statistically. The finding that oestrous ewes preferred the company of rams while anoestrous ewes did not, is consistent with the observations of ram-seeking behaviour reported for wild bighorn and Dall's sheep (Geist, 1971) and domestic sheep observed under both free-ranging and more controlled test conditions (Hafez, 1951; Inkster, 1957; Lindsay and Robinson, 1961a,b; Lindsay, 1966; Lindsay and Fletcher, 1972). These results also parallel the results of Tilbrook (1987a), who found that rams preferred oestrous ewes to anoestrous ewes. Results from Experiment 3 revealed that ewes may have individual preferences that are independent of male characteristics manipulated in this study. However, this effect was not found consistently across experiments, suggesting
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that individual preferences are far less important than other characteristics such as age and/or body size, sexual performance or rates of male sexual solicitation. Key and MacIver (1977) also reported individual preferences among ewes for rams, but they did not speculate as to the nature of these preferences. In Experiment 2, female preferences were found to be highly correlated with the rates of ram sexual solicitations. This is consistent with the hypothesis of Lindsay and Robinson (1961b) that the more sexually vigorous rams are preferred as mating partners. Hulet el al. (1962b) and Tilbrook et al. (1987) reported a high correlation between the rates of ram sexual solicitations and ejaculations. The present results suggest that this correlation may be due in part to female preferences for the highly solicitous rams. It is interesting to note that Tilbrook (1987a) and Tilbrook et al. (1987) found no relationship and a very weak relationship, respectively, between ewe sexual solicitations and ram mating preferences. This suggests that rams and ewes may use different criteria in determining their preferences. Hulet et al. (1962b) reported that ram social dominance and age are also correlated with ejaculation rates, making it difficult to determine the relative importance of these factors (age, dominance or sexual solicitations) independently of each other. Covariance analysis may be one way to assess the relative importance of such confounded variables. In Experiments 2 and 3, the covariance analysis demonstrated that when the variance due to sexual solicitations was accounted for, the factors of age and prior reproductive performance were still important in ewe social preferences. Ewes preferred older rams and those with a history of higher sexual performance, independent of their rates of sexual solicitation. These data are consistent with the hypotheses of Geist ( 1971 ) and Gibson and Jewell (1982) that ewes prefer older, larger rams, and the hypotheses of Lindsay and Robinson (1961b) and Gibson and Jewell (1982) that ewes prefer rams of greater sexual vigour and/or efficiency. One observation from Experiment 3 suggests that ram sexual performance may be more important to ewes than age and/or body size. In that experiment, ewes showed no differences in time spent with one pair of ram lambs vs. two other pairs of ram yearlings presented at different times. The nature of the cues used by ewes to discriminate rams that differ in sexual performance is not clear. They are not the patterns of sexual solicitation shown by the rams in the presence of the ewes, for when differences in sexual solicitations are accounted for, preferences for higher performing rams remain. One possibility is that the ewes individually recognize and remember prior sexual experience with the rams and discriminate among them based on this prior experience. All of the ewes in this experiment had experienced several tests of copulatory behaviour with the stimulus rams used here. Furthermore, Banks (1964) reports that rams can individually recognize and discriminate among ewes that they have recently copulated or not copulated with. Alternatively, ewes may have no specific memory of ram performance, but use other cues
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(e.g. odour) provided by the rams during the preference tests that were unmeasured. Finally, the results of Experiment 4 suggest that the social attractivity of some rams, but not all, may be enhanced simply by the presence of other oestrous ewes interacting with those rams. This suggests that the "harems" of oestrous ewes following rams reported for free-roaming sheep (Bourke, 1967; Mattner et al., 1967) may be one cue that ewes could use to find and discriminate among sexually active rams. If only the more socially dominant rams attract such harems, as reported by Bourke (1967), then such males should attract even more ewes for mating. It is noteworthy that two of the characteristics that were most preferred by ewes, increased age a n d / o r size and increased sexual solicitations, have been found in other studies to be correlated with ram sexual performance (e.g. higher rates of ejaculations). This suggests that ewe mate choice may be partially responsible for differences in reproductive performance among rams. This hypothesis does not negate the role of ram mate choice for specific ewe characteristics (e.g. Hafez, 1951; Key and MacIver, 1977; Tilbrook, 1987a,b; Tilbrook and Lindsay, 1987 ), success in intrasexual competition among ewes for rams (e.g. Lindsay and Robinson, 1961a; Hulet et al., 1962a; Banks, 1964; Mattner et al., 1967) or intrasexual competition among rams for ewes (e.g. Inkster, 1957; Lindsay and Robinson, 1961a; Hulet el al., 1962b; Bourke, 1967; Grubb, 1974). Halliday (1983) has pointed out that mate choice by one sex can exist even in the presence of intense intrasexual competition, both within the more choosy sex and for the less choosy sex. He cites examples in elephant seals (Mirounga angustirostris) (Cox and LeBoeuf, 1977; Cox, 1981) and mottled sculpins (Cottus bairdi) (Brown, 1981 ) where mate choice co-exists with strong intrasexual competition. It is common in multisire breeding flocks for some ewes to be mated an unnecessarily large number of times, while others may not be mated at all (see review by Tilbrook et al., 1987). Since intrasexual competition and mate choice can influence who mates with whom and how often, any breeding management scheme that reduces the significance of these factors should result in a more even distribution of matings and an increase in flock reproductive efficiency. Producers might be able to increase the breeding efficiency of their flocks by grouping females by size to reduce the impact of female-female competition and matching rams with regard to age, size, sexual activity and breed to reduce the effectiveness of female choice. ACKNOWLEDGEMENTS
The authors would like to acknowledge the assistance of John Hay and Gil Dow in maintaining the test subjects. David Lyons provided valuable advice
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in designing this experiment. Thanks are due to Susan Meier for preparing the figure.
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Tilbrook, A.J., 1987a. The influence of factors associated with oestrus on the sexual "attractiveness" of ewes to rams. Appl. Anim. Behav. Sci., 17: 117-128. Tilbrook, A.J., 1987b. Physical and behavioural factors affecting the sexual "attractiveness" of the ewe. Appl. Anim. Behav. Sci., 17: 109-115. Tilbrook, A.J. and Lindsay, D.R., 1987. Differences in the sexual "attractiveness" of oestrous ewes to rams. Appl. Anim. Behav. Sci., 17: 129-138. Tilbrook, A.J., Cameron, A.W.N. and Lindsay, D.R., 1987. The influence of ram mating preferences and social interaction between rams on the proportion of ewes mated at field joining. Appl. Anim. Behav. Sci., 18: 173-184.