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Preparturient behavior of confined ewes: time budgets, frequencies, spatial distribution and sequential analysis
Applied Animal Behaviour Science, 34 (1992) 329-344
329
Elsevier Science Publishers B.V., Amsterdam
Preparturient behavior of confined ewes: time budgets, frequencies, spatial distribution and sequential analysis A . C . E c h e v e r r i a,l, H . W . G o n y o u " a n d A . W . G h e n t b
~Department q/Animal Sciences, UniversiO, of Illinois. 1207 H~ Gregoo'Drive. Urbana, IL 61801, USA bDepartment of Ecology. Ethology and Evolution, UniversiO, qflllinois, 505 S. Goodwin, Urbana, IL 61801, USA (Accepted 5 March 1992 )
ABSTRACT Echeverri, A.C., Gonyou, H.W. and Ghent, A.W., 1992. Preparturient behavior of confined ewes: time budgets, frequencies, spatial distribution and sequential analysis..4ppl. Anita. Behav. Sci., 34: 329-344. The objective of this study was to determine and quantify the pattern of behavioral changes which occur prior to parturition in sheep. A total of 15 ewes were observed continually for 12 h prior 1o lambing using time-lapse video recordings. During observations, ewes were housed in a group of eight in a 2.7 m x S . 8 m pen. All observable behaviors were recorded with an electronic evenl recorder. Time budgets and frequencies of behaviors were determined for each 2 h period. Two event sequences for 20 different behaviors were tallied and pooled across ewes for each period. Spatial distributions of the focal ewe and the group were recorded at 5 min intervals for the 12 h prepartum. Ewes spent more time standing during the final 2 h (78% of total time) than 12-10 h before lambing (48%: P< 0.01 ). Time spent sniffing the ground increased during the final 2 h (30.8%) compared with periods of up to 4 h before lambing ( 11.8%: P < 0.01 ). The frequencies of several behaviors were greater ( P < 0.01 ) during the final 2 h period than 12-10 h before lambing: active social interactions, passive interactions, standing up, steps taken, ground sniffing, pawing the ground, circling and flanking. The first period in which a significant difference in activity was observed, compared with 12-10 h prepartum was 8-6 h for time spent standing, 6-4 h for steps taken, 4-2 h for time spent ground sniffing, frequency of standing up, pawing, circling and flanking, and 2-0 h for active and passive social interactions. The observed frequencies of a large number of two-event behavior sequences were found to deviate from their expected values during periods 4-2 and 2-0 h prepartum (P< 0.05 ). Most of the sequences occurring more frequently than expected involved either sniffing of other animals or restlessness in the preparturient ewe, but not both. Restlessness in the preparturient ewe involved either grounddirected investigation or self-directed behaviors and posture changes. Ground sniffing and circling frequently occurred in sequences with any of these general groupings of behavior. Lambing ewes were
Correspondence to." H.W. Gonyou, Department of Animal Sciences, University of Illinois, 1207 W. Gregory Drive, Urbana, IL 61801, USA. ~Present address: Department of Microbiology and Immunology, University of California at Los Angeles, Los Angeles, CA, USA.
© 1992 Elsevier Science Publishers B.V. All rights reserved 0168-1591/92/$05.00
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associated with significantlyfewerpenmates than expectedduring the final 2 h beforeparturition (P< 0.05). Duringthe 12 h prepartum,therewas a significantoverallpattern for ewesand the group to moveawayfromeachotheras lambingbecameimminent(P < 0.05).
INTRODUCTION Lamb mortality is high in commercial operations and has been reported to range from 10 to 20% (Kirk and Anderson, 1982). The majority of these losses occur during parturition and the following 4 days (Dalton et al., 1980; Kirk and Anderson, 1982 ). Several factors are responsible for this low reproductive efficiency. Some lambs, especially those of very high birth weights, die during parturition (Dalton et al., 1980). On the other hand, lambs of very low birth weights are more susceptible to starvation, exposure and desertion (Winfield, 1970 ). The development of highly prolific sheep will require careful management and timely intervention in order to avoid increased lamb death and mismothering during the perinatal period. Early detection of parturition will facilitate good management. Characterization of changes in the behavior of the preparturient ewe should facilitate the early recognition of impending parturition and appropriate management. Most descriptions of preparturient behavior in the ewe have not been based on complete ethograms; they have been mainly qualitative and have concentrated on the periods immediately before expulsion of the fetus and thereafter. Some behavioral changes before parturition that have been described previously include isolation, restlessness and maternal interest in other ewes' lambs (Arnold and Morgan, 1975; Gonyou and Stookey, 1983 ). Few studies have involved ewes in confinement. The purpose of this study was three-fold. First, to quantify changes in the time budgets and frequency of normal and 'preparturient' behaviors of confined ewes prior to lambing. Second, to detect the occurrence of two-event behavioral sequences of interest in the preparturient ewe. Finally, to determine whether ewes that are confined in pens are separated from the rest of the flock as parturition approaches. ANIMALS, MATERIALSAND METHODS
Facilities The study was performed at the sheep farm of the University of Illinois at Urbana-Champaign from December 1985 to March 1986. Ewes were housed in a barn with a southern opening, adjusted for temperature and humidity control. The average m i n i m u m and maximum daily temperatures recorded in the experimental pen were I°C (range - 8 - 7 ° C ) and 10°C (range 3-
PREPARTURIENT BEHAVIOR OF CONFINED EWES
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19 ° C), respectively. The pen measured 2.7 m × 8.8 m and was surrounded by 2.2 m high plywood walls to provide visual isolation from the remainder of the barn. The pen floor was covered with straw bedding. Feed racks were located on both sides along the length of the pen. Every morning, at 08:00 h, the ewes were fed 1.4 kg of alfalfa hay and 0.45 kg of a 14% crude protein ration of corn, oats, soybean meal and wheat bran per ewe. An automatic heated waterer provided continuous access to water.
Animals and management Animals used in the study were Suffolk, Hampshire, Dorset and crossbred ewes. The pen contained eight ewes in late gestation at any given time. Ewes were painted with an identification number, weighed and examined for any abnormalities, before entering the pen. Shortly after lambing, the ewe and her lambs were removed. A gestating ewe was promptly introduced into the pen to replace each lambing female. A total of 70 ewes lambed in the pen during the study. Two criteria were employed to select a total of 15 ewes as experimental subjects: each ewe had to be in the pen for a m i n i m u m of 12 h before lambing and the delivery had to be unassisted. Three of the selected ewes were primiparous. Subjects were divided into three categories according to the time of day at parturition: 00:00-07 : 59 h, 08:00-15 : 59 h and 16:00-23 : 59 h. There were six, four and five ewes, respectively, in these time of day categories.
Behavioral observations Two video cameras were mounted at the north and south ends of the pen. Recording equipment and video monitors were set up in an adjacent room. Ewes were videotaped continually, using time-lapse video recordings at 0.9 frames s-~. Focal animal observations were made of each of the 15 experimental ewes during the 12 h prepartum. Observations were also made at 2624 and 38-36 h prepartum for 13 of the 15 ewes, to determine levels of each behavior during the day before lambing. A behavioral catalogue was constructed by watching the videotapes of several ewes in order to define and name all observable behaviors (Table 1; Lehner, 1979). The 12 h period before lambing for each ewe was divided into six 2 h prepartum periods (i.e. 12-10, 10-8, 8-6, 6-4, 4-2 and 2-0 h prepartum) and these were viewed in a random order. Behaviors were recorded with an electronic event recorder. Data files generated were loaded onto a computer for subsequent analysis to determine the frequency and duration of recorded behaviors. The times spent in the behavioral states of standing, ground sniffing and feeding were calculated using the start and stop times of each state. The frequencies of all behavioral events during each 2 h prepartum period were tal-
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TABLE 1 Catalogue of behaviors observed in ewes during the 12 h prepartum Item
Definition
Behavioral states
Standing Lying Feeding Ground sniffing
Time Time Time Time
interval interval interval interval
between between between between
standing up and lying down lying down and standing up start and stop feeding start and stop ground sniffing
Active social behavior Sniffs lamb Licks lamb Nurses lamb Butts ewe Chases ewe Sniffs vulva Sniffs ewe Chins ewe
Focal Focal Focal Focal Focal Focal Focal Focal
ewe sniffs another female's lamb ewe licks another female's lamb ewe nurses another female's lamb ewe butts another female ewe chases another femalc cwc sniffs another female's vulva ewe sniffs another female ( non-vulvar area ) ewe rubs her chin across another female's back
Passive social behavior Butts focal Chases focal Pushes focal Sniffs local vulva Sniffs local Chins local
Any female butts focal ewe Any female chases focal ewe .Any female pushes focal ewe Any female sniffs local ewe's vulva Any female sniffs focal ewe (non-vulvar arca) Any female rubs her chin across focal's back
Locomotive behavior Stands up Lies down Stretches Turns Steps
Focal Focal Focal Focal Focal
Common preparturient bchaviors Start ground sniffing Stop ground sniffing Short ground sniff Paws Circles Flanks Licks self
Ewe lowers head to the ground and begins to sniff Ewe raises head from ground and stops sniffing Ground sniffing bout lasting less than 7.5 s Ewe scrapes the ground with her forefeet Ewe turns around an imaginary axis, in a circular fashion Ewe rubs her sides with her head Ewe licks herself
Feeding behavior Start feeding Stop feeding Drinks
Ewe starts eating Ewe ceases to eat Ewe drinks at waterer
Behavioral events
ewe gets up from lying position ewe lies down ewe stretches, may be lying or standing ewe changes direction while walking in pen ewe takes an average of two steps, from one to three steps
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lied. Social interactions were classified as active or passive (Table 1 ) and totaled. Analyses of variance (ANOVA) were performed on data for 12 h prepartum, using the General Linear Models program of the Statistical Analysis Systems Institute ( 1985 ). Variables included in the model were ewe, time of day, prepartum period and a period by time of day interaction. Additional ANOVA were performed including periods 26-24 and 38-36 h prepartum. Means separation tests, using least significant differences, were performed if significant effects of interest were found in the previous analyses (Zar, 1984 ).
Behavior sequences Two-event behavior sequences were tallied for a total of 20 behaviors of interest. The behaviors analyzed were lamb sniffing, butting by focal and nonfocal ewes, vulva and body sniffing by focal and non-focal ewes, steps, standing up, lying down, turning, short ground sniffs (less than 7.5 s), straining, pawing, circling, flanking, and start and stop times for longer bouts of ground sniffing and feeding. For complete descriptions of these behaviors, with the exception of straining, see Table 1. Straining involved contraction of the ewe's flanks, often accompanied by stretching of the neck. The data for all ewes within a 2 h prepartum period were pooled. A X-" analysis was performed for each two-event sequence to determine whether the observed frequencies of any of the sequences deviated from their expected values (Lehner, 1979). Expected values for each sequence were estimated as the product of individual probabilities of each event within a given time period. Cells with both expected and observed values of less than five were not included in the results.
Spatial distribution For analysis of spatial distribution patterns, the observation pen was divided into front and back halves with an imaginary line. The spatial distribution of focal ewes and the rest of the group was determined at 5 min intervals for each observation period. An analysis was performed on the number of ewes in the same half of the pen as the focal ewe during each 2 h period of the 12 h before lambing. A second analysis was performed on the sequential changes in spatial distribution of each focal ewe and the majority group to determine movement trends during the last 12 h and the last 4 h prepartum. Four or more of the seven non-focal ewes in one half of the pen constituted the majority group. Associations of each ewe with or away from the majority group for the six 2 h periods ( 12 points h - i × 12 h = 144 points) were arrayed in a long (2 × 144 ) ordered contingency table, subject to simplifying compressions of runs of similar association (Ghent, 1984a). G a m m a coefficients ( G o o d m a n and Kruskal, 1954 ) were calculated from the ordered table for each of the 15 focal
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ewes, separately for the last 12 h and the last 4 h prepartum. Since each gamma coefficient is itselfa paired difference between concordant and disconcordant movements of each ewe and her group, each of the two batches ( 12 h and 4 h ) of 15 coefficients could be tested as a group (Ghent, 1984a ) by Wilcoxon's paired-sample procedure (Wilcoxon and Wilcox, 1964; Zar, 1984 ). The qualities of gamma that suit it especially well to biological research have been reviewed (Ghent, 1984b).
RESULTS
Time budgets and fi'equencies
Standing Preparturient ewes spent more time standing as they neared parturition: an average of 93.7 min (78.1% of time) during the 2-0 h period preceding lambing versus 53.7 min (46.7%) during the 12-10 h period. The first significant indication of this tendency occurred during the 8-6 h prepartum period (Fig. 1). ANOVA showed that this behavior differed significantly among ewes ( P < 0.01 ) and was affected by the interaction between time of day and prepartum period ( P < 0.01 ). Time of day was not a significant determinant of this behavior. Standing
Ground
Sniffing .¢
40
o~
308
A 30
E
"3 ,-
.~
20
o o ,r-, o
o
10
o a.
12-10
10-08
Period
08-06
Before
06-04
04-02
Lambing (h)
02-00
12-10
10-08
08-06
06-04
04-02
02-00
Period Before Lambing (h)
Fig. 1. Time budgets of preparturient ewes for standing and ground sniffing during 2 h periods before parturition. Solid bars indicate periods within 12 h of parturition. Open bars are 24 h prior to the adjacent solid bar. Solid bars with a common letter superscript do not differ. An asterisk indicates a 2 h period which evidenced a significant increase in the behavior over the previous 2 h period.
PREPARTURIENT BEHAVIOR OF CONFINED EWES
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Ground sniffing The amount of time ewes spent ground sniffing increased as parturition approached (Fig. 1). Ewes spent an average of 31.5 min (30.8%) engaging in this behavior during the period 2-0 h versus 11.4 min (10.5%) during the period 12-10 h. The behavior increased significantly 4-2 h prepartum and again during the period 2-0 h. Time of day did affect time spent ground sniffing (P< 0.05 ), but there were no significant effects of ewe or the time of day by period interaction. The number of bouts of ground sniffing increased along with time spent ground sniffing. The first significant increase was observed by the period 4-2 h. During the period 2-0 h, ewes sniffed the ground an average total of 64.8 times, compared with 18.1 times during the period 1210 h. There was no significant time of day effect. Ewe and time of day by period interaction effects approached significance (P< 0.10). Ground sniffing was uncommon the day before parturition. Eating Time spent at the feeder averaged 7.26 min per 2 h during the 12 h preparrum and did not differ among the 2 h periods. Eating behavior showed a significant time of day effect (P<0.01) and time of day by period interaction (P<0.01). Active social interactions The frequency at which preparturient ewes initiated social interactions with their penmates increased dramatically during the period 2-0 h before parturition (Table 2). Ewe (P<0.01) and time of day by period interaction (P<0.01) effects were significant for this behavior, but time of day was not. TABLE 2 F r e q u e n c i e s o f different b e h a v i o r s by ewes d u r i n g 2 h p e r i o d s before p a r t u r i t i o n Behavior
Preparlum period (h) 12-10
Active social interactions P a s s i v e social interactions N u m b e r of t i m e s stood up Steps tak en Pawing Circling Flanking
10-8
8-6
6-4
4-2
2-0
26-24
38-36
1.5 a
1.8 a
1.9 a
3.1 a
8.1 ~
20.1 b
0.5
1.5
1.7 ~
1.1"
1.5 a
2.1 ~
6.5 a'b
13.1 b
1.5
1.8
3.2 a
3.3 ~
3.3 a
3.8 a
5.7 ~'°
10.70
2.6
2.2
110.7 a 4.3 ab 1.3" 3,5"
185.1 b 8.40"c 3.7 ~ 2.5 ~
174.80 14.4 ''d 18.9 b 11.0 b
361.5 c 19.6 o 28.9 c 20.80
60.8 1.6 0.5 2.5
104.2 0.2 0.3 2.9
68.9 a 3.2 "-b 2.4 a 2.1 ~
104.3 ~ 2.4 ~ 1.7 ~ 2.3 ~
M e a n s in rows which do not share a c o m m o n s u p e r s c r i p t are s i g n i f i c a n t l y different ( P < 0.05 )
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A.C. ECHEVERRIET AL.
The frequency of active social interactions on the day before parturition was very low. The breakdown of the different types of active social interactions was as follows: 59.9% sniffing another ewe's vulva, 13.6% sniffing another ewe's body, 12.9% sniffing another ewe's lamb, 5.3% chinning another ewe, 3.0% butting another ewe, 3.0% pushing another ewe, 1.3% chasing another ewe and 1.0% licking another ewe's lamb.
Passive social interactions The frequency of social interactions directed towards the focal ewe also increased during the final 2 h before parturition (Table 2). Ewes differed ( P < 0.01 ) for this behavior, but neither time of day nor time of day by period interaction affected the level of activity. As with active interactions, passive interactions were few on the previous day. The breakdown of the different types of passive social interactions was as follows: 82.8% vulva sniffing, 12.5% body sniffing, 1.6% chinning, 1.6% butting and 1.6% pushing.
Standing up As ewes approached parturition, there was a dramatic increase in the number of times they stood up and lay down (Table 2). The first significant increase was observed during the period 4-2 h. There were significant ewe ( P < 0 . 0 1 ) and time of day by period interaction ( P < 0 . 0 1 ) effects, but no time of day effect. The frequencies during 38-36 and 26-24 h were similar to that during 12-10 h.
Steps The number of steps taken by preparturient ewes increased in manner similar to standing up (Table 2), although the first statistically significant increase was observed earlier, during the period 6-4 h. A second increase occurred during the final 2 h prepartum. There was a significant ewe effect ( P < 0 . 0 1 ) for this variable, but neither time of day nor time of day by period interaction effects. Steps taken the previous day were similar in frequency to those in the periods more than 6 h before birth occurred.
Pawing The number of pawing bouts ewes engaged in increased as the time of parturition approached (Table 2). The first significant increase in pawing occurred by the period 4-2 h during the 12 h interval before lambing. There was no significant time of day effect for this variable; ewe and time of day by period interaction effects approached significance ( P < 0.10). Pawing was infrequent on the day before parturition.
PREPARTURIENT BEHAVIOROF CONFINED EWES
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Circling The number of times preparturient ewes circled also increased significantly as they approached lambing (Table 2). There was a significant increase in circling by the period 4-2 h. ANOVA showed a significant ewe effect ( P < 0.05 ), but no time of day or time of day by period interaction effects for the six 2 h periods before lambing. Circling was observed less than once per hour on the day prior to parturition.
Flanking Flanking increased significantly during the final two, 2 h periods before lambing (Table 2). ANOVA showed a significant ewe effect ( P < 0.01 ), but neither time of day nor time of day by period interaction effects were observed. Flanking on the day before lambing occurred at a rate similar to that from 12 to 4 h prepartum.
Sequential analysis Two-event sequences were analyzed for each time period to test whether their occurrence deviated from expected values. As ewes approached parturition, the numbers of two-event sequences that deviated from their expected frequencies increased substantially (Table 3 ). The two-event sequences that increased significantly over expected values a few hours before lambing are depicted in Fig. 2. These sequences can be roughly divided into those involving sniffing of other animals (social behaviors), ground-directed investigation and self-directed behavior. Two behaviors, circling and ground sniffing, were noteworthy as they occurred in sequences involving all three types of behaviors. Although three-event sequences were not analyzed, it is possible that circling and ground sniffing served as a means of transition between the behavioral groupings. TABLE 3 Number of two-event sequences which deviated from the expected frequencies during each 2 h period before parturition ( P < 0.05 ) Time period (h)
Above expected
Below expected
Total
2-0 4-2 6-4 8-6 10-8 12-10
35 33 12 9 10 9
50 25 8 6 3 4
85 58 20 15 13 13
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A.C.ECHEVERRIETAL.
Fig. 2. Diagram of two-event sequences which occurred at frequencies greater than expected during the 4 h before parturition. GS, ground sniffing: SB, sniffs body; SFB, sniffs focal ewe's body; SFV, sniffs focal ewe's vulva; StGS, stops ground sniffing bout: SV, sniffs vulva.
Spatial analysis The percentage o f non-focal ewes which were associated with the focal ewe in one half o f the pen deviated significantly from 50% only during the period 2 - 0 h ( P < 0 . 0 1 ) . During this period, the focal ewe was with the majority o f ewes in the pen only 40.3% of the time. Focal ewes and the majority groups were then analyzed for m o v e m e n t trends in relation to each other. In only four ewes out o f 15 over the last 12 h, and in only one ewe out o f 15 over the last 4 h, was there an overall tendency for increased proximity o f the focal ewe and the other seven ewes. The Wilcoxon paired tests indicated that the p r e d o m i n a n t trend to increased isolation o f the focal ewe with approaching parturition was statistically significant over the last 12 h (two-sided, P = 0 . 0 2 4 9 ) and more strongly so over the last 4 h (two-sided, P = 0 . 0 0 3 4 ) . A complicating factor in these analyses was that some focal ewes spent prolonged periods resting with or otherwise accompanying minority groups (three or fewer ewes) during the initial 2 - 4 h o f these 12 h studies, thereby weaken-
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ing (Ewes 36 and 70 ) or reversing (Ewes 49, 52 and 56 ) their apparent trends over all 12 h compared to their strong trends to increased isolation during the last 4 h. Only Ewe 63 (an extremely restless animal that moved between majority and minority associations more often than any other) showed a trend to increased proximity with the other ewes during the last 4 h. DISCUSSION
Time budgets and frequencies An ideal behavioral predictor of parturition should show a dramatic change in frequency over time before the event and be relatively unaffected by other factors such as time of day and individual animal. Early evidence of impending parturition would be desirable and previous reports have suggested that behavioral changes are evident as early as 24 h before birth (Atroshi and Osterberg, 1979 ). None of the behaviors observed in this study increased earlier than 8 h prepartum, although observations more than 12 h before birth were limited. Of the behaviors observed, only the frequency of pawing and ground sniffing were unaffected by ewe and time of day or interaction effects. Pawing increased eight-fold during the 6 h prepartum, making it an excellent indicator of parturition. Although Arnold and Morgan ( 1975 ) reported breed differences in pawing behavior, we did not observe any differences among the limited number of ewes observed. Owens et al. (1980) interpreted pawing as a sign of restlessness, while McGlone and Stobart ( 1986 ) suggested that postpartum pawing is a rudiment of aggression. We interpret pawing as a type of nest-building behavior, similar to that observed in sows and other species, which may be related to comfort seeking. Ground sniffing, both the frequency and time involved, tripled during the last 4 h before parturition. This modest increase could limit the usefulness of the behavior as an indicator of impending parturition, but the lack of ewe effects are favorable. Smith (1965) and Sharafeldin et al. (1971) also reported increases in ground sniffing before parturition. The behavior may be related to an attraction to birth fluids which develops 3-13 h before parturition (Levy et al., 1983), as sniffing normally increases after fluids are discharged (Smith, 1965). Several behaviors increased during the final 6 h prepartum, but evidenced significant ewe effects. A five-fold increase in walking, indicated in steps taken, was evident as early as 6 h prepartum. Other reports have described aimless walking, trotting and running (Owens et al., 1980; Shackelton and Haywood, 1985 ), but Fraser ( 1968 ) reported a lack of movement in preparturient ewes. Facility design may affect prepartum movement as Gonyou and Stookey (1985) reported a reduction in steps taken when free-access cubicles were available to groups of confined ewes.
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A.C. ECHEVERRI ET AL.
Other behaviors which followed a pattern similar to walking were flanking and circling. Since these behaviors increased dramatically during the 4 h prepartum and are relatively rare at other times, they should be good indicators of impending birth. Flanking may be related to discomfort caused by contractions while circling may, as with pawing, be related to birth site preparation. Both add to the restlessness reported by other researchers (Wallace, 1949: Shackelton and Haywood, 1985 ). Passive social interactions differed among ewes, while active interactions differed among ewes and with the time of day by period interaction. Time of day effects, or interactions with time of day, limit the usefulness of a behavior as a predictor of parturition, unless there is a dramatic prepartum increase which exceeds that of normal diurnal variation. Both types of social interactions occurred at very high levels during the 2 h before parturition. The preparturient ewes initiated more encounters, including a higher proportion of aggressive interactions, than did non-parturient ewes. Other reports have not noted the increase in social interactions that we observed. It is likely that social interactions are more c o m m o n in confinement conditions in which parturient ewes cannot isolate themselves from each other. Previous reports have indicated that the time spent standing and the frequency of standing up (Wallace, 1949; Owens et al., 1980) increase prior to parturition. Although we observed similar patterns, the increases were relatively small (65% and 300% for time and frequency, respectively). The fact that ewe and time of day by period effects were significant limits the use of these behaviors as predictors of parturition. Our observed lack of effect of impending parturition on feeding behavior, perhaps masked by the time of day effect resulting from our feeding schedule, does not support the use of this behavior, as suggested by Sharafeldin et al. ( 1971 ), as an indicator of parturition.
Sequential analysis The total numbers of two-event sequences that deviated from their expected values increased dramatically as lambing neared. It is possible that as motivational levels increase, sequential events are more likely to be of similar motivational origin and random sequences less frequent. Of interest is the fact that although some sequences occurred more often than expected, a large number occurred less frequently than expected. Those behaviors occurring in sequence may be expected to have a c o m m o n causal factor, or the first stimulates the second. Sequences occurring rarely are likely to consist of behaviors with different causal factors. Sniffing another ewe, or being sniffed by one, often resulted in reciprocation by the recipient. Sniffing of the body led to sniffing of the vulva, but not vice versa, suggesting that sniffing was somewhat goal directed. Social sniff-
PREPARTURIENT BEHAVIOR OF CONFINED EWES
341
ing was only prevalent during the final 2 h before parturition, which coincides with the development of an attraction to birth fluids (Levy et al., 1983 ). The association of these behaviors with each other, the m o v e m e n t from the body to the vulva and the timing of these behaviors all support an interest in birth fluids as a c o m m o n causal factor. The transition to ground sniffing may also be related to interest in birth fluids, but the frequent change to circling is less understandable. Several of the non-social behaviors appear to be interrelated and associated with investigation of the physical environment. Ground sniffing frequently led to, or continued during, walking and pawing of the ground. Circling also led to pawing or the end of a ground-sniffing bout. The transition to lying usually involved the end of a bout of ground sniffing. It would appear that these behaviors are related to investigating the environment in a search for a suitable birth site. Gonyou and Stookey (1985) observed that ewes which choose to give birth in cubicles take fewer steps during the final hour before parturition, perhaps because they have selected a satisfactory birth site. A final group of behaviors appear to be related to the comfort of the ewe. Straining and flanking frequently precede each other, and result in the ewe standing or, if already in the standing posture, ground sniffing or circling. The transition to either the social sniffing behaviors or the environmental investigatory behaviors involves either circling or ground sniffing. In general, sequences involving behaviors from more than one of the groupings delineated above were rare. Some of these sequences are conspicuous by their infrequent occurrence. Social sniffing did not lead to walking, or vice versa. The lack of association between m o v e m e n t and social sniffing indicates that ewes did not try to avoid sniffing by walking away, or move toward ewes with the intent of engaging in sniffing. Although both pawing the ground and flanking are part of the increased restlessness observed in prepartum ewes, they appear to be in separate classes of behaviors. The role of ground sniffing and circling is obviously very important as they serve as transition behaviors among all behavior groups. Behaviors may serve such a role if they share c o m m o n motivational factors with each behavior group. It can easily be envisioned how social sniffing leads to sniffing other surfaces, such as the ground, and how ground sniffing leads to other investigative behaviors such as pawing. The transition among behavior groups through circling is less easily understood. Although circling may appear to be related to flanking, its relationship to social sniffing is less obvious. Circling may be a type of conflict behavior which occurs when motivation levels for other behaviors are high, but neither behavior predominates.
Spatial distribution In a few cases, the group moved away from the focal ewe and in a few others the focal ewe avoided the group, but the most frequent occurrence was one of
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A.¢. ECHEVERR[ ETAL.
mutual avoidance. The group may be disrupted by the high levels of activity and restlessness displayed by the lambing ewe. Another possibility is that nonparturient ewes are repelled by the odor o f a m n i o t i c fluids. The results of the sequential analysis suggest that the focal ewe does not approach the group to initiate social interactions or leave the group to avoid interaction. M o v e m e n t was usually associated with ground sniffing and probably reflected searching for a suitable birth site. These results, although obtained in a confinement situation, support the conclusions of previous workers who stated that the separation of ewes in pastures at the time of parturition could be due to either the m o v e m e n t of the ewe or of the group (Arnold and Morgan, 1975; Stevens et al., 1981).
CONCLUSIONS
Time budgets and frequencies Several behaviors related to parturition, locomotion, social interactions and general activity increase during the 12 h before parturition in confined ewes. The majority of the changes in behavior are first evident 4 h before birth. C o m m o n preparturient behaviors such as pawing, ground sniffing, circling and flanking are least affected by time of day or interaction effects. Pawing is probably the best indicator of impending parturition as it increases an average of eight-fold, beginning 6 h before birth, and does not differ among ewes. Social interactions involving the preparturient ewe increase dramatically during the final 2 h before the lamb is born. The high level of social interactions observed may be related to the high density of animals in a confinement situation. Locomotor activities such as walking and standing up increased, but varied with the ewe involved. These behaviors are not likely to be as reliable predictors of impending parturition. Analysis of the frequencies of two-event behavioral sequences suggests that preparturient behavior involves three distinct groupings. Social sniffing involving the preparturient ewe and another ewe or lamb is probably related to increased interest in birth fluids during the final hours before lambing. Ground sniffing, pawing of the ground and walking during a bout of ground sniffing frequently lead to the selection of a lying site. Flanking and straining appear to be related to internal discomfort, and frequently lead to standing. Both ground sniffing and circling serve as transition behaviors among these three groups. Preparturient ewes become separated from the majority of the flock due to the m o v e m e n t of the ewe, the flock, or both, during the final hours before lambing occurs.
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ACKNOWLEDGMENTS
This study was partially funded by the Illinois Sheep and Wool Marketing Board. We extend appreciation to A. Richard Cobb and his staff at the sheep unit.
REFERENCES Arnold, G.W. and Morgan, P.D., 1975. Behaviour of the ewe and lamb at lambing and its relationship to lamb mortality. Appl. Anita. Ethol., 2: 25-46. Atroshi, F. and Osterberg, S., 1979. The behavior of Finn sheep during and shortly after lambing. Acta Agric. Scand., 29: 258-262. Dalton, D.C., Knight, T.W. and Johnson, D.L., 1980. Lamb survival in sheep breeds on New Zealand hill country. N.Z.J. Agric. Res., 23: 167-173. Fraser, A.F., 1968. Parturition. In: A.F. Fraser (Editor), Reproductive Bebaviour in Ungulates. Academic Press, London/New York, pp. 113-131. Ghent, A.W., 1984a. Gamma as a paired statistic for replicate ordered tables in biology. Am. Midl. Nat., 112: 192-195. Ghent, A.W., 1984b. Examination of five Tau variants suited to ordered contingency tables, from the viewpoint of biological research. Am. Midl. Nat., 112: 332-348. Gonyou, H.W. and Stookey, J.M., 1983. Use of lambing cubicles and the behavior of ewes at parturition. J. Anim. Sci., 56: 787-791. Gonyou, H.W. and Stookey, J.M., 1985. Behavior of parturient ewes in group-lambing pens with and without cubicles. Appl. Anita. Behav. Sci., 14: 163-171. Goodman, L.A. and Kruskal, W.H., 1954. Measures of association for cross classifications. J. Am. Slat. Assoc., 49: 732-764. Kirk, J.H. and Anderson, B.C., 1982. Reducing lamb mortality: a two year study. Vet. Med. Small Anim. Clin., 77: 1247-1252. Lehner, P.N., 1979. Handbook of Ethological Methods. Garland STPM, New York, pp. 24297. Levy, F., Poindron, P. and Le Neindre, P., 1983. Attraction and repulsion by amniotic fluids and their olfactory control in the ewe around parturition. Physiol. Behav., 31: 687-692. McGlone, J.J. and Stobart, R.H., 1986. A quantitative ethogram of behavior of yearling ewes during two hours post-partum. Appl. Anita. Behav. Sci., 16: 157-164. Owens, J.L., Bindon, B.M., Edey, T.N. and Piper, L.R., 1980. Neonatal behaviour in high fecundity "'Booroola'" Merino ewes. Rev. Rural Sci., 4:113-116. Shackelton, D.M. and Haywood, J., 1985. Early mother-young interactions in California bighorn sheep, Ovis canadensis cali/brnia. Can. J. Zool., 63: 868-875. Sharafeldin, M.A., Ragab, M.T. and Kandeel, A.A., 1971. Behaviour of ewes during parturition. J. Agric. Sci., (Camb.) 76: 419-422. Smith, F.V., 1965. Instinct and learning in the attachment of lamb and ewe. Anita. Behav., 13: 84-86. Statistical Analysis Systems Institute, 1985. SAS User's Guide: Statistics, Version 5 edn. SAS Institute, Cary, NC. Stevens, D., Alexander, G. and Lynch, J . J . , 1981. Do Merino ewes seek isolation or shelter at lambing? Appl. Anita. Ethol., 7:149-155. Wallace, L.R., 1949. Observations of lambing behaviour in ewes. Proc. N.Z. Soc. Anim. Prod., 9: 85-96.
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Wilcoxon, F. and Wilcox, R.A., 1964. Some Rapid Approximate Statistical Procedures. Lederle Laboratories, Pearl River, NY, 59 pp. Winfield, C.G., 1970. The effect of stocking intensity at lambing on lamb survival and ewe and lamb behaviour. Proc. Aust. Soc. Anim. Prod., 8: 291-296. Zar, J.H., 1984. Biostatistical Analysis, 2nd revised edn. Prentice Hall, Englewood Cliffs, N J, 718 pp.
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Elsevier Science Publishers B.V., Amsterdam
Preparturient behavior of confined ewes: time budgets, frequencies, spatial distribution and sequential analysis A . C . E c h e v e r r i a,l, H . W . G o n y o u " a n d A . W . G h e n t b
~Department q/Animal Sciences, UniversiO, of Illinois. 1207 H~ Gregoo'Drive. Urbana, IL 61801, USA bDepartment of Ecology. Ethology and Evolution, UniversiO, qflllinois, 505 S. Goodwin, Urbana, IL 61801, USA (Accepted 5 March 1992 )
ABSTRACT Echeverri, A.C., Gonyou, H.W. and Ghent, A.W., 1992. Preparturient behavior of confined ewes: time budgets, frequencies, spatial distribution and sequential analysis..4ppl. Anita. Behav. Sci., 34: 329-344. The objective of this study was to determine and quantify the pattern of behavioral changes which occur prior to parturition in sheep. A total of 15 ewes were observed continually for 12 h prior 1o lambing using time-lapse video recordings. During observations, ewes were housed in a group of eight in a 2.7 m x S . 8 m pen. All observable behaviors were recorded with an electronic evenl recorder. Time budgets and frequencies of behaviors were determined for each 2 h period. Two event sequences for 20 different behaviors were tallied and pooled across ewes for each period. Spatial distributions of the focal ewe and the group were recorded at 5 min intervals for the 12 h prepartum. Ewes spent more time standing during the final 2 h (78% of total time) than 12-10 h before lambing (48%: P< 0.01 ). Time spent sniffing the ground increased during the final 2 h (30.8%) compared with periods of up to 4 h before lambing ( 11.8%: P < 0.01 ). The frequencies of several behaviors were greater ( P < 0.01 ) during the final 2 h period than 12-10 h before lambing: active social interactions, passive interactions, standing up, steps taken, ground sniffing, pawing the ground, circling and flanking. The first period in which a significant difference in activity was observed, compared with 12-10 h prepartum was 8-6 h for time spent standing, 6-4 h for steps taken, 4-2 h for time spent ground sniffing, frequency of standing up, pawing, circling and flanking, and 2-0 h for active and passive social interactions. The observed frequencies of a large number of two-event behavior sequences were found to deviate from their expected values during periods 4-2 and 2-0 h prepartum (P< 0.05 ). Most of the sequences occurring more frequently than expected involved either sniffing of other animals or restlessness in the preparturient ewe, but not both. Restlessness in the preparturient ewe involved either grounddirected investigation or self-directed behaviors and posture changes. Ground sniffing and circling frequently occurred in sequences with any of these general groupings of behavior. Lambing ewes were
Correspondence to." H.W. Gonyou, Department of Animal Sciences, University of Illinois, 1207 W. Gregory Drive, Urbana, IL 61801, USA. ~Present address: Department of Microbiology and Immunology, University of California at Los Angeles, Los Angeles, CA, USA.
© 1992 Elsevier Science Publishers B.V. All rights reserved 0168-1591/92/$05.00
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associated with significantlyfewerpenmates than expectedduring the final 2 h beforeparturition (P< 0.05). Duringthe 12 h prepartum,therewas a significantoverallpattern for ewesand the group to moveawayfromeachotheras lambingbecameimminent(P < 0.05).
INTRODUCTION Lamb mortality is high in commercial operations and has been reported to range from 10 to 20% (Kirk and Anderson, 1982). The majority of these losses occur during parturition and the following 4 days (Dalton et al., 1980; Kirk and Anderson, 1982 ). Several factors are responsible for this low reproductive efficiency. Some lambs, especially those of very high birth weights, die during parturition (Dalton et al., 1980). On the other hand, lambs of very low birth weights are more susceptible to starvation, exposure and desertion (Winfield, 1970 ). The development of highly prolific sheep will require careful management and timely intervention in order to avoid increased lamb death and mismothering during the perinatal period. Early detection of parturition will facilitate good management. Characterization of changes in the behavior of the preparturient ewe should facilitate the early recognition of impending parturition and appropriate management. Most descriptions of preparturient behavior in the ewe have not been based on complete ethograms; they have been mainly qualitative and have concentrated on the periods immediately before expulsion of the fetus and thereafter. Some behavioral changes before parturition that have been described previously include isolation, restlessness and maternal interest in other ewes' lambs (Arnold and Morgan, 1975; Gonyou and Stookey, 1983 ). Few studies have involved ewes in confinement. The purpose of this study was three-fold. First, to quantify changes in the time budgets and frequency of normal and 'preparturient' behaviors of confined ewes prior to lambing. Second, to detect the occurrence of two-event behavioral sequences of interest in the preparturient ewe. Finally, to determine whether ewes that are confined in pens are separated from the rest of the flock as parturition approaches. ANIMALS, MATERIALSAND METHODS
Facilities The study was performed at the sheep farm of the University of Illinois at Urbana-Champaign from December 1985 to March 1986. Ewes were housed in a barn with a southern opening, adjusted for temperature and humidity control. The average m i n i m u m and maximum daily temperatures recorded in the experimental pen were I°C (range - 8 - 7 ° C ) and 10°C (range 3-
PREPARTURIENT BEHAVIOR OF CONFINED EWES
331
19 ° C), respectively. The pen measured 2.7 m × 8.8 m and was surrounded by 2.2 m high plywood walls to provide visual isolation from the remainder of the barn. The pen floor was covered with straw bedding. Feed racks were located on both sides along the length of the pen. Every morning, at 08:00 h, the ewes were fed 1.4 kg of alfalfa hay and 0.45 kg of a 14% crude protein ration of corn, oats, soybean meal and wheat bran per ewe. An automatic heated waterer provided continuous access to water.
Animals and management Animals used in the study were Suffolk, Hampshire, Dorset and crossbred ewes. The pen contained eight ewes in late gestation at any given time. Ewes were painted with an identification number, weighed and examined for any abnormalities, before entering the pen. Shortly after lambing, the ewe and her lambs were removed. A gestating ewe was promptly introduced into the pen to replace each lambing female. A total of 70 ewes lambed in the pen during the study. Two criteria were employed to select a total of 15 ewes as experimental subjects: each ewe had to be in the pen for a m i n i m u m of 12 h before lambing and the delivery had to be unassisted. Three of the selected ewes were primiparous. Subjects were divided into three categories according to the time of day at parturition: 00:00-07 : 59 h, 08:00-15 : 59 h and 16:00-23 : 59 h. There were six, four and five ewes, respectively, in these time of day categories.
Behavioral observations Two video cameras were mounted at the north and south ends of the pen. Recording equipment and video monitors were set up in an adjacent room. Ewes were videotaped continually, using time-lapse video recordings at 0.9 frames s-~. Focal animal observations were made of each of the 15 experimental ewes during the 12 h prepartum. Observations were also made at 2624 and 38-36 h prepartum for 13 of the 15 ewes, to determine levels of each behavior during the day before lambing. A behavioral catalogue was constructed by watching the videotapes of several ewes in order to define and name all observable behaviors (Table 1; Lehner, 1979). The 12 h period before lambing for each ewe was divided into six 2 h prepartum periods (i.e. 12-10, 10-8, 8-6, 6-4, 4-2 and 2-0 h prepartum) and these were viewed in a random order. Behaviors were recorded with an electronic event recorder. Data files generated were loaded onto a computer for subsequent analysis to determine the frequency and duration of recorded behaviors. The times spent in the behavioral states of standing, ground sniffing and feeding were calculated using the start and stop times of each state. The frequencies of all behavioral events during each 2 h prepartum period were tal-
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TABLE 1 Catalogue of behaviors observed in ewes during the 12 h prepartum Item
Definition
Behavioral states
Standing Lying Feeding Ground sniffing
Time Time Time Time
interval interval interval interval
between between between between
standing up and lying down lying down and standing up start and stop feeding start and stop ground sniffing
Active social behavior Sniffs lamb Licks lamb Nurses lamb Butts ewe Chases ewe Sniffs vulva Sniffs ewe Chins ewe
Focal Focal Focal Focal Focal Focal Focal Focal
ewe sniffs another female's lamb ewe licks another female's lamb ewe nurses another female's lamb ewe butts another female ewe chases another femalc cwc sniffs another female's vulva ewe sniffs another female ( non-vulvar area ) ewe rubs her chin across another female's back
Passive social behavior Butts focal Chases focal Pushes focal Sniffs local vulva Sniffs local Chins local
Any female butts focal ewe Any female chases focal ewe .Any female pushes focal ewe Any female sniffs local ewe's vulva Any female sniffs focal ewe (non-vulvar arca) Any female rubs her chin across focal's back
Locomotive behavior Stands up Lies down Stretches Turns Steps
Focal Focal Focal Focal Focal
Common preparturient bchaviors Start ground sniffing Stop ground sniffing Short ground sniff Paws Circles Flanks Licks self
Ewe lowers head to the ground and begins to sniff Ewe raises head from ground and stops sniffing Ground sniffing bout lasting less than 7.5 s Ewe scrapes the ground with her forefeet Ewe turns around an imaginary axis, in a circular fashion Ewe rubs her sides with her head Ewe licks herself
Feeding behavior Start feeding Stop feeding Drinks
Ewe starts eating Ewe ceases to eat Ewe drinks at waterer
Behavioral events
ewe gets up from lying position ewe lies down ewe stretches, may be lying or standing ewe changes direction while walking in pen ewe takes an average of two steps, from one to three steps
PREPARTURIENT BEHAVIOR OF CONFINED EWES
333
lied. Social interactions were classified as active or passive (Table 1 ) and totaled. Analyses of variance (ANOVA) were performed on data for 12 h prepartum, using the General Linear Models program of the Statistical Analysis Systems Institute ( 1985 ). Variables included in the model were ewe, time of day, prepartum period and a period by time of day interaction. Additional ANOVA were performed including periods 26-24 and 38-36 h prepartum. Means separation tests, using least significant differences, were performed if significant effects of interest were found in the previous analyses (Zar, 1984 ).
Behavior sequences Two-event behavior sequences were tallied for a total of 20 behaviors of interest. The behaviors analyzed were lamb sniffing, butting by focal and nonfocal ewes, vulva and body sniffing by focal and non-focal ewes, steps, standing up, lying down, turning, short ground sniffs (less than 7.5 s), straining, pawing, circling, flanking, and start and stop times for longer bouts of ground sniffing and feeding. For complete descriptions of these behaviors, with the exception of straining, see Table 1. Straining involved contraction of the ewe's flanks, often accompanied by stretching of the neck. The data for all ewes within a 2 h prepartum period were pooled. A X-" analysis was performed for each two-event sequence to determine whether the observed frequencies of any of the sequences deviated from their expected values (Lehner, 1979). Expected values for each sequence were estimated as the product of individual probabilities of each event within a given time period. Cells with both expected and observed values of less than five were not included in the results.
Spatial distribution For analysis of spatial distribution patterns, the observation pen was divided into front and back halves with an imaginary line. The spatial distribution of focal ewes and the rest of the group was determined at 5 min intervals for each observation period. An analysis was performed on the number of ewes in the same half of the pen as the focal ewe during each 2 h period of the 12 h before lambing. A second analysis was performed on the sequential changes in spatial distribution of each focal ewe and the majority group to determine movement trends during the last 12 h and the last 4 h prepartum. Four or more of the seven non-focal ewes in one half of the pen constituted the majority group. Associations of each ewe with or away from the majority group for the six 2 h periods ( 12 points h - i × 12 h = 144 points) were arrayed in a long (2 × 144 ) ordered contingency table, subject to simplifying compressions of runs of similar association (Ghent, 1984a). G a m m a coefficients ( G o o d m a n and Kruskal, 1954 ) were calculated from the ordered table for each of the 15 focal
334
A.C. ECHEVERRIETAL
ewes, separately for the last 12 h and the last 4 h prepartum. Since each gamma coefficient is itselfa paired difference between concordant and disconcordant movements of each ewe and her group, each of the two batches ( 12 h and 4 h ) of 15 coefficients could be tested as a group (Ghent, 1984a ) by Wilcoxon's paired-sample procedure (Wilcoxon and Wilcox, 1964; Zar, 1984 ). The qualities of gamma that suit it especially well to biological research have been reviewed (Ghent, 1984b).
RESULTS
Time budgets and fi'equencies
Standing Preparturient ewes spent more time standing as they neared parturition: an average of 93.7 min (78.1% of time) during the 2-0 h period preceding lambing versus 53.7 min (46.7%) during the 12-10 h period. The first significant indication of this tendency occurred during the 8-6 h prepartum period (Fig. 1). ANOVA showed that this behavior differed significantly among ewes ( P < 0.01 ) and was affected by the interaction between time of day and prepartum period ( P < 0.01 ). Time of day was not a significant determinant of this behavior. Standing
Ground
Sniffing .¢
40
o~
308
A 30
E
"3 ,-
.~
20
o o ,r-, o
o
10
o a.
12-10
10-08
Period
08-06
Before
06-04
04-02
Lambing (h)
02-00
12-10
10-08
08-06
06-04
04-02
02-00
Period Before Lambing (h)
Fig. 1. Time budgets of preparturient ewes for standing and ground sniffing during 2 h periods before parturition. Solid bars indicate periods within 12 h of parturition. Open bars are 24 h prior to the adjacent solid bar. Solid bars with a common letter superscript do not differ. An asterisk indicates a 2 h period which evidenced a significant increase in the behavior over the previous 2 h period.
PREPARTURIENT BEHAVIOR OF CONFINED EWES
335
Ground sniffing The amount of time ewes spent ground sniffing increased as parturition approached (Fig. 1). Ewes spent an average of 31.5 min (30.8%) engaging in this behavior during the period 2-0 h versus 11.4 min (10.5%) during the period 12-10 h. The behavior increased significantly 4-2 h prepartum and again during the period 2-0 h. Time of day did affect time spent ground sniffing (P< 0.05 ), but there were no significant effects of ewe or the time of day by period interaction. The number of bouts of ground sniffing increased along with time spent ground sniffing. The first significant increase was observed by the period 4-2 h. During the period 2-0 h, ewes sniffed the ground an average total of 64.8 times, compared with 18.1 times during the period 1210 h. There was no significant time of day effect. Ewe and time of day by period interaction effects approached significance (P< 0.10). Ground sniffing was uncommon the day before parturition. Eating Time spent at the feeder averaged 7.26 min per 2 h during the 12 h preparrum and did not differ among the 2 h periods. Eating behavior showed a significant time of day effect (P<0.01) and time of day by period interaction (P<0.01). Active social interactions The frequency at which preparturient ewes initiated social interactions with their penmates increased dramatically during the period 2-0 h before parturition (Table 2). Ewe (P<0.01) and time of day by period interaction (P<0.01) effects were significant for this behavior, but time of day was not. TABLE 2 F r e q u e n c i e s o f different b e h a v i o r s by ewes d u r i n g 2 h p e r i o d s before p a r t u r i t i o n Behavior
Preparlum period (h) 12-10
Active social interactions P a s s i v e social interactions N u m b e r of t i m e s stood up Steps tak en Pawing Circling Flanking
10-8
8-6
6-4
4-2
2-0
26-24
38-36
1.5 a
1.8 a
1.9 a
3.1 a
8.1 ~
20.1 b
0.5
1.5
1.7 ~
1.1"
1.5 a
2.1 ~
6.5 a'b
13.1 b
1.5
1.8
3.2 a
3.3 ~
3.3 a
3.8 a
5.7 ~'°
10.70
2.6
2.2
110.7 a 4.3 ab 1.3" 3,5"
185.1 b 8.40"c 3.7 ~ 2.5 ~
174.80 14.4 ''d 18.9 b 11.0 b
361.5 c 19.6 o 28.9 c 20.80
60.8 1.6 0.5 2.5
104.2 0.2 0.3 2.9
68.9 a 3.2 "-b 2.4 a 2.1 ~
104.3 ~ 2.4 ~ 1.7 ~ 2.3 ~
M e a n s in rows which do not share a c o m m o n s u p e r s c r i p t are s i g n i f i c a n t l y different ( P < 0.05 )
336
A.C. ECHEVERRIET AL.
The frequency of active social interactions on the day before parturition was very low. The breakdown of the different types of active social interactions was as follows: 59.9% sniffing another ewe's vulva, 13.6% sniffing another ewe's body, 12.9% sniffing another ewe's lamb, 5.3% chinning another ewe, 3.0% butting another ewe, 3.0% pushing another ewe, 1.3% chasing another ewe and 1.0% licking another ewe's lamb.
Passive social interactions The frequency of social interactions directed towards the focal ewe also increased during the final 2 h before parturition (Table 2). Ewes differed ( P < 0.01 ) for this behavior, but neither time of day nor time of day by period interaction affected the level of activity. As with active interactions, passive interactions were few on the previous day. The breakdown of the different types of passive social interactions was as follows: 82.8% vulva sniffing, 12.5% body sniffing, 1.6% chinning, 1.6% butting and 1.6% pushing.
Standing up As ewes approached parturition, there was a dramatic increase in the number of times they stood up and lay down (Table 2). The first significant increase was observed during the period 4-2 h. There were significant ewe ( P < 0 . 0 1 ) and time of day by period interaction ( P < 0 . 0 1 ) effects, but no time of day effect. The frequencies during 38-36 and 26-24 h were similar to that during 12-10 h.
Steps The number of steps taken by preparturient ewes increased in manner similar to standing up (Table 2), although the first statistically significant increase was observed earlier, during the period 6-4 h. A second increase occurred during the final 2 h prepartum. There was a significant ewe effect ( P < 0 . 0 1 ) for this variable, but neither time of day nor time of day by period interaction effects. Steps taken the previous day were similar in frequency to those in the periods more than 6 h before birth occurred.
Pawing The number of pawing bouts ewes engaged in increased as the time of parturition approached (Table 2). The first significant increase in pawing occurred by the period 4-2 h during the 12 h interval before lambing. There was no significant time of day effect for this variable; ewe and time of day by period interaction effects approached significance ( P < 0.10). Pawing was infrequent on the day before parturition.
PREPARTURIENT BEHAVIOROF CONFINED EWES
337
Circling The number of times preparturient ewes circled also increased significantly as they approached lambing (Table 2). There was a significant increase in circling by the period 4-2 h. ANOVA showed a significant ewe effect ( P < 0.05 ), but no time of day or time of day by period interaction effects for the six 2 h periods before lambing. Circling was observed less than once per hour on the day prior to parturition.
Flanking Flanking increased significantly during the final two, 2 h periods before lambing (Table 2). ANOVA showed a significant ewe effect ( P < 0.01 ), but neither time of day nor time of day by period interaction effects were observed. Flanking on the day before lambing occurred at a rate similar to that from 12 to 4 h prepartum.
Sequential analysis Two-event sequences were analyzed for each time period to test whether their occurrence deviated from expected values. As ewes approached parturition, the numbers of two-event sequences that deviated from their expected frequencies increased substantially (Table 3 ). The two-event sequences that increased significantly over expected values a few hours before lambing are depicted in Fig. 2. These sequences can be roughly divided into those involving sniffing of other animals (social behaviors), ground-directed investigation and self-directed behavior. Two behaviors, circling and ground sniffing, were noteworthy as they occurred in sequences involving all three types of behaviors. Although three-event sequences were not analyzed, it is possible that circling and ground sniffing served as a means of transition between the behavioral groupings. TABLE 3 Number of two-event sequences which deviated from the expected frequencies during each 2 h period before parturition ( P < 0.05 ) Time period (h)
Above expected
Below expected
Total
2-0 4-2 6-4 8-6 10-8 12-10
35 33 12 9 10 9
50 25 8 6 3 4
85 58 20 15 13 13
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A.C.ECHEVERRIETAL.
Fig. 2. Diagram of two-event sequences which occurred at frequencies greater than expected during the 4 h before parturition. GS, ground sniffing: SB, sniffs body; SFB, sniffs focal ewe's body; SFV, sniffs focal ewe's vulva; StGS, stops ground sniffing bout: SV, sniffs vulva.
Spatial analysis The percentage o f non-focal ewes which were associated with the focal ewe in one half o f the pen deviated significantly from 50% only during the period 2 - 0 h ( P < 0 . 0 1 ) . During this period, the focal ewe was with the majority o f ewes in the pen only 40.3% of the time. Focal ewes and the majority groups were then analyzed for m o v e m e n t trends in relation to each other. In only four ewes out o f 15 over the last 12 h, and in only one ewe out o f 15 over the last 4 h, was there an overall tendency for increased proximity o f the focal ewe and the other seven ewes. The Wilcoxon paired tests indicated that the p r e d o m i n a n t trend to increased isolation o f the focal ewe with approaching parturition was statistically significant over the last 12 h (two-sided, P = 0 . 0 2 4 9 ) and more strongly so over the last 4 h (two-sided, P = 0 . 0 0 3 4 ) . A complicating factor in these analyses was that some focal ewes spent prolonged periods resting with or otherwise accompanying minority groups (three or fewer ewes) during the initial 2 - 4 h o f these 12 h studies, thereby weaken-
PREPARTURIENT BEHAVIOR OF CONFINED EWES
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ing (Ewes 36 and 70 ) or reversing (Ewes 49, 52 and 56 ) their apparent trends over all 12 h compared to their strong trends to increased isolation during the last 4 h. Only Ewe 63 (an extremely restless animal that moved between majority and minority associations more often than any other) showed a trend to increased proximity with the other ewes during the last 4 h. DISCUSSION
Time budgets and frequencies An ideal behavioral predictor of parturition should show a dramatic change in frequency over time before the event and be relatively unaffected by other factors such as time of day and individual animal. Early evidence of impending parturition would be desirable and previous reports have suggested that behavioral changes are evident as early as 24 h before birth (Atroshi and Osterberg, 1979 ). None of the behaviors observed in this study increased earlier than 8 h prepartum, although observations more than 12 h before birth were limited. Of the behaviors observed, only the frequency of pawing and ground sniffing were unaffected by ewe and time of day or interaction effects. Pawing increased eight-fold during the 6 h prepartum, making it an excellent indicator of parturition. Although Arnold and Morgan ( 1975 ) reported breed differences in pawing behavior, we did not observe any differences among the limited number of ewes observed. Owens et al. (1980) interpreted pawing as a sign of restlessness, while McGlone and Stobart ( 1986 ) suggested that postpartum pawing is a rudiment of aggression. We interpret pawing as a type of nest-building behavior, similar to that observed in sows and other species, which may be related to comfort seeking. Ground sniffing, both the frequency and time involved, tripled during the last 4 h before parturition. This modest increase could limit the usefulness of the behavior as an indicator of impending parturition, but the lack of ewe effects are favorable. Smith (1965) and Sharafeldin et al. (1971) also reported increases in ground sniffing before parturition. The behavior may be related to an attraction to birth fluids which develops 3-13 h before parturition (Levy et al., 1983), as sniffing normally increases after fluids are discharged (Smith, 1965). Several behaviors increased during the final 6 h prepartum, but evidenced significant ewe effects. A five-fold increase in walking, indicated in steps taken, was evident as early as 6 h prepartum. Other reports have described aimless walking, trotting and running (Owens et al., 1980; Shackelton and Haywood, 1985 ), but Fraser ( 1968 ) reported a lack of movement in preparturient ewes. Facility design may affect prepartum movement as Gonyou and Stookey (1985) reported a reduction in steps taken when free-access cubicles were available to groups of confined ewes.
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Other behaviors which followed a pattern similar to walking were flanking and circling. Since these behaviors increased dramatically during the 4 h prepartum and are relatively rare at other times, they should be good indicators of impending birth. Flanking may be related to discomfort caused by contractions while circling may, as with pawing, be related to birth site preparation. Both add to the restlessness reported by other researchers (Wallace, 1949: Shackelton and Haywood, 1985 ). Passive social interactions differed among ewes, while active interactions differed among ewes and with the time of day by period interaction. Time of day effects, or interactions with time of day, limit the usefulness of a behavior as a predictor of parturition, unless there is a dramatic prepartum increase which exceeds that of normal diurnal variation. Both types of social interactions occurred at very high levels during the 2 h before parturition. The preparturient ewes initiated more encounters, including a higher proportion of aggressive interactions, than did non-parturient ewes. Other reports have not noted the increase in social interactions that we observed. It is likely that social interactions are more c o m m o n in confinement conditions in which parturient ewes cannot isolate themselves from each other. Previous reports have indicated that the time spent standing and the frequency of standing up (Wallace, 1949; Owens et al., 1980) increase prior to parturition. Although we observed similar patterns, the increases were relatively small (65% and 300% for time and frequency, respectively). The fact that ewe and time of day by period effects were significant limits the use of these behaviors as predictors of parturition. Our observed lack of effect of impending parturition on feeding behavior, perhaps masked by the time of day effect resulting from our feeding schedule, does not support the use of this behavior, as suggested by Sharafeldin et al. ( 1971 ), as an indicator of parturition.
Sequential analysis The total numbers of two-event sequences that deviated from their expected values increased dramatically as lambing neared. It is possible that as motivational levels increase, sequential events are more likely to be of similar motivational origin and random sequences less frequent. Of interest is the fact that although some sequences occurred more often than expected, a large number occurred less frequently than expected. Those behaviors occurring in sequence may be expected to have a c o m m o n causal factor, or the first stimulates the second. Sequences occurring rarely are likely to consist of behaviors with different causal factors. Sniffing another ewe, or being sniffed by one, often resulted in reciprocation by the recipient. Sniffing of the body led to sniffing of the vulva, but not vice versa, suggesting that sniffing was somewhat goal directed. Social sniff-
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ing was only prevalent during the final 2 h before parturition, which coincides with the development of an attraction to birth fluids (Levy et al., 1983 ). The association of these behaviors with each other, the m o v e m e n t from the body to the vulva and the timing of these behaviors all support an interest in birth fluids as a c o m m o n causal factor. The transition to ground sniffing may also be related to interest in birth fluids, but the frequent change to circling is less understandable. Several of the non-social behaviors appear to be interrelated and associated with investigation of the physical environment. Ground sniffing frequently led to, or continued during, walking and pawing of the ground. Circling also led to pawing or the end of a ground-sniffing bout. The transition to lying usually involved the end of a bout of ground sniffing. It would appear that these behaviors are related to investigating the environment in a search for a suitable birth site. Gonyou and Stookey (1985) observed that ewes which choose to give birth in cubicles take fewer steps during the final hour before parturition, perhaps because they have selected a satisfactory birth site. A final group of behaviors appear to be related to the comfort of the ewe. Straining and flanking frequently precede each other, and result in the ewe standing or, if already in the standing posture, ground sniffing or circling. The transition to either the social sniffing behaviors or the environmental investigatory behaviors involves either circling or ground sniffing. In general, sequences involving behaviors from more than one of the groupings delineated above were rare. Some of these sequences are conspicuous by their infrequent occurrence. Social sniffing did not lead to walking, or vice versa. The lack of association between m o v e m e n t and social sniffing indicates that ewes did not try to avoid sniffing by walking away, or move toward ewes with the intent of engaging in sniffing. Although both pawing the ground and flanking are part of the increased restlessness observed in prepartum ewes, they appear to be in separate classes of behaviors. The role of ground sniffing and circling is obviously very important as they serve as transition behaviors among all behavior groups. Behaviors may serve such a role if they share c o m m o n motivational factors with each behavior group. It can easily be envisioned how social sniffing leads to sniffing other surfaces, such as the ground, and how ground sniffing leads to other investigative behaviors such as pawing. The transition among behavior groups through circling is less easily understood. Although circling may appear to be related to flanking, its relationship to social sniffing is less obvious. Circling may be a type of conflict behavior which occurs when motivation levels for other behaviors are high, but neither behavior predominates.
Spatial distribution In a few cases, the group moved away from the focal ewe and in a few others the focal ewe avoided the group, but the most frequent occurrence was one of
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mutual avoidance. The group may be disrupted by the high levels of activity and restlessness displayed by the lambing ewe. Another possibility is that nonparturient ewes are repelled by the odor o f a m n i o t i c fluids. The results of the sequential analysis suggest that the focal ewe does not approach the group to initiate social interactions or leave the group to avoid interaction. M o v e m e n t was usually associated with ground sniffing and probably reflected searching for a suitable birth site. These results, although obtained in a confinement situation, support the conclusions of previous workers who stated that the separation of ewes in pastures at the time of parturition could be due to either the m o v e m e n t of the ewe or of the group (Arnold and Morgan, 1975; Stevens et al., 1981).
CONCLUSIONS
Time budgets and frequencies Several behaviors related to parturition, locomotion, social interactions and general activity increase during the 12 h before parturition in confined ewes. The majority of the changes in behavior are first evident 4 h before birth. C o m m o n preparturient behaviors such as pawing, ground sniffing, circling and flanking are least affected by time of day or interaction effects. Pawing is probably the best indicator of impending parturition as it increases an average of eight-fold, beginning 6 h before birth, and does not differ among ewes. Social interactions involving the preparturient ewe increase dramatically during the final 2 h before the lamb is born. The high level of social interactions observed may be related to the high density of animals in a confinement situation. Locomotor activities such as walking and standing up increased, but varied with the ewe involved. These behaviors are not likely to be as reliable predictors of impending parturition. Analysis of the frequencies of two-event behavioral sequences suggests that preparturient behavior involves three distinct groupings. Social sniffing involving the preparturient ewe and another ewe or lamb is probably related to increased interest in birth fluids during the final hours before lambing. Ground sniffing, pawing of the ground and walking during a bout of ground sniffing frequently lead to the selection of a lying site. Flanking and straining appear to be related to internal discomfort, and frequently lead to standing. Both ground sniffing and circling serve as transition behaviors among these three groups. Preparturient ewes become separated from the majority of the flock due to the m o v e m e n t of the ewe, the flock, or both, during the final hours before lambing occurs.
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ACKNOWLEDGMENTS
This study was partially funded by the Illinois Sheep and Wool Marketing Board. We extend appreciation to A. Richard Cobb and his staff at the sheep unit.
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