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Behaviour and seasonal variation in heart rate in domestic sheep, Ovis aries
AnOn. Behav., 1988, 36, 35-43
Behaviour and seasonal variation in heart rate in domestic sheep, Ovis aries N. M. B A L D O C K * t , R. M. SIBLY*$ & P. D. P E N N I N G §
*Department of Pure and Applied Zoology, University of Reading, Whiteknights, PO Box 228, Reading, Berkshire RG6 2A J, U.K. §Animal and Grassland Research Institute, Hurley, Maidenhead, Berkshire SL6 5LR, U.K. Abstract. Three major causes of heart rate variation in undisturbed adult ewes were identified: behaviour, season and individual identity. Heart rate was 8 beats/min lower when the ewe was lying than when she was standing. It was increased by ruminating by 2 beats/min above the value for idling, and by a further 6 beats/min when the ewe changed to grazing. It seems that the increases in heart rate when the ewe was standing were simply added to those associated with ruminating or grazing. Heart rate declined slightly during bouts of unchanged behaviour. It varied seasonally from a minimum in December to a maximum some 50% (46 beats/min) higher in June. This variation was closely linked with daylength, basal metabolic rate, food availability, food consumption and the reproductive cycle, although it also occurred in nonbreeding animals. Changes in heart rate associated with daylength may be the secondary result of the effects ofdaylength on metabolic rate. After taking all these effects into account, there remained variation between five ewes of 16 beats/min.
The association between behaviour and heart rate has been studied in humans (e.g. Strand 1978; Smith & Kampine 1980), and some work has been done on other animals (e.g. bighorn sheep, Ovis canadensis, MacArthur et al. 1979; white-tailed deer, Odocoileus virginianus, Moen 1978; Jacobsen 1979). In view of this, it is surprising that no comprehensive study exists, of the type reported here, relating heart rate to behaviour, environmental variables and individual identity, since a full understanding of the implications of behaviour for heart rate would have many uses. For example, it would help assess the metabolic implications of behaviour, because a major function of the blood is to supply oxygen to the muscles. Oxygen supply depends not only on heart rate, but also on the stroke volume of the heart and arterial-venous oxygen differences (Shephard 1982). Nevertheless, heart rate is a reasonably good index of the metabolism of mammals and birds, at rest or exercising moderately, provided they are free from stress (Johnson & Gessaman 1973; but see also Brockway 1978). The study reported here satisfies these conditions. Correlations between individual heart rate and energy expenditure have been good (greater than 0"85) in most recent studies (Holmes et al. 1976; Pauls 1980; Kamau & Maloiy 1982; Fukuhara et al. 1983; Tobioka et al. 1983; Yama-
moto et al. 1985; Yamamoto 1986). Seasonal variation in heart rate is expected because basal metabolic rate (Blaxter & Boyne 1982) and the amount of food consumed per day (Gordon 1964; Milne et al. 1978; Kay 1979; Blaxter et al. 1982) change from a minimum in midwinter to a maximum in midsummer, in parallel with changes in daylength. Indeed daylength is the principal cause of seasonal changes in food intake (Kay 1979). Higher metabolic activity requires an increased oxygen supply to the body tissues and this in turn is likely to require an increased blood supply, and, therefore, an increased heart rate. In this paper, we investigate the effects on heart rate of behaviour, individual identity and environmental variables. In order to obtain information on undisturbed sheep, ewes were kept in relatively normal farm conditions, and a series of monthly recordings was made over a period of a year. Multiple regression was used to identify the magnitude and confidence limits of each effect.
METHODS
Animals
All work was carried out at the Animal and Grassland Research Institute, Hurley, near Maidenhead, Berkshire, U.K. during 1983 and 1984. The study animals were domestic sheep, Ovis
t Present address: 47, Corfe Road, Melksham, Wiltshire, U.K. $ To whom all correspondence should be addressed. 35
36
Animal Behaviour, 36, 1
aries, from a flock of 149 Scottish half bred ewes (Border Leicester ram x Cheviot ewe) 2 and 3 years old. These ewes had all been handled previously. On 24 January 1983, six randomly chosen ewes were separated into a subflock (flock 1) for further study. Recordings were made from five of these animals on 17 study days between 16 March 1983 and 9 February 1984. No records were made from the sixth animal, which was included as a 'reserve'. A further 16 randomly chosen ewes were separated into a subflock (flock 2) on 19 February 1984. Recordings were made from four of these animals on three study days between 9 and 30 March 1984. All the animals were kept on pasture, though intake was supplemented by hay during the winter.
Recording Equipment The recording method was based on a taperecorder system available commercially for the recording and analysis of ECG in humans (Oxford Medical Systems, Nuffield Way, Abingdon, U.K.). As developed for sheep, the system comprised two electrodes (attached to or immediately below the skin) connected to a tape-recorder mounted in a special harness on the animal's back, and a replay unit with signal decoder and microprocessor to transfer data to floppy disk for eventual transfer to a mainframe computer. Full details are given in Baldock et al. (in press).
Behaviour Recordings All observations of behaviour were made from a parked vehicle overlooking the field containing the ewes. Other vehicles were regularly parked nearby. We obtained access discreetly and quietly, making every effort not to disturb the sheep. As far as we could tell, the behaviour of the sheep was not affected by the observer's presence.
Behavioural categories Categories were chosen to be mutually exclusive and to cover all commonly occurring behaviours. Behaviours were classified as either standing or lying followed by a further classification as defined below. (1) Grazing: the initial intake of grass was taken as the start of a grazing bout. The termination of a bout occurred when the animal either lifted her head above the horizontal or lay down. Occasional steps were taken (but see category 7).
(2) Eating hay: the manipulating, ingesting or masticating of hay from the feeder. (3) Alert: neck raised and ears pricked forward. (4) Idling: any posture not involvingjaw or limb movements, and not in an alert or head down position. (5) Ruminating: rumination bouts began when a bolus was seen to be regurgitated. The end of a bout occurred when jaw movements had ceased for longer than 20 s, Or the animal had changed posture. (6) Head down: an animal with her head touching the ground and not moving her jaw. The individual'seyes were often closed, but this was not taken as a criterion for this category. (7) Walking: slow motion during which the animal was not grazing, in which at least one forefoot and one hindfoot were on the ground at any one time. In addition, notes were made of other occasional behaviours (e.g. drinking, vocalizing). Behaviour was recorded at intervals of 1 min. Since behaviour could be observed carefully prior to recording, it is thought that errors were negligible. Identification of animals was aided by painting numbers on the fleeces and backpacks,
Experimental Procedure On each study day the study animals were moved into a handling pen and harnesses, tape-recorder and electrodes (where necessary) were attached. The animals were then released back into the pasture in which they were ordinarily kept. Since it was known that the effects of this handling procedure disappeared within 5 min of release from the pen (Baldock et al., in press), heart rate and behaviour were sampled thereafter at 1-min intervals for 4-7 h between 0900 and 1800 hours. During the observation period normal farm activities continued, resulting in minor disturbances, which were noted.
Analysis In order to gain an overall, if somewhat simplistic model of the causes of heart-rate variability in sheep, multiple regression analyses were carried out on the data from each flock, fitting the equation heart rate =
a + Eeixi q-- ~biyi + Edizi Jr cl + ~ i
i
i
(1)
37
Baldock et al.. Heart rate and behaviour in sheep
Here a is a constant. The variable xi is a dummy variable (McCullagh & Nelder 1983, page 40) taking the value I if the heart rate is that of ewe number i, zero otherwise. The number of xl variables corresponds to the number of ewes minus one (see below). The coefficient ei (to be estimated in the regression analysis) therefore represents the effect of being ewe number i. For example if ewe number 2 bad heart rate 20 beats/min higher than ewe number 3 (other things being equal, see below) then e2 - e3 + 20 beats/min. The number of x~ variables is one less than the number of ewes because there would otherwise be too many degrees of freedom in the regression. This is because by convention in the statistical package used (Glim 3.77, McCullagh & Nclder 1983) the constant a (in equation 1) represents the average heart rate of ewe number 1 when performing behaviour number 1 (i.e. 'standing grazing') on the first observation day (16 March 1983). Therefore the regression does not provide values el, b] or d~ since this eventuality has already been allowed for. The variable y~ is a dummy variable taking the value l if the measured heart rate occurred while behaviour number i was being performed, zero otherwise. The number ofy~ variables corresponds to the number of behaviours that were recorded. The coefficient b~ therefore represents the effect on heart rate of performing behaviour number i. The variable zl is a dummy variable taking the value I if the heart rate occurred on study day number i. The number of z~ variables corresponds to the number of study days minus one. The coefficient di represents the effect on heart rate of day number i. For example if in the third recording (made on 4 May) heart rate was 29.6 beats/min lower than in the fourth recording made on 5 June (other things being equal) then d3= d 4 - 29.6 beats/min. The variable l measures bout duration (in rain) and the coefficient c represents the effect on heart rate of bout duration, e is the residual error, i.e. the discrepancy between predicted and observed heart rate. A number of checks were made on the distribution of e from which it appeared safe to assume e had a normal distribution. The order in which factors were entered into the analysis was changed systematically in order to gain an understanding of the relative importance of each factor. The final order was used in the analyses of both flocks and was decided on by consideration of the relative biological importance of each factor.
• standing grazing
o
• standing idling
~ lying idling
• standing alert
o lying head down
120
Lying ruminating
[2
•
t
t~
~100
gO
g
-"
•*,
0
I•
~o
o
o
[]
'k
o ~
0
80
COO d:~ ~
•
OD
O 0
o
60
0
1
2 Time (hi
3
t+
Figure 1. The heart rate and behaviour of ewe 5 on 13
April 1983.
RESULTS An example of a recording is shown in Fig. 1. The animal spent about half her time standing and half lying, and the heart rate was consistently higher by some 20 beats/rain when she was standing. Table I shows that the predictor variables shown in equation (1) accounted for 65% of the variation in heart rate in flock I, and 50% of the variation in flock 2. These figures indicate success in predicting instantaneous heart rate (i.e. the reciprocal of the interval between successive heart beats), which is probably subject to a certain amount of random noise, and is affected by environmental variables (e.g. sight of dogs) not entered in the regression, apart from the known measurement errors of our equipment (about 3 beats/min, Baldock 1985). The residual standard deviations for the two flocks were
Table I. Results of multiple regression analysis on data
from flocks 1 and 2 showing the percentage of the total heart-rate variation explained by each class of variable % Total heart-rate variation Variable class Ewe Behaviour Bout length Day Total
Flock 1
Flock 2
21 6 1 38 66
19 28 0 3 50
Animal Behaviour, 36, 1
38
10 b e a t s / m i n a n d 7 b e a t s / m i n , so the v a r i a t i o n a c c o u n t e d for is p r o b a b l y n e a r the limit o f w h a t is achievable w i t h o u r e q u i p m e n t a n d m e t h o d o f analysis. M o r e o f the v a r i a t i o n was explained in flock 1 t h a n in flock 2 b e c a u s e the d a y effects p r o d u c e d m u c h less v a r i a t i o n in the latter, w h i c h was o b s e r v e d over a s h o r t e r p e r i o d . T h e e x p l a n a tion o f this result is d i s c u s s e d below. E s t i m a t e s o f the effects o f the p r e d i c t o r variables are s h o w n in T a b l e II. T h e r e were large differences T a b l e !I. Effect (beats/min) on heart rate of each of the predictor variables shown in equation (l)
Parameter
Flock 1
Flock 2
Estimate (SE)
Estimate (SE)
in h e a r t rate b e t w e e n the ewes (the r a n g e s b e i n g 16 a n d 15 b e a t s / m i n in flocks 1 a n d 2 respectively). C o n s i s t e n t l y different levels o f h e a r t rate b e t w e e n individuals are also seen in o t h e r studies o f s h e e p ( W e b s t e r 1967; M a c A r t h u r et al. 1979; S y m e & E l p h i c k 1982) a n d in white-tailed d e e r ( M o e n 1978). S o m e o f the differences in flock 1 c o u l d be e x p l a i n e d o n t h e basis o f the e w e ' s w e i g h t a n d age (71%, dJ] = 2, dJ~= 2, F = 2 - 4 2 , Ns), t h e o l d e r ewes h a v i n g lower h e a r t rates. S y m e ( p e r s o n a l c o m m u n i c a t i o n ) f o u n d a similar r e l a t i o n s h i p b e t w e e n age a n d h e a r t rate in M e r i n o sheep. H o w e v e r , this c a n n o t be t h e c o m p l e t e e x p l a n a t i o n b e c a u s e similar v a r i a t i o n o c c u r r e d in flock 2, in w h i c h all ewes were the s a m e age.
Effects
General mean Ewe 2 Ewe 3 Ewe 4 Ewe 5 Ewe 8 Ewe 9 Ewe I0 Standing idling Standing alert Standing ruminating Lying idling Lying head down Lying ruminating Lying grazing Walking Standing eating hay Bout length (min) 13 April 1983 20 April 1983 4 May 1983 5 June 1983 12 June 1983 2 July 1983 16 July 1983 9 August 1983 24 August 1983 13 October 1983 18 October 1983 15 November 1983 24 November 1983 9 December 1983 17 January 1984 9 February 1984 20 March 1984 30 March 1984
100.6 - 11-9 - 8.2 - 3.8 4.1
-
10.2 8.0 8.3 17.3 16.3 14.5 9.7 2.0 3.2 0.06 7.4 24.6 - 7.6 22.0 27.0 5.6 6.4 5-3 - 2.0 - 7.4 -- 1.9 - 5.7 - 11-5 - 19.4 - 2-6 1.3
(0.7) (0.5) (0.5) (0.4) (0.4)
81.4 -----
(0.4) -----
--
-
10.7
(0.5)
--
-
5.2
(0.5)
--
-15.1
(0-5)
- 4.9 - 5-1 - 6.9 - 15.1 -14.3 - 9.5
(1.2) (0.9) (2.0) (0.6) (0.8) (0-4)
(0.5) (0.8) (0.7) (0.5) (0.5) (0-4) (1.1)
--
.2) 0.7 (O.7) 0.2 (0.007) -- 0.02 (0.8) --
(I
--
(1.0) (O.7) (0.01) --
(1.4)
--
--
(1.3)
----
----
----------
----------
(0.9) (0.7) (0.9) (0-7) (0.7) (0.7) (0-9) (0.9) (0.8) (0.6) (0.7) (0.7) (0-7) ---
-
--
-
-
of
Behaviour
C h a n g e s in h e a r t rate a s s o c i a t e d w i t h c h a n g e s in b e h a v i o u r h a d a r a n g e o f 17 b e a t s / m i n in flock 1 a n d 16 b e a t s / m i n in flock 2 (Table II). T h e c h a n g e s in h e a r t rate are illustrated in Fig. 2. T h e r e is a n excellent c o r r e l a t i o n b e t w e e n the analyses c a r r i e d o u t i n d e p e n d e n t l y for t h e t w o flocks. I n each case the lowest h e a r t rate was a s s o c i a t e d with lying idling. A n increase o f a b o u t 8 b e a t s / m i n o c c u r r e d when the animal stood, and about another 7 beats/ m i n if she t h e n w a l k e d . S u p e r i m p o s e d o n these are c h a n g e s a s s o c i a t e d w i t h j a w m o v e m e n t s , so t h a t ruminating added about 2 beats/min and grazing a b o u t 8 b e a t s / m i n . A l t h o u g h this is s o m e t h i n g o f a simplification ( b e c a u s e o u r ' s t a n d i n g g r a z i n g ' categ o r y a l l o w e d o c c a s i o n a l leg m o v e m e n t s ) it d o e s suggest t h e h y p o t h e s i s t h a t the c h a n g e s in h e a r t rate a s s o c i a t e d w i t h i n d e p e n d e n t m o v e m e n t s m a y be additive, in t h e sense t h a t if m o v e m e n t A increases h e a r t rate b y hA b e a t s / m i n , a n d m o v e m e n t B b y hB b e a t s / m i n , t h e n if the t w o m o v e m e n t s are m a d e s i m u l t a n e o u s l y , h e a r t rate will increase by h A + h s b e a t s / m i n . I n o r d e r to test this h y p o t h e s i s , d a t a f r o m T a b l e II p e r t a i n i n g to s t a n d i n g o r lying, idling, r u m i n a t i n g , o r grazing, were used to see w h e t h e r d e v i a t i o n s f r o m the s t a n d i n g - g r a z i n g values c o u l d be a d e q u a t e l y d e s c r i b e d b y t h e equation
-
2.8
(0.4)
2.5
(0.4)
- - = missing data. Values show the differences from the heart rate of ewe 1 when standing grazing on 16 March 1983 (flock 1), or ewe 7 when standing grazing on 9 March 1984 (flock 2). See Methods for further details.
h e a r t rate = lxl+ mxm + rxr + e
(2)
w h e r e xt, xm a n d x, are d u m m y variables such t h a t xl = 1, xm = 1 o r xr = 1 if the a n i m a l is lying, idling, o r r u m i n a t i n g , respectively; o t h e r w i s e the d u m m y variables are zero. T h u s if all the d u m m y variables are zero the a n i m a l was n o t lying, n o t idling a n d
Baldock et al.." Heart rate and behaviour in sheep Flock 1 •
Flock 2
•
o
m~ --5
-10 "t -15
Lying
Standing
Figure 2. Heart-rate changes associated with various behaviours.
not ruminating, i.e. it was standing grazing. Equation (2) accounts for 96% of the variation, using three predictor variables, which is virtually all of the 97% accounted for by a 5-predictor model of the type shown in equation (1). This supports the hypothesis that changes in heart rate associated with individual movements are additive. The estimates obtained suggest that heart rate is lowest when the animal is lying idling. If the animal stands then heart rate is increased by 7.6 beats/min. If it changes from idling to any other behaviour then heart rate increases further, by 8-1 beats/min if it changes to grazing, or 2.1 beats/min if it changes to ruminating. Standard errors were 1.6 beats/min in each case ( N = 6). These results provide a quantitative summary of some of the data in Fig. 2.
Seasonal Variation As explained in the introduction, seasonal variation in heart rate, in parallel with daylength, was predicted, from a minimum in midwinter to a maximum in midsummer. The expected seasonal changes in heart rate are seen when the effects of the day variables are plotted against date for flock 1 (Fig. 3). Thus heart rate increased by 46 beats/min from a minimum in December to a maximum in June, and thereafter declined steadily until the following December. As a check on these results
39
the data for each ewe were analysed separately (using equation 1 without the ewe variables); the individual ewes showed parallel changes in heart rate (Fig. 3b). Changes in heart rate are taken to be zero on 16 March 1983 (see Methods). Since many environmental variables vary in parallel between the solstices in June and December, there is little chance of accurately distinguishing their effects. Nevertheless, as a first step, daylength (which varies sinusoidally between extreme values at the solstices) and temperature (which lags somewhat behind daylength) were investigated. Daylength was the most important predictor of the changes in heart rate shown in Fig. 3a, accounting for 76% of the variation (F=44-8, dJ]=l, dj~=15, P<0.01). When entered subsequently, temperature accounted for a further 10% (F=9.9, dfl = 1, dJ~= 14, P<0.01). (When entered first, temperature accounted for 24% of the seasonal variation in heart rate with an estimated effect of 0.6 beats/min per °C.) There was no cumulative effect of the experiment on heart rate as judged by the negligible effect of time since the first recording, after allowance had been made for daylength and temperature (F=0-1, d~ = 1, dJ~= 13, ys). Since breeding has an annual cycle, some of the variation seen in Fig. 3 might be due to the metabolic demands of reproduction. All ewes in flock 1 were artificially inseminated on 10 November 1983 and some became pregnant and gave birth to a single lamb as indicated in Fig. 3b. Ewes 1 and 4 were lactating in June and July 1983. There was no difference between the heart rates of the pregnant and non-pregnant ewes in November and December, when the metabolic demands of reproduction are low (Agricultural Research Council 1980), but there is a suggestion that between February and July (when metabolic demands of reproduction are highest, Agricultural Research Council 1980) heart rate was higher in the breeding than in the non-breeding animals (Fig. 3b). With such small sample sizes we did not attempt to estimate the magnitude of these effects. However, it is clear from Fig. 3 that the changes in heart rate in non-breeding animals parallel those in breeding animals, so direct metabolic demands of breeding are unlikely to be the whole explanation for the seasonal variation in heart rate. An increase of (~7 beats/min was found between the heart rates of two ewes recorded 5 days postshearing compared with their heart rates 2 days pre-shearing (standard errors were less than 2 in
40
Animal Behaviour, 36, 1
~-20
o .c/\ ~
/
o Hearf rate change
~ Oayiengfh ETemparafure
a
"~40 N.
6
0
o/° , / ~ ' - - ~ , ~ \ \ / p, ',,
/
12 ~-20 oJ
i.~
[]
\'X9
N'A'N'J
'J 'A'S'O
' N ' D 'J ' F '
1983
Ip
198#
Im
"~ 40
Im 2 Z~m
--20
Im 1 Z,p
5 5
5p
I
5
4 5p~ 1 521
5
~£sp
'M'A'M'J
'J ' A ' S ' O 1983
' N ' D 'J ' F ' 1984
Figure 3. Seasonal changes in heart rate. (a) Heart-rate data from Table II excluding days when only one ewe was recorded. Daylength and ambient temperature are also shown. (b) Results of independent analyses carried out for each ewe separately. Numbers refer to ewe identity. p: pregnant; m: lactating.
both cases). Shearing occurred on 7 June 1983. Seasonal variation at this time of year was decreasing heart rate by about I beat/min per week so these results could not be due to the seasonal variation described above.
DISCUSSION This study has identified three major causes of variation in heart rate in adult ewes: behaviour (Fig. 2), season (Fig. 3) and individual identity. A linear model of the causes of change in heart rate accounted for up to 65% of the variation (Table I), and yielded precise estimates of the effects of each predictor with standard errors generally less than 1 beat/rain (Table II).
Effects of Behaviour The changes in heart rate associated with behaviour tally with expectations. Thus heart rate was 8 beats/min lower when the ewe was lying than when she was standing. It was increased by ruminating by 2 beats/min above the value for idling, and was 8 beats/min higher for grazing than for idling ewes. It seems the heart-rate costs of standing are simply added to those associated with ruminating or grazing, which is why successful prediction is possible using equation (2). This is not surprising since the blood supplies energy to the muscles, and the total energy cost presumably equals the sum of the costs of fuelling each independent group of muscles. The figure for grazing (plus 8 beats/min) may include some leg as well as jaw movements, however, because 'standing grazing' involves sheep in taking occasional steps (see definitions of behavioural categories). Although these remarks do not apply to 'lying grazing', this was very transient and often preceded standing up, and it is possible that heart rate increased then in anticipation of standing up. It would be interesting to take this analysis further; the restriction to the behaviours analysed was imposed only by lack of sufficient data on other behaviours. Similar changes in heart rate with behaviour occur in bighorn sheep (MacArthur et al. 1979) and in white-tailed deer (Moen 1978). Both studies used behavioural categories 'bedded' (i.e. lying), 'standing', 'feeding' and 'walking'. These categories were mutually exclusive and not exactly equivalent to ours; for example, in our study feeding and standing sometimes occurred together. In bighorn sheep heart rate increased from 52 beats/rain when the sheep was bedded, by 5 beats/rain when the sheep stood, 21 beats/min when the sheep fed, or 29 beats/min when the sheep walked. In white-tailed deer (analysed using a different method, see below) heart rate increased from 72 beats/min when the deer was bedded, by 14 beats/rain when the deer was standing, 18 beats/min when the deer was feeding, or 30 beats/min when the deer was walking. The corresponding figures in our study would be an increase from about 80 beats/min when the ewe was lying, by 8 beats/min when she was standing, 16 beats/rain when she was standing feeding, or 15 beats/min when she was walking. Qualitatively similar changes also occur in calves (Holmes et al. 1976), ponies (Youkel et al. 1985) and humans (Strand 1978; Smith & Kampine
Baldock et al.: Heart rate and behaviour in sheep
1980). Allowing for species differences these figures are in fairly good agreement.
Seasonal Variation
Dramatic seasonal variation in heart rate in parallel with daylength is shown in Fig. 3, with a minimum in December and a maximum some 50% (46 beats/min) higher in June. This was expected because metabolic rate is known to show the same pattern, and changes in metabolic rate are likely to be reflected in changes in heart rate, as explained in the introduction. Thus Blaxter & Boyne (1982) showed that both fasting and maintenance metabolic rate vary seasonally, apparently sinusoidally from minima in midwinter to maxima 33% higher in midsummer. These results were derived from experiments in which animals were held at constant temperature and fed a fixed amount per day irrespective of season. Daylength varied naturally. Since food intake was constant, it could not have caused the observed changes in metabolic rate. However, other experiments have shown that voluntary intake of food shows the same pattern of variation (Gordon 1964; Milne et al. 1978; Kay 1979; Blaxter et al. 1982), probably in response to the changing metabolic needs (Blaxter & Boyne 1982). The heat associated with ingestion and digestion will therefore also vary seasonally, and can be expected to amplify the fluctuations in basal metabolic rate. Thus if there were a causal chain (daylength) (metabolic rate) ~ heart rate, this would partly explain our results, though the situation is complicated by the metabolic demands of reproduction in some of our animals and by changes in the quality and availability of food. Consider the implications if both reproduction and food processing are metabolically expensive. The total metabolic cost of processing food is probably at a minimum overwinter, when sheep on pasture in Britain have low intakes and are losing weight and condition. Reproductive costs are also low since pregnancy is in its early stages. New, more nutritional, grass becomes available, and more food is processed, in the spring, which is also the time of maximal fetal growth preceding birth. Metabolic costs increase on both counts. As the days lengthen, more time is available for daylight feeding and lactational requirements are maximal. During the summer the nutritive value of forage begins to decline, and the offspring are then fed less by the mother. Further
41
details of the energy costs of reproduction are to be found in Brockway et al. (1963). Thus the seasonal cycles of food availability and reproduction run in parallel; the metabolic costs of processing food and of reproduction in females may be closely correlated, and both may be correlated with basal metabolic rate and with heart rate. Ambient temperature lags behind daylength in the annual cycle, and some of the variation in heart rate may be to do with heating and cooling the body. Below a critical environmental temperature heat production is increased to maintain homeothermy, and heart rate therefore rises as temperature falls (Blaxter 1962; Brody 1964). Above this critical temperature little variation in heart rate with temperature is expected until the upper critical temperature is reached. On this basis, heart rate should be a maximum when ambient temperature is lowest, but this is the opposite of what was observed (Fig. 3). Therefore temperature regulation cannot be an important cause of the seasonal variation in heart rate. However, temperature regulation may account for the slight increase (6 beats/min) in heart rate in the week after shearing, when the ambient temperatures were in the range 8-20°C. Other studies have also shown an increase in heart rate inversely dependent on environmental temperature in the 2 weeks after shearing (Wodzicka-Tomaszewska 1 9 6 3 ; Wodzicka-Tomaszewska & Walmsley 1966; Donnelly et al. 1974), and food intake rises at pasture following shearing (Penning et al. 1986). The functional implications of the seasonal variation in basal metabolic rate deserve some attention. The reduction in winter must reduce energy consumption and to some extent alleviate the loss of weight and condition then experienced. Presumably, however, this is at some cost to the animal; if there were no cost, greater energy efficiency could be achieved year round, thus freeing resources to invest, for example, in offspring. What could be the cost of lowering metabolic rate? We suggest that the animals are more sluggish in winter, less prepared for flight in the event of danger. In the wild this would entail a mortality cost, but this could be worth paying in the winter in order to reduce the chances of starvation. The hypothesis that the animals are less prepared for flight in winter could be tested by observing their response to threatening stimuli, although a rigorous test would have to be carried
42
Animal Behaviour, 36, 1
out in controlled environmental conditions. Similar seasonal variation in heart rate has been reported in white-tailed deer (Moen 1978) and caribou (Rangifer tarandus, White & Fancy 1986). Moen pooled the heart-rate data from different individuals and fitted annual sine waves separately to data relating to each of four behaviours (bedded, standing, walking, and feeding): the amplitude of the sine wave was found by regression and the phase by iteration (the same phase was used for each behaviour). Heart rates were lowest on 15 February and highest on 15 August. The range of the annual oscillation was about 35 beats/min, compared with 46 beats/min here, and the minimum heart rate when lying was similar to that found here. Thus though Moen's results are broadly similar to ours, the exact timing of the peak and trough appear to differ, though this is not easy to assess because of the different methods of analysis. Nevertheless, it is clear from Fig. 3b that the minimum heart rate in our study occurred earlier than February and the maximum occurred earlier than August.
Energetic Implications What are the implications for energy expenditure of variation in heart rate? N o data are available on seasonal variation, but the increase in heart rate when an animal changes from lying to standing was estimated by Hall & Brody (1933) at 11-7 kJ/kg per day, by Joyce & Blaxter (1964) as 7.1 kJ/kg per day and by Webster & Valks (1966) at 11.8 kJ/kg per day. This gives an energy cost of approximately 700 kJ per day, or 486 J per min, in animals weighing 70 kg, such as those studied here. Since our results suggest that heart rate then increases by 7-6 beats/ min, it may be that metabolic rate increases by 64 J per min for every beat-per-rain increase in heart rate. Attractively simple as this result appears, it would require extensive checking in the field before we could know how accurate it is.
ACKNOWLEDGMENTS We are very grateful to Professor D. M. Broom for general and to Dr R. D. Stern for statistical advice, to Dr J. Brockway for invaluable comments on the manuscript, to A. R. Austin for veterinary services, a n d t o R. J. Orr, G. E. H o o p e r and members of the farm staff at A.G.R.I. for helping with the management of the sheep.
REFERENCES Agricultural Research Council. 1980. The Nutrient Requirements of Ruminant Livestock. Farnham Royal: Commonwealth Agricultural Bureaux. Baldock, N. M. 1985. Heart rate and behaviour recorded in sheep during undisturbed conditions and various husbandry practices. Ph.D. thesis, University of Reading. Baldock, N. M., Penning, P. D. & Sibly, R. M. In press. A system for recording sheep ECG in the field using a miniature 24-hour tape recorder. Comp. Electron. Agric. Blaxter, K. L. 1962. The Energy Metabolism of Ruminants. London: Hutchinson. Blaxter, K. L. & Boyne, A. W. 1982. Fasting and maintenance metabolism of sheep. J. agric. Sci., Camb., 99, 611~520. Blaxter, K. L., Fowler, V. R. & Gill, J. C. 1982. A study of the growth of sheep to maturity. J. agric. Sci., Camb., 98, 405420. Brockway, J. M. 1978. Escape from the chamber: alternative methods for large animal calorimetry. Proc. Nutr. Soc., 37, 13-19. Brockway, J. M., McDonald, J. D. & Pullar, J. D. 1963. The energy cost of reproduction in sheep. J. Physiol., 167, 318 327. Brody, S. 1964. Bioenergetics and Growth. New York: Hafner. Donnelly, J. B., Lynch, J. J. & Webster, M. E. D. 1974. Climatic adaption in recently shorn merino sheep. Inc. J. Biometeorol., 18, 233 247. Fukuhara, K., Sawai, T. & Yamamoto, S. 1983. The relationship between heart rate and heat production of dairy cows in prepartum and postpartum. Jap. J. Zootech. Sci., 54, 497 501. Gordon, J. G. 1964. Effect of time of year on the roughage intake of housed sheep. Nature, Lond., 204, 798-799. Hall, W. C. & Brody, S. 1933. Res. Bull. Mo. Agric. Exp. Stn., No. 180. Holmes, C. W., Stephens, D. B. & Toner, J. N. 1976. Heart rate as a possible indicator of the energy metabolism of calves kept out-of-doors. Livestock Prod. Sci., 3, 333-341. Jacobsen, N. K. 1979. Changes in heart rate with growth and activity of white-tailed deer fawns (Odocoileus virginianus). Comp. Biochem. Physiol., 62A, 885-888. Johnson, S. F. & Gessaman, J. A. 1973. An evaluation of heart rate as an indirect monitor of free-living energy metabolism. In: Ecological Energeties of Homeotherms (Ed. by J. A. Gessaman), pp. 44-54. Logan: Utah State University Press. Joyce, J. P. & Blaxter, K. L. 1964. The effect of air movement, air temperature and infrared radiation on the energy requirements of sheep. Br. J. Nutr., 18, 5-27. Kamau, J. M. Z. & Maloiy, G. M. O. 1982. The relationship between rate of oxygen consumption, heart rate and thermal conductance of the dik-dik antelope (Rhynchotragus kirkiO at various ambient temperatures. Comp. Biochem. Physiol., 73A, 21-24. Kay, R. N. B. 1979. Seasonal changes of appetite in deer and sheep. Agric. Res. Coun. Res. Rev., 5, 13-15. MacArthur, R. A., Johnston, R. H. & Geist, V. 1979.
Baldock et al.: Heart rate and behaviour in sheep Factors influencing heart rate in free-ranging bighorn sheep: a physiological approach to the study of wildlife harassment. Can. J. Zool., 52, 201(~2021. McCullagh, P. & Nelder, J. A. 1983. Generalised Linear Models. London: Chapman & Hall. Milne, J. A., MacRae, J. C., Spence, A. M. & Wilson, S. 1978. A comparison of the voluntary intake and digestion of a range of forages at different times of the year by sheep and the red deer (Cervus elaphus). Br. J. Nutr., 40, 347-357. Moen, A. N. 1978. Seasonal changes in heart rates, activity, metabolism, and foraging intake of whitetailed deer. J. Wildl. Mgmt, 42, 715-738. Pauls, R. W. 1980. Heart rate as an index of energy expenditure in red squirrels (Tamiasciurus hudsonicus). Comp. Biochem. Physiol., 67A, 409-418. Penning, P. D., Hooper, G. E. & Treacher, T. T. 1986. The effect of herbage allowance on intake and performance of ewes suckling twin lambs. Grass For. Sci., 41, 199-208. Shephard, R. J. 1982. Physiology and Biochemistry of Exercise. New York: Praeger. Smith, J. J. & Kampine, J. P. 1980. Circulatory Physiology. London: Williams & Wilkins. Strand, F. L. 1978. Physiology. New York: Collier Macmillan. Syme, L. A. & Elphick, G. R. 1982. Heart rate and the behaviour of sheep in yards. Appl. Anita. Ethol., 9, 3136. Tobioka, H., Kikuchi, M., Kato, M., Shibata, M., Kume, S., Takizwa, S., Yagi, M. & Nakanishi, Y. 1983. The
43
relationship between heart rate and heat production of Japanese brown cattle. Proc. Fac. Agric. Kyushu Tokai Univ., 2, 21 34. Webster, A. J. F. 1967. Continuous measurement of heart rate as an indicator of the energy expenditure of sheep. Br. J. Nutr., 21, 76~785. Webster, A. J. F. & Valks, D. 1966. The energy cost of standing in sheep. Proc. Nutri. Soc., 25, xxii. White, R. G. & Fancy, S. G. 1986. Nutrition and energetics of indigenous northern ungulates. In: Grazing Research at Northern Latitudes (Ed. by O. Gudmundsson), pp. 25%269. New York: Plenum Press. Wodzicka-Tomaszewska, M. 1963. The effect of shearing on the appetite of sheep. N. Z. J. agric. Res., 6, 440~447. Wodzicka-Tomaszewska, M. & Walmsley, R. R. 1966. A note on the testing of a sheep heart-rate transmitter. N. Z. J. agric. Res., 9, 455-459. Yamamoto, S. 1986. The relationship between heart rate and heat production of laying hens, using a fast response calorimetry. Jap. J. Zootech. Sci., 57, 310 316. Yamamoto, S., Sumida, M. & Kosako, T. 1985. Evaluation of fast-response calorimetry, used for calibration of the relationship between heart rate and heat production in farm animals. Jap. J. Zootech. Sci., 56, 947 953. Youkel, R. J., Camerale, J. M., Houpt, K. A. & Houpt, T. R. 1985. Humoral, hormonal and behavioural correlates of feeding in ponies: the effects of meal frequency. J. Anim. Sci., 61, 1103-1110.
(Received 14 October 1986; revised 24 February 1987; MS. number." 2912)
Behaviour and seasonal variation in heart rate in domestic sheep, Ovis aries N. M. B A L D O C K * t , R. M. SIBLY*$ & P. D. P E N N I N G §
*Department of Pure and Applied Zoology, University of Reading, Whiteknights, PO Box 228, Reading, Berkshire RG6 2A J, U.K. §Animal and Grassland Research Institute, Hurley, Maidenhead, Berkshire SL6 5LR, U.K. Abstract. Three major causes of heart rate variation in undisturbed adult ewes were identified: behaviour, season and individual identity. Heart rate was 8 beats/min lower when the ewe was lying than when she was standing. It was increased by ruminating by 2 beats/min above the value for idling, and by a further 6 beats/min when the ewe changed to grazing. It seems that the increases in heart rate when the ewe was standing were simply added to those associated with ruminating or grazing. Heart rate declined slightly during bouts of unchanged behaviour. It varied seasonally from a minimum in December to a maximum some 50% (46 beats/min) higher in June. This variation was closely linked with daylength, basal metabolic rate, food availability, food consumption and the reproductive cycle, although it also occurred in nonbreeding animals. Changes in heart rate associated with daylength may be the secondary result of the effects ofdaylength on metabolic rate. After taking all these effects into account, there remained variation between five ewes of 16 beats/min.
The association between behaviour and heart rate has been studied in humans (e.g. Strand 1978; Smith & Kampine 1980), and some work has been done on other animals (e.g. bighorn sheep, Ovis canadensis, MacArthur et al. 1979; white-tailed deer, Odocoileus virginianus, Moen 1978; Jacobsen 1979). In view of this, it is surprising that no comprehensive study exists, of the type reported here, relating heart rate to behaviour, environmental variables and individual identity, since a full understanding of the implications of behaviour for heart rate would have many uses. For example, it would help assess the metabolic implications of behaviour, because a major function of the blood is to supply oxygen to the muscles. Oxygen supply depends not only on heart rate, but also on the stroke volume of the heart and arterial-venous oxygen differences (Shephard 1982). Nevertheless, heart rate is a reasonably good index of the metabolism of mammals and birds, at rest or exercising moderately, provided they are free from stress (Johnson & Gessaman 1973; but see also Brockway 1978). The study reported here satisfies these conditions. Correlations between individual heart rate and energy expenditure have been good (greater than 0"85) in most recent studies (Holmes et al. 1976; Pauls 1980; Kamau & Maloiy 1982; Fukuhara et al. 1983; Tobioka et al. 1983; Yama-
moto et al. 1985; Yamamoto 1986). Seasonal variation in heart rate is expected because basal metabolic rate (Blaxter & Boyne 1982) and the amount of food consumed per day (Gordon 1964; Milne et al. 1978; Kay 1979; Blaxter et al. 1982) change from a minimum in midwinter to a maximum in midsummer, in parallel with changes in daylength. Indeed daylength is the principal cause of seasonal changes in food intake (Kay 1979). Higher metabolic activity requires an increased oxygen supply to the body tissues and this in turn is likely to require an increased blood supply, and, therefore, an increased heart rate. In this paper, we investigate the effects on heart rate of behaviour, individual identity and environmental variables. In order to obtain information on undisturbed sheep, ewes were kept in relatively normal farm conditions, and a series of monthly recordings was made over a period of a year. Multiple regression was used to identify the magnitude and confidence limits of each effect.
METHODS
Animals
All work was carried out at the Animal and Grassland Research Institute, Hurley, near Maidenhead, Berkshire, U.K. during 1983 and 1984. The study animals were domestic sheep, Ovis
t Present address: 47, Corfe Road, Melksham, Wiltshire, U.K. $ To whom all correspondence should be addressed. 35
36
Animal Behaviour, 36, 1
aries, from a flock of 149 Scottish half bred ewes (Border Leicester ram x Cheviot ewe) 2 and 3 years old. These ewes had all been handled previously. On 24 January 1983, six randomly chosen ewes were separated into a subflock (flock 1) for further study. Recordings were made from five of these animals on 17 study days between 16 March 1983 and 9 February 1984. No records were made from the sixth animal, which was included as a 'reserve'. A further 16 randomly chosen ewes were separated into a subflock (flock 2) on 19 February 1984. Recordings were made from four of these animals on three study days between 9 and 30 March 1984. All the animals were kept on pasture, though intake was supplemented by hay during the winter.
Recording Equipment The recording method was based on a taperecorder system available commercially for the recording and analysis of ECG in humans (Oxford Medical Systems, Nuffield Way, Abingdon, U.K.). As developed for sheep, the system comprised two electrodes (attached to or immediately below the skin) connected to a tape-recorder mounted in a special harness on the animal's back, and a replay unit with signal decoder and microprocessor to transfer data to floppy disk for eventual transfer to a mainframe computer. Full details are given in Baldock et al. (in press).
Behaviour Recordings All observations of behaviour were made from a parked vehicle overlooking the field containing the ewes. Other vehicles were regularly parked nearby. We obtained access discreetly and quietly, making every effort not to disturb the sheep. As far as we could tell, the behaviour of the sheep was not affected by the observer's presence.
Behavioural categories Categories were chosen to be mutually exclusive and to cover all commonly occurring behaviours. Behaviours were classified as either standing or lying followed by a further classification as defined below. (1) Grazing: the initial intake of grass was taken as the start of a grazing bout. The termination of a bout occurred when the animal either lifted her head above the horizontal or lay down. Occasional steps were taken (but see category 7).
(2) Eating hay: the manipulating, ingesting or masticating of hay from the feeder. (3) Alert: neck raised and ears pricked forward. (4) Idling: any posture not involvingjaw or limb movements, and not in an alert or head down position. (5) Ruminating: rumination bouts began when a bolus was seen to be regurgitated. The end of a bout occurred when jaw movements had ceased for longer than 20 s, Or the animal had changed posture. (6) Head down: an animal with her head touching the ground and not moving her jaw. The individual'seyes were often closed, but this was not taken as a criterion for this category. (7) Walking: slow motion during which the animal was not grazing, in which at least one forefoot and one hindfoot were on the ground at any one time. In addition, notes were made of other occasional behaviours (e.g. drinking, vocalizing). Behaviour was recorded at intervals of 1 min. Since behaviour could be observed carefully prior to recording, it is thought that errors were negligible. Identification of animals was aided by painting numbers on the fleeces and backpacks,
Experimental Procedure On each study day the study animals were moved into a handling pen and harnesses, tape-recorder and electrodes (where necessary) were attached. The animals were then released back into the pasture in which they were ordinarily kept. Since it was known that the effects of this handling procedure disappeared within 5 min of release from the pen (Baldock et al., in press), heart rate and behaviour were sampled thereafter at 1-min intervals for 4-7 h between 0900 and 1800 hours. During the observation period normal farm activities continued, resulting in minor disturbances, which were noted.
Analysis In order to gain an overall, if somewhat simplistic model of the causes of heart-rate variability in sheep, multiple regression analyses were carried out on the data from each flock, fitting the equation heart rate =
a + Eeixi q-- ~biyi + Edizi Jr cl + ~ i
i
i
(1)
37
Baldock et al.. Heart rate and behaviour in sheep
Here a is a constant. The variable xi is a dummy variable (McCullagh & Nelder 1983, page 40) taking the value I if the heart rate is that of ewe number i, zero otherwise. The number of xl variables corresponds to the number of ewes minus one (see below). The coefficient ei (to be estimated in the regression analysis) therefore represents the effect of being ewe number i. For example if ewe number 2 bad heart rate 20 beats/min higher than ewe number 3 (other things being equal, see below) then e2 - e3 + 20 beats/min. The number of x~ variables is one less than the number of ewes because there would otherwise be too many degrees of freedom in the regression. This is because by convention in the statistical package used (Glim 3.77, McCullagh & Nclder 1983) the constant a (in equation 1) represents the average heart rate of ewe number 1 when performing behaviour number 1 (i.e. 'standing grazing') on the first observation day (16 March 1983). Therefore the regression does not provide values el, b] or d~ since this eventuality has already been allowed for. The variable y~ is a dummy variable taking the value l if the measured heart rate occurred while behaviour number i was being performed, zero otherwise. The number ofy~ variables corresponds to the number of behaviours that were recorded. The coefficient b~ therefore represents the effect on heart rate of performing behaviour number i. The variable zl is a dummy variable taking the value I if the heart rate occurred on study day number i. The number of z~ variables corresponds to the number of study days minus one. The coefficient di represents the effect on heart rate of day number i. For example if in the third recording (made on 4 May) heart rate was 29.6 beats/min lower than in the fourth recording made on 5 June (other things being equal) then d3= d 4 - 29.6 beats/min. The variable l measures bout duration (in rain) and the coefficient c represents the effect on heart rate of bout duration, e is the residual error, i.e. the discrepancy between predicted and observed heart rate. A number of checks were made on the distribution of e from which it appeared safe to assume e had a normal distribution. The order in which factors were entered into the analysis was changed systematically in order to gain an understanding of the relative importance of each factor. The final order was used in the analyses of both flocks and was decided on by consideration of the relative biological importance of each factor.
• standing grazing
o
• standing idling
~ lying idling
• standing alert
o lying head down
120
Lying ruminating
[2
•
t
t~
~100
gO
g
-"
•*,
0
I•
~o
o
o
[]
'k
o ~
0
80
COO d:~ ~
•
OD
O 0
o
60
0
1
2 Time (hi
3
t+
Figure 1. The heart rate and behaviour of ewe 5 on 13
April 1983.
RESULTS An example of a recording is shown in Fig. 1. The animal spent about half her time standing and half lying, and the heart rate was consistently higher by some 20 beats/rain when she was standing. Table I shows that the predictor variables shown in equation (1) accounted for 65% of the variation in heart rate in flock I, and 50% of the variation in flock 2. These figures indicate success in predicting instantaneous heart rate (i.e. the reciprocal of the interval between successive heart beats), which is probably subject to a certain amount of random noise, and is affected by environmental variables (e.g. sight of dogs) not entered in the regression, apart from the known measurement errors of our equipment (about 3 beats/min, Baldock 1985). The residual standard deviations for the two flocks were
Table I. Results of multiple regression analysis on data
from flocks 1 and 2 showing the percentage of the total heart-rate variation explained by each class of variable % Total heart-rate variation Variable class Ewe Behaviour Bout length Day Total
Flock 1
Flock 2
21 6 1 38 66
19 28 0 3 50
Animal Behaviour, 36, 1
38
10 b e a t s / m i n a n d 7 b e a t s / m i n , so the v a r i a t i o n a c c o u n t e d for is p r o b a b l y n e a r the limit o f w h a t is achievable w i t h o u r e q u i p m e n t a n d m e t h o d o f analysis. M o r e o f the v a r i a t i o n was explained in flock 1 t h a n in flock 2 b e c a u s e the d a y effects p r o d u c e d m u c h less v a r i a t i o n in the latter, w h i c h was o b s e r v e d over a s h o r t e r p e r i o d . T h e e x p l a n a tion o f this result is d i s c u s s e d below. E s t i m a t e s o f the effects o f the p r e d i c t o r variables are s h o w n in T a b l e II. T h e r e were large differences T a b l e !I. Effect (beats/min) on heart rate of each of the predictor variables shown in equation (l)
Parameter
Flock 1
Flock 2
Estimate (SE)
Estimate (SE)
in h e a r t rate b e t w e e n the ewes (the r a n g e s b e i n g 16 a n d 15 b e a t s / m i n in flocks 1 a n d 2 respectively). C o n s i s t e n t l y different levels o f h e a r t rate b e t w e e n individuals are also seen in o t h e r studies o f s h e e p ( W e b s t e r 1967; M a c A r t h u r et al. 1979; S y m e & E l p h i c k 1982) a n d in white-tailed d e e r ( M o e n 1978). S o m e o f the differences in flock 1 c o u l d be e x p l a i n e d o n t h e basis o f the e w e ' s w e i g h t a n d age (71%, dJ] = 2, dJ~= 2, F = 2 - 4 2 , Ns), t h e o l d e r ewes h a v i n g lower h e a r t rates. S y m e ( p e r s o n a l c o m m u n i c a t i o n ) f o u n d a similar r e l a t i o n s h i p b e t w e e n age a n d h e a r t rate in M e r i n o sheep. H o w e v e r , this c a n n o t be t h e c o m p l e t e e x p l a n a t i o n b e c a u s e similar v a r i a t i o n o c c u r r e d in flock 2, in w h i c h all ewes were the s a m e age.
Effects
General mean Ewe 2 Ewe 3 Ewe 4 Ewe 5 Ewe 8 Ewe 9 Ewe I0 Standing idling Standing alert Standing ruminating Lying idling Lying head down Lying ruminating Lying grazing Walking Standing eating hay Bout length (min) 13 April 1983 20 April 1983 4 May 1983 5 June 1983 12 June 1983 2 July 1983 16 July 1983 9 August 1983 24 August 1983 13 October 1983 18 October 1983 15 November 1983 24 November 1983 9 December 1983 17 January 1984 9 February 1984 20 March 1984 30 March 1984
100.6 - 11-9 - 8.2 - 3.8 4.1
-
10.2 8.0 8.3 17.3 16.3 14.5 9.7 2.0 3.2 0.06 7.4 24.6 - 7.6 22.0 27.0 5.6 6.4 5-3 - 2.0 - 7.4 -- 1.9 - 5.7 - 11-5 - 19.4 - 2-6 1.3
(0.7) (0.5) (0.5) (0.4) (0.4)
81.4 -----
(0.4) -----
--
-
10.7
(0.5)
--
-
5.2
(0.5)
--
-15.1
(0-5)
- 4.9 - 5-1 - 6.9 - 15.1 -14.3 - 9.5
(1.2) (0.9) (2.0) (0.6) (0.8) (0-4)
(0.5) (0.8) (0.7) (0.5) (0.5) (0-4) (1.1)
--
.2) 0.7 (O.7) 0.2 (0.007) -- 0.02 (0.8) --
(I
--
(1.0) (O.7) (0.01) --
(1.4)
--
--
(1.3)
----
----
----------
----------
(0.9) (0.7) (0.9) (0-7) (0.7) (0.7) (0-9) (0.9) (0.8) (0.6) (0.7) (0.7) (0-7) ---
-
--
-
-
of
Behaviour
C h a n g e s in h e a r t rate a s s o c i a t e d w i t h c h a n g e s in b e h a v i o u r h a d a r a n g e o f 17 b e a t s / m i n in flock 1 a n d 16 b e a t s / m i n in flock 2 (Table II). T h e c h a n g e s in h e a r t rate are illustrated in Fig. 2. T h e r e is a n excellent c o r r e l a t i o n b e t w e e n the analyses c a r r i e d o u t i n d e p e n d e n t l y for t h e t w o flocks. I n each case the lowest h e a r t rate was a s s o c i a t e d with lying idling. A n increase o f a b o u t 8 b e a t s / m i n o c c u r r e d when the animal stood, and about another 7 beats/ m i n if she t h e n w a l k e d . S u p e r i m p o s e d o n these are c h a n g e s a s s o c i a t e d w i t h j a w m o v e m e n t s , so t h a t ruminating added about 2 beats/min and grazing a b o u t 8 b e a t s / m i n . A l t h o u g h this is s o m e t h i n g o f a simplification ( b e c a u s e o u r ' s t a n d i n g g r a z i n g ' categ o r y a l l o w e d o c c a s i o n a l leg m o v e m e n t s ) it d o e s suggest t h e h y p o t h e s i s t h a t the c h a n g e s in h e a r t rate a s s o c i a t e d w i t h i n d e p e n d e n t m o v e m e n t s m a y be additive, in t h e sense t h a t if m o v e m e n t A increases h e a r t rate b y hA b e a t s / m i n , a n d m o v e m e n t B b y hB b e a t s / m i n , t h e n if the t w o m o v e m e n t s are m a d e s i m u l t a n e o u s l y , h e a r t rate will increase by h A + h s b e a t s / m i n . I n o r d e r to test this h y p o t h e s i s , d a t a f r o m T a b l e II p e r t a i n i n g to s t a n d i n g o r lying, idling, r u m i n a t i n g , o r grazing, were used to see w h e t h e r d e v i a t i o n s f r o m the s t a n d i n g - g r a z i n g values c o u l d be a d e q u a t e l y d e s c r i b e d b y t h e equation
-
2.8
(0.4)
2.5
(0.4)
- - = missing data. Values show the differences from the heart rate of ewe 1 when standing grazing on 16 March 1983 (flock 1), or ewe 7 when standing grazing on 9 March 1984 (flock 2). See Methods for further details.
h e a r t rate = lxl+ mxm + rxr + e
(2)
w h e r e xt, xm a n d x, are d u m m y variables such t h a t xl = 1, xm = 1 o r xr = 1 if the a n i m a l is lying, idling, o r r u m i n a t i n g , respectively; o t h e r w i s e the d u m m y variables are zero. T h u s if all the d u m m y variables are zero the a n i m a l was n o t lying, n o t idling a n d
Baldock et al.." Heart rate and behaviour in sheep Flock 1 •
Flock 2
•
o
m~ --5
-10 "t -15
Lying
Standing
Figure 2. Heart-rate changes associated with various behaviours.
not ruminating, i.e. it was standing grazing. Equation (2) accounts for 96% of the variation, using three predictor variables, which is virtually all of the 97% accounted for by a 5-predictor model of the type shown in equation (1). This supports the hypothesis that changes in heart rate associated with individual movements are additive. The estimates obtained suggest that heart rate is lowest when the animal is lying idling. If the animal stands then heart rate is increased by 7.6 beats/min. If it changes from idling to any other behaviour then heart rate increases further, by 8-1 beats/min if it changes to grazing, or 2.1 beats/min if it changes to ruminating. Standard errors were 1.6 beats/min in each case ( N = 6). These results provide a quantitative summary of some of the data in Fig. 2.
Seasonal Variation As explained in the introduction, seasonal variation in heart rate, in parallel with daylength, was predicted, from a minimum in midwinter to a maximum in midsummer. The expected seasonal changes in heart rate are seen when the effects of the day variables are plotted against date for flock 1 (Fig. 3). Thus heart rate increased by 46 beats/min from a minimum in December to a maximum in June, and thereafter declined steadily until the following December. As a check on these results
39
the data for each ewe were analysed separately (using equation 1 without the ewe variables); the individual ewes showed parallel changes in heart rate (Fig. 3b). Changes in heart rate are taken to be zero on 16 March 1983 (see Methods). Since many environmental variables vary in parallel between the solstices in June and December, there is little chance of accurately distinguishing their effects. Nevertheless, as a first step, daylength (which varies sinusoidally between extreme values at the solstices) and temperature (which lags somewhat behind daylength) were investigated. Daylength was the most important predictor of the changes in heart rate shown in Fig. 3a, accounting for 76% of the variation (F=44-8, dJ]=l, dj~=15, P<0.01). When entered subsequently, temperature accounted for a further 10% (F=9.9, dfl = 1, dJ~= 14, P<0.01). (When entered first, temperature accounted for 24% of the seasonal variation in heart rate with an estimated effect of 0.6 beats/min per °C.) There was no cumulative effect of the experiment on heart rate as judged by the negligible effect of time since the first recording, after allowance had been made for daylength and temperature (F=0-1, d~ = 1, dJ~= 13, ys). Since breeding has an annual cycle, some of the variation seen in Fig. 3 might be due to the metabolic demands of reproduction. All ewes in flock 1 were artificially inseminated on 10 November 1983 and some became pregnant and gave birth to a single lamb as indicated in Fig. 3b. Ewes 1 and 4 were lactating in June and July 1983. There was no difference between the heart rates of the pregnant and non-pregnant ewes in November and December, when the metabolic demands of reproduction are low (Agricultural Research Council 1980), but there is a suggestion that between February and July (when metabolic demands of reproduction are highest, Agricultural Research Council 1980) heart rate was higher in the breeding than in the non-breeding animals (Fig. 3b). With such small sample sizes we did not attempt to estimate the magnitude of these effects. However, it is clear from Fig. 3 that the changes in heart rate in non-breeding animals parallel those in breeding animals, so direct metabolic demands of breeding are unlikely to be the whole explanation for the seasonal variation in heart rate. An increase of (~7 beats/min was found between the heart rates of two ewes recorded 5 days postshearing compared with their heart rates 2 days pre-shearing (standard errors were less than 2 in
40
Animal Behaviour, 36, 1
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Figure 3. Seasonal changes in heart rate. (a) Heart-rate data from Table II excluding days when only one ewe was recorded. Daylength and ambient temperature are also shown. (b) Results of independent analyses carried out for each ewe separately. Numbers refer to ewe identity. p: pregnant; m: lactating.
both cases). Shearing occurred on 7 June 1983. Seasonal variation at this time of year was decreasing heart rate by about I beat/min per week so these results could not be due to the seasonal variation described above.
DISCUSSION This study has identified three major causes of variation in heart rate in adult ewes: behaviour (Fig. 2), season (Fig. 3) and individual identity. A linear model of the causes of change in heart rate accounted for up to 65% of the variation (Table I), and yielded precise estimates of the effects of each predictor with standard errors generally less than 1 beat/rain (Table II).
Effects of Behaviour The changes in heart rate associated with behaviour tally with expectations. Thus heart rate was 8 beats/min lower when the ewe was lying than when she was standing. It was increased by ruminating by 2 beats/min above the value for idling, and was 8 beats/min higher for grazing than for idling ewes. It seems the heart-rate costs of standing are simply added to those associated with ruminating or grazing, which is why successful prediction is possible using equation (2). This is not surprising since the blood supplies energy to the muscles, and the total energy cost presumably equals the sum of the costs of fuelling each independent group of muscles. The figure for grazing (plus 8 beats/min) may include some leg as well as jaw movements, however, because 'standing grazing' involves sheep in taking occasional steps (see definitions of behavioural categories). Although these remarks do not apply to 'lying grazing', this was very transient and often preceded standing up, and it is possible that heart rate increased then in anticipation of standing up. It would be interesting to take this analysis further; the restriction to the behaviours analysed was imposed only by lack of sufficient data on other behaviours. Similar changes in heart rate with behaviour occur in bighorn sheep (MacArthur et al. 1979) and in white-tailed deer (Moen 1978). Both studies used behavioural categories 'bedded' (i.e. lying), 'standing', 'feeding' and 'walking'. These categories were mutually exclusive and not exactly equivalent to ours; for example, in our study feeding and standing sometimes occurred together. In bighorn sheep heart rate increased from 52 beats/rain when the sheep was bedded, by 5 beats/rain when the sheep stood, 21 beats/min when the sheep fed, or 29 beats/min when the sheep walked. In white-tailed deer (analysed using a different method, see below) heart rate increased from 72 beats/min when the deer was bedded, by 14 beats/rain when the deer was standing, 18 beats/min when the deer was feeding, or 30 beats/min when the deer was walking. The corresponding figures in our study would be an increase from about 80 beats/min when the ewe was lying, by 8 beats/min when she was standing, 16 beats/rain when she was standing feeding, or 15 beats/min when she was walking. Qualitatively similar changes also occur in calves (Holmes et al. 1976), ponies (Youkel et al. 1985) and humans (Strand 1978; Smith & Kampine
Baldock et al.: Heart rate and behaviour in sheep
1980). Allowing for species differences these figures are in fairly good agreement.
Seasonal Variation
Dramatic seasonal variation in heart rate in parallel with daylength is shown in Fig. 3, with a minimum in December and a maximum some 50% (46 beats/min) higher in June. This was expected because metabolic rate is known to show the same pattern, and changes in metabolic rate are likely to be reflected in changes in heart rate, as explained in the introduction. Thus Blaxter & Boyne (1982) showed that both fasting and maintenance metabolic rate vary seasonally, apparently sinusoidally from minima in midwinter to maxima 33% higher in midsummer. These results were derived from experiments in which animals were held at constant temperature and fed a fixed amount per day irrespective of season. Daylength varied naturally. Since food intake was constant, it could not have caused the observed changes in metabolic rate. However, other experiments have shown that voluntary intake of food shows the same pattern of variation (Gordon 1964; Milne et al. 1978; Kay 1979; Blaxter et al. 1982), probably in response to the changing metabolic needs (Blaxter & Boyne 1982). The heat associated with ingestion and digestion will therefore also vary seasonally, and can be expected to amplify the fluctuations in basal metabolic rate. Thus if there were a causal chain (daylength) (metabolic rate) ~ heart rate, this would partly explain our results, though the situation is complicated by the metabolic demands of reproduction in some of our animals and by changes in the quality and availability of food. Consider the implications if both reproduction and food processing are metabolically expensive. The total metabolic cost of processing food is probably at a minimum overwinter, when sheep on pasture in Britain have low intakes and are losing weight and condition. Reproductive costs are also low since pregnancy is in its early stages. New, more nutritional, grass becomes available, and more food is processed, in the spring, which is also the time of maximal fetal growth preceding birth. Metabolic costs increase on both counts. As the days lengthen, more time is available for daylight feeding and lactational requirements are maximal. During the summer the nutritive value of forage begins to decline, and the offspring are then fed less by the mother. Further
41
details of the energy costs of reproduction are to be found in Brockway et al. (1963). Thus the seasonal cycles of food availability and reproduction run in parallel; the metabolic costs of processing food and of reproduction in females may be closely correlated, and both may be correlated with basal metabolic rate and with heart rate. Ambient temperature lags behind daylength in the annual cycle, and some of the variation in heart rate may be to do with heating and cooling the body. Below a critical environmental temperature heat production is increased to maintain homeothermy, and heart rate therefore rises as temperature falls (Blaxter 1962; Brody 1964). Above this critical temperature little variation in heart rate with temperature is expected until the upper critical temperature is reached. On this basis, heart rate should be a maximum when ambient temperature is lowest, but this is the opposite of what was observed (Fig. 3). Therefore temperature regulation cannot be an important cause of the seasonal variation in heart rate. However, temperature regulation may account for the slight increase (6 beats/min) in heart rate in the week after shearing, when the ambient temperatures were in the range 8-20°C. Other studies have also shown an increase in heart rate inversely dependent on environmental temperature in the 2 weeks after shearing (Wodzicka-Tomaszewska 1 9 6 3 ; Wodzicka-Tomaszewska & Walmsley 1966; Donnelly et al. 1974), and food intake rises at pasture following shearing (Penning et al. 1986). The functional implications of the seasonal variation in basal metabolic rate deserve some attention. The reduction in winter must reduce energy consumption and to some extent alleviate the loss of weight and condition then experienced. Presumably, however, this is at some cost to the animal; if there were no cost, greater energy efficiency could be achieved year round, thus freeing resources to invest, for example, in offspring. What could be the cost of lowering metabolic rate? We suggest that the animals are more sluggish in winter, less prepared for flight in the event of danger. In the wild this would entail a mortality cost, but this could be worth paying in the winter in order to reduce the chances of starvation. The hypothesis that the animals are less prepared for flight in winter could be tested by observing their response to threatening stimuli, although a rigorous test would have to be carried
42
Animal Behaviour, 36, 1
out in controlled environmental conditions. Similar seasonal variation in heart rate has been reported in white-tailed deer (Moen 1978) and caribou (Rangifer tarandus, White & Fancy 1986). Moen pooled the heart-rate data from different individuals and fitted annual sine waves separately to data relating to each of four behaviours (bedded, standing, walking, and feeding): the amplitude of the sine wave was found by regression and the phase by iteration (the same phase was used for each behaviour). Heart rates were lowest on 15 February and highest on 15 August. The range of the annual oscillation was about 35 beats/min, compared with 46 beats/min here, and the minimum heart rate when lying was similar to that found here. Thus though Moen's results are broadly similar to ours, the exact timing of the peak and trough appear to differ, though this is not easy to assess because of the different methods of analysis. Nevertheless, it is clear from Fig. 3b that the minimum heart rate in our study occurred earlier than February and the maximum occurred earlier than August.
Energetic Implications What are the implications for energy expenditure of variation in heart rate? N o data are available on seasonal variation, but the increase in heart rate when an animal changes from lying to standing was estimated by Hall & Brody (1933) at 11-7 kJ/kg per day, by Joyce & Blaxter (1964) as 7.1 kJ/kg per day and by Webster & Valks (1966) at 11.8 kJ/kg per day. This gives an energy cost of approximately 700 kJ per day, or 486 J per min, in animals weighing 70 kg, such as those studied here. Since our results suggest that heart rate then increases by 7-6 beats/ min, it may be that metabolic rate increases by 64 J per min for every beat-per-rain increase in heart rate. Attractively simple as this result appears, it would require extensive checking in the field before we could know how accurate it is.
ACKNOWLEDGMENTS We are very grateful to Professor D. M. Broom for general and to Dr R. D. Stern for statistical advice, to Dr J. Brockway for invaluable comments on the manuscript, to A. R. Austin for veterinary services, a n d t o R. J. Orr, G. E. H o o p e r and members of the farm staff at A.G.R.I. for helping with the management of the sheep.
REFERENCES Agricultural Research Council. 1980. The Nutrient Requirements of Ruminant Livestock. Farnham Royal: Commonwealth Agricultural Bureaux. Baldock, N. M. 1985. Heart rate and behaviour recorded in sheep during undisturbed conditions and various husbandry practices. Ph.D. thesis, University of Reading. Baldock, N. M., Penning, P. D. & Sibly, R. M. In press. A system for recording sheep ECG in the field using a miniature 24-hour tape recorder. Comp. Electron. Agric. Blaxter, K. L. 1962. The Energy Metabolism of Ruminants. London: Hutchinson. Blaxter, K. L. & Boyne, A. W. 1982. Fasting and maintenance metabolism of sheep. J. agric. Sci., Camb., 99, 611~520. Blaxter, K. L., Fowler, V. R. & Gill, J. C. 1982. A study of the growth of sheep to maturity. J. agric. Sci., Camb., 98, 405420. Brockway, J. M. 1978. Escape from the chamber: alternative methods for large animal calorimetry. Proc. Nutr. Soc., 37, 13-19. Brockway, J. M., McDonald, J. D. & Pullar, J. D. 1963. The energy cost of reproduction in sheep. J. Physiol., 167, 318 327. Brody, S. 1964. Bioenergetics and Growth. New York: Hafner. Donnelly, J. B., Lynch, J. J. & Webster, M. E. D. 1974. Climatic adaption in recently shorn merino sheep. Inc. J. Biometeorol., 18, 233 247. Fukuhara, K., Sawai, T. & Yamamoto, S. 1983. The relationship between heart rate and heat production of dairy cows in prepartum and postpartum. Jap. J. Zootech. Sci., 54, 497 501. Gordon, J. G. 1964. Effect of time of year on the roughage intake of housed sheep. Nature, Lond., 204, 798-799. Hall, W. C. & Brody, S. 1933. Res. Bull. Mo. Agric. Exp. Stn., No. 180. Holmes, C. W., Stephens, D. B. & Toner, J. N. 1976. Heart rate as a possible indicator of the energy metabolism of calves kept out-of-doors. Livestock Prod. Sci., 3, 333-341. Jacobsen, N. K. 1979. Changes in heart rate with growth and activity of white-tailed deer fawns (Odocoileus virginianus). Comp. Biochem. Physiol., 62A, 885-888. Johnson, S. F. & Gessaman, J. A. 1973. An evaluation of heart rate as an indirect monitor of free-living energy metabolism. In: Ecological Energeties of Homeotherms (Ed. by J. A. Gessaman), pp. 44-54. Logan: Utah State University Press. Joyce, J. P. & Blaxter, K. L. 1964. The effect of air movement, air temperature and infrared radiation on the energy requirements of sheep. Br. J. Nutr., 18, 5-27. Kamau, J. M. Z. & Maloiy, G. M. O. 1982. The relationship between rate of oxygen consumption, heart rate and thermal conductance of the dik-dik antelope (Rhynchotragus kirkiO at various ambient temperatures. Comp. Biochem. Physiol., 73A, 21-24. Kay, R. N. B. 1979. Seasonal changes of appetite in deer and sheep. Agric. Res. Coun. Res. Rev., 5, 13-15. MacArthur, R. A., Johnston, R. H. & Geist, V. 1979.
Baldock et al.: Heart rate and behaviour in sheep Factors influencing heart rate in free-ranging bighorn sheep: a physiological approach to the study of wildlife harassment. Can. J. Zool., 52, 201(~2021. McCullagh, P. & Nelder, J. A. 1983. Generalised Linear Models. London: Chapman & Hall. Milne, J. A., MacRae, J. C., Spence, A. M. & Wilson, S. 1978. A comparison of the voluntary intake and digestion of a range of forages at different times of the year by sheep and the red deer (Cervus elaphus). Br. J. Nutr., 40, 347-357. Moen, A. N. 1978. Seasonal changes in heart rates, activity, metabolism, and foraging intake of whitetailed deer. J. Wildl. Mgmt, 42, 715-738. Pauls, R. W. 1980. Heart rate as an index of energy expenditure in red squirrels (Tamiasciurus hudsonicus). Comp. Biochem. Physiol., 67A, 409-418. Penning, P. D., Hooper, G. E. & Treacher, T. T. 1986. The effect of herbage allowance on intake and performance of ewes suckling twin lambs. Grass For. Sci., 41, 199-208. Shephard, R. J. 1982. Physiology and Biochemistry of Exercise. New York: Praeger. Smith, J. J. & Kampine, J. P. 1980. Circulatory Physiology. London: Williams & Wilkins. Strand, F. L. 1978. Physiology. New York: Collier Macmillan. Syme, L. A. & Elphick, G. R. 1982. Heart rate and the behaviour of sheep in yards. Appl. Anita. Ethol., 9, 3136. Tobioka, H., Kikuchi, M., Kato, M., Shibata, M., Kume, S., Takizwa, S., Yagi, M. & Nakanishi, Y. 1983. The
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relationship between heart rate and heat production of Japanese brown cattle. Proc. Fac. Agric. Kyushu Tokai Univ., 2, 21 34. Webster, A. J. F. 1967. Continuous measurement of heart rate as an indicator of the energy expenditure of sheep. Br. J. Nutr., 21, 76~785. Webster, A. J. F. & Valks, D. 1966. The energy cost of standing in sheep. Proc. Nutri. Soc., 25, xxii. White, R. G. & Fancy, S. G. 1986. Nutrition and energetics of indigenous northern ungulates. In: Grazing Research at Northern Latitudes (Ed. by O. Gudmundsson), pp. 25%269. New York: Plenum Press. Wodzicka-Tomaszewska, M. 1963. The effect of shearing on the appetite of sheep. N. Z. J. agric. Res., 6, 440~447. Wodzicka-Tomaszewska, M. & Walmsley, R. R. 1966. A note on the testing of a sheep heart-rate transmitter. N. Z. J. agric. Res., 9, 455-459. Yamamoto, S. 1986. The relationship between heart rate and heat production of laying hens, using a fast response calorimetry. Jap. J. Zootech. Sci., 57, 310 316. Yamamoto, S., Sumida, M. & Kosako, T. 1985. Evaluation of fast-response calorimetry, used for calibration of the relationship between heart rate and heat production in farm animals. Jap. J. Zootech. Sci., 56, 947 953. Youkel, R. J., Camerale, J. M., Houpt, K. A. & Houpt, T. R. 1985. Humoral, hormonal and behavioural correlates of feeding in ponies: the effects of meal frequency. J. Anim. Sci., 61, 1103-1110.
(Received 14 October 1986; revised 24 February 1987; MS. number." 2912)