Fostering in sheep. III. Facilitation by the use of odorants

Applied Animal Behaviour Science, 14 (1985) 3 4 5 - - 3 5 4

345

Elsevier Science Publishers B.V., A m s t e r d a m - - P r i n t e d in The Netherlands

FOSTERING IN SHEEP. III. FACILITATION BY THE USE OF ODORANTS

G. A L E X A N D E R and D. S T E V E N S

CSIRO Division of Animal Production, Sydney (P.O. Box 239, Blacktown, N.S.W. 2148) (Australia) ( A c c e p t e d for publication 27 F e b r u a r y 1985)

ABSTRACT A l e x a n d e r , G. and Stevens, D., 1985. Fostering in sheep. III. Facilitation by the use o f odorants. Appl. Anita. Behav. Sci., 14: 345--354. L a m b s were t h o r o u g h l y a n o i n t e d with various odoriferous substances to test the facilitatory effects on substitutive fostering on to multiparous Merino ewes held in individual pens. The ewes were first familiarised with an o d o r a n t by anointing their o w n lamb with it 24 h before a similarly a n o i n t e d foster lamb was presented. The odorants were n e a t s f o o t oil, w o o l wax, vegetable oil, butyric and p r o p i o n i c acids, mercaptoethanol, vanillin, m e t h y l salicylate and eucalyptus oil. A c c e p t a n c e of foster lambs was assessed over the n e x t 48 h. O d o r a n t s were n o t applied to the ewes. All eight foster lambs treated with n e a t s f o o t oil were accepted within 24 h; seven i m m e d i a t e l y . There were few i m m e d i a t e acceptances with the o t h e r odorants, but f r o m t w o to five lambs o u t of groups of six were p e r m a n e n t l y fostered by 48 h. Only one foster lamb was accepted in the control group of 12 in which no o d o r a n t was used. Fostering was m o s t successful with n e a t s f o o t oil and w o o l wax, b o t h substances that originated f r o m r u m i n a n t skin. F o s t e r i n g was less successful in tests that o m i t t e d pre-exposure of the ewes to their o w n lambs treated with n e a t s f o o t oil, w o o l wax or vegetable oil. T o x i c i t y problems were e n c o u n t e r e d with ethanol solutions of m e r c a p t o e t h a n o l , m e t h y l salicylate, eucalyptus oil and n e a t s f o o t oil.

INTRODUCTION

Sheep producers and researchers into lactation and lamb growth are sometimes faced with the problem of fostering lambs on to ewes that are not their natural mothers (Alexander et al., 1985). The difficulties are due to development of specific recognition of the lamb by its m o t h e r within several hours of birth, coupled with the strong tendency for ewes to suckle their own lamb(s) exclusively (Lent, 1974). Lambs can be readily fostered soon after birth, before the ewe can distinguish her own lamb from aliens, but there are often practical reasons why fostering is not attempted until lambs are 1 or 2 days old.

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346 Lamb odour is the critical cue to the ewe's indentification of her offspring (Alexander and Stevens, 1981). Realizing this, farmers have traditionally attempted to foster lambs by anointing them, and sometimes the foster mother's nose also, with odoriferous substances ( " o d o r a n t s " ) such as kerosene (Lamond, 1949). Commercial firms have also marketed an aerosol smelling strongly of vanilla and a nasal spray of local anaesthetic t h a t were purported to facilitate fostering. However, no systematic study of these preparations, or of the use of odorants generally, has been published. In a previous study, we found that Merino ewes were still able to distinguish their own anaesthetized lambs from aliens when the lambs were anointed with one or other of a variety of odorants (Alexander and Stevens, 1982). Hence, it seemed to us to be unlikely that the simple use of odorants would facilitate fostering. Therefore, in a study of odorants that might be useful, an a t t e m p t was made to facilitate fostering by prior treatment o f the ewe's own lamb with an odorant that was also applied to the foster lamb. It was hoped that ewes would come to identify their lambs with the exogenous odour and would have difficulty in distinguishing between their own and foster lambs. However, some ewes were given odorant-treated foster lambs w i t h o u t prior exposure to the odorant. METHODS

Outline of procedure The study was done near Sydney in November 1983, with 85 sevenyear-old multiparous Merino ewes lambing on a 1-ha pasture and supplem e n t e d with oat-grain and lucerne hay. Most of the ewes bore single lambs. The ewes and their lambs were removed from the lambing paddock within 24 h of birth, and were placed in 1 X 1.5 m individual o u t d o o r pens under a canvas awning where they were offered water, approximately 750 g oatgrain and 1 kg lucerne hay dally. One to two days later, the animals were allotted to sets of 2 or 3 ewe and lamb pairs, with each ewe scheduled to become the foster mother of a lamb from another ewe in the same set. The sets were arranged after initial acceptance tests of the ewes with alien lambs, so t h a t no lamb was accepted by its scheduled foster mother. In the afternoon of the same day, the lambs in the same set were treated with a c o m m o n odorant and were left with their mothers until the following morning, by which time t h e y were 2--3 days old. Odorant was then re-applied to freshen the odour, and 1 h later the lambs were isolated for 1-2 h to promote behavioural interactions when the lambs were presented to the foster mothers. The ewes' behaviour towards the foster lambs was observed for several minutes at the time of introduction until the behavioural patterns became clear, and was again observed on the following two mornings immediately after a 1--2-h separation. The success

347 of the treatment was then assessed. Any lamb showing no sign of being accepted was removed for hand-rearing, returned to its m o t h e r who was tethered if unwilling to re-accept her lamb, or left with the tethered foster ewe. Where acceptance was partial, the ewe and lamb were left together w i t h o u t intervention for further daily tests. Most successfully-fostered ewes and lambs were placed in a 1-ha paddock with other ewes and lambs, and were re-tested for acceptance in a 5 × 5 m enclosure 3--12 days later. Lambs were weighed daily while in the fostering pens and again at the final acceptance test. The weight changes were used in conjunction with the behavioural tests, to assess the success of fostering. In addition, with three odorants, a few ewes were given odorant-treated foster lambs without prior treatment of their own lamb with the same odorant, to test whether the initial familiarization period facilitated fostering. Behavioural acceptance tests Acceptance of the foster lamb was indicated by behaviour when the lamb was returned to the ewe in the fostering pen after the period of separation. Ewes accepting the foster lambs bleated softly, showed close and sustained olfactory interest in the lamb, and readily suckled the lamb. Ewes rejecting the lamb bleated loudly, circled to avoid the lamb after a brief olfactory investigation, and sometimes made threatening gestures with the head, or butted the lamb. Partial acceptance was indicated by sustained olfactory interest and brief suckling, with the ewe occasionally moving to interrupt suckling while continuing to stiff at the lamb. Odorants and their application The choice of the nine odorants tested (Table 1) was arbitrary, but most were included in a previous study (Alexander and Stevens, 1982). Oily odorants were poured over the lamb and spread over the body with a gloved hand; alcohol-based odorants were applied through a hypodermic needle with the point bent to produce a diffuse spray. The initial and " t o u c h - u p " applications of oily odorants were about 250 and 120 ml, respectively, and of alcohol-based odorants 100 and 25 ml, respectively. Control lambs were treated with ethyl alcohol only. The concentrations of alcohol-diluted odorants were initially selected arbitrarily, but due to toxicity problems {Table III), some concentrations were reduced to the levels shown in Table I. Con trol group To minimize the possible number of rejected lambs, a c o m m o n control group was established for this and a concurrent experiment on "additive"

6

6 6 6

6 6 6 12

Undiluted

5% in ethanol 2.5% in ethanol 10% in ethanol

2.5% in ethanol 20% in ethanol 20% in ethanol 100% ethanol

Black and Gold Brand, Daftaw, Blacktown, Australia Fluka A.G., Buchs, S.G., Switzerland Ajax Chemicals Ltd., Sydney, Australia Sigma Chemical Co., St. Louis, U.S.A. The Sheldon Drug Co. Pty. Ltd., Sydney, Australia Hopkins and Williams Pty. Ltd., Essex, England Merck, W. Germany CSR Chemicals Ltd., Sydney, Australia

Vegetable oil (blended edible vegetable oil, poly-unsat., < 5 mg cholesterol/100 g)

Mercapto-ethanol (2-hydroxyethyl mercaptan, laboratory grade)

Oil of Wintergreen, laboratory grade (methyl salicylate)

Vanillin (4-hydroxy 3-methoxy benzaldehyde, laboratory grade)

Eucalyptus oil

Butyric acid (laboratory grade)

Propionic acid (A.R.)

Control, ethyl alcohol (laboratory grade)

(B.P.)

6

Undiluted

F.H. Faulding and Co. Ltd., Thebarton, Australia

Wool wax (wool fat, anhydrous B.P.)

Own lamb pre-treated with odorant

6

5

6

Own lamb not pre-treated with odorant

No. of ewes tested with:

8

Concentration tested (v]v)

Undiluted

Supplier

Davis Gelatine Organisation Neatsfoot oil (commercial inedible special grade, F F A 14.8%) Melbourne, Australia

Odorant

Odorants tested for facilitation of fostering

TABLE I

QO

C~

349

fostering (Alexander and Stevens, 1985}. In that experiment, untreated control lambs were exchanged between ewes and half were returned to their own mothers after 24 h while the other half remained as foster " t w i n " lambs with these same ewes. Consequently, control data were available for only the first 24 h of fostering.

Statistical comparisons Fisher's exact test was used for all statistical comparisons. RESULTS

Effect of odorant on acceptance of own lamb Application of wool wax and propionic acid caused initial rejection of own lamb by 6/7 and 3/6 ewes, respectively, but by the following morning only one wool-wax-treated lamb was still rejected by its dam (Table II); this ewe was removed from the experiment.

Acceptance o f odorant-treated foster lamb after 24 h familiarisation Acceptance of neatsfoot-treated foster lambs was exceptional; 7 of the 8 lambs were fully accepted immediately, and the other was also accepted by next morning. Almost all 48 foster lambs treated with the other odorants were first rejected by the foster mothers, but by the following morning 23 were being suckled, and a further five lambs of the 46 that were left with the foster ewes were accepted during the next 48 h (Table II). This pooled acceptance rate 24 h after presentation o f the foster lambs was higher than in the control group (23/48 v. 1/12, P = 0.02), b u t amongst the individual odorants other than neatsfoot soil, only the acceptance rate for wool-wax was significantly above that in the control group (5/6 v. 1/12, P = 0.004). Six ewes that accepted the foster lambs had their own odorant-treated lamb returned 24 h after the foster had been introduced; two had neatsfoottreated lambs, 2 had wool-wax-treated lambs, 1 had a butyric-acid-treated lamb and 1 had a propionic-acid-treated lamb. All continued to accept the foster lamb, while all but one with a wool-wax-treated lamb and the one with a propionic-acid-treated lamb also accepted their own lambs after return.

Acceptance of foster lamb after 3--12 days in the flock All lambs that had been accepted in the foster pens without operator intervention were still accepted by their foster mothers after 3--12 days in the flock of ewes and lambs. Of the 23 lambs whose natural mother

Yes No Yes No Yes No Yes Yes Yes Yes Yes Yes Yes

N e a t s f o o t oil

Wool w a x

V e g e t a b l e oil

Mercapto ethanol

B u t y r i c acid

P r o p i o n i c acid

Vanillin

E u c a l y p t u s oil

M e t h y l salicylate

Control

1--3

2

2

2

2

2

2--3 1--3

1--3 2

2--3 1--3

Age o f f o s t e r lamb at start of fostering (days) ~

12

6

6

6

6

6

6

6 6

62 5

8 6

No. o f ewes tested

12

6

6

6

6(3) 3

6

6

6 --

62(5)3 --

8 --

Own lamb after application of odorant

0

0

0

0

0

1

0

0 1

1 0

7 0

At exchange

Foster lamb

1

2

3

3

3

3

2

3 3

4 0

8 1

After 24 h

Number of lambs accepted

1 T i m e s since t h e ewes l a m b e d were similar t o t h e c o r r e s p o n d i n g ages of t h e f o s t e r l a m b s . = A n a d d i t i o n a l ewe p e r m a n e n t l y r e j e c t e d its l a m b ; e w e d i s c a r d e d f r o m e x p e r i m e n t . 3 No. o f o w n l a m b s t e m p o r a r i l y r e j e c t e d is s h o w n in p a r e n t h e s e s . 4 No. a c c e p t e d b y 7 2 h. s O w n lamb also present.

Pre-exposure to odorant

Odorant

Acceptance of lambs after treatment with odorants

T A B L E II

2s

2

3

3

3

4

3(4) 4

4 3

5 0

8 2

After 48 h

0/0

0/2

0/Z

0/2

0/2

0/4

O/2 0/0

2/4 0/0

3/6 0/0

Own lamb after 3--12 days in flock

¢j1

351

was also present in this flock, only five were accepted by the m o t h e r at the final test, and of these, three had been treated with neatsfoot oil and two with wool-wax.

Acceptance o f foster lamb without prior treatment o f own lamb with odorant Acceptances at 24 and 48 h by ewes not pre-exposed to the odorant on their own lambs were below those by ewes whose own lamb had been treated with odorant. The differences at 48 h were statistically significant for neatsfoot oil (2/6 v. 8/8, P = 0.015) and wool wax (0/5 v. 5/6, P = 0.013), although not for vegetable oil (3/6 v. 4/6).

Acceptance after intervention, 48 h after start o f fostering Sixteen lambs t h a t had not been accepted by the foster ewe within 48 h were returned to their own mothers, who had also rejected their foster lambs. Six of the lambs were accepted immediately, but the other 10 lambs were rejected. However, after tethering, five of the ewes re-accepted their own lamb within 48 h. Another 13 lambs that had n o t been accepted within 48 h were left with the tethered foster ewe; six were accepted within 24 h and another six within 48 h. The unaccepted lambs were able to obtain some milk from the tethered ewes, but were finally removed for handrearing.

Weight changes o f lambs Behavioural acceptance was associated with mean (+ SEM) weight gains by lambs of 210 + 30 g/day (range 150--559 g/day) while in the fostering TABLE III Formulations that resulted in lamb deaths Odorant

Concentration in Volume applied ethanol (%) (solution (ml) I or emulsion)

Proportion of lambs dying

Mercapto-ethanol

20

100

3/6

Methyl salicylate

12.5

100

4/4

Eucalyptus oil

Pure 50 10

200 100 100

1/1 4/4 2 1/1

Neatsfoot oil

33

250

2 2/2

i Most by spraying; neatsfoot oil by rubbing on with gloved hand. 2 Includes one lamb rendered unconscious but recovered.

352 pens, and 160 + 60 g/day in the field. Rejected lambs lost weight progressively.

Toxicity of odorants At the beginning of the experiments, application of high concentrations of mercaptoethanol, m e t h y l salicylate and eucalyptus oil in ethanol unexpectedly caused death or unconsciousness in lambs (Table III), and a similar effect of neatsfoot oil emulsified in ethanol was observed in a concurrent exploratory study. No autopsy or clinical examination of affected lambs was performed. DISCUSSION The results show that odorants can be used to facilitate fostering in sheep. Not only was one odorant, neatsfoot oil, highly successful (8/8 successes), but all the odorants tested gave somewhat higher acceptance rates than in the control animals, and the difference was significant when the results for the odorants other than neatsfoot oil were pooled. However, toxicity problems, encountered with some odorants applied in high concentration in alcohol, call for caution in selection of odorants, concentrations and vehicle. The toxicity was obviously due to absorption of odorant and/or vehicle via the skin, but the pathology was n o t investigated. The results also show that ewes can be trained to associate an exogenous odour with their own lamb, and therefore tend to confuse a foster with their own lamb treated with the same odorant. Since most of the ewes, other than those treated with neatsfoot oil, accepted their own lambs immediately after treatment with odorant, but rejected the treated alien lambs 24 h later, the o d o r a n t facilitation of fostering does n o t depend on the complete masking of the odour of own and/or foster lamb. However, the use of odorants appears to be about as effective as complete masking by washing (Alexander et al., 1983). Almost all ewes will ultimately accept alien lambs after 1 week or more if they are confined together with the ewe restrained to enable the foster lamb to suck (Hulet et al., 1979; Alexander and Bradley, 1985). Interference with the lamb's odour thus hastens the change in the odour m e m o r y of the ewe, and dispenses with the need for restraint in most ewes. In those n o t accepting lambs within 48 h, a period of 24--48 h restraint was usually effective. The results give credence to farmers' claims that odorant treatment facilitates fostering, but indicate that a high success rate could n o t be expected in the absence of training, at least in Merinos. The results with vanillin, the basis of a commercial aid to fostering, were no better than those with most of the other odorants tested. Although few additive fosterings were attempted, the results also indicate that a proportion of ewes

353

could be induced to accept an extra lamb by use of odorants and removal o f own lamb for 24 h or less. Amongst the nine odorants, the t w o most successful, neatsfoot oil and wool wax, gave results which suggested them to be in different classes from those of other odorants. Thus, most neatsfoot-treated foster lambs were immediately accepted by neatsfoot-"trained" ewes, while there were few acceptances with other odorants, and most wool-wax-treated lambs were immediately but temporarily rejected by their own ewes, while lambs treated with other odorants were mostly accepted. Both of these odorants have a composition that is likely to be related to that of lamb odour, since wool wax consists of secretions of sheep skin and the currently used Australian neatsfoot oil is derived from digestion of cattle skin (A. Whittet, Davis Gelatine Co., Australia, personal communication, 1983). Neatsfoot oil m a y contain many of the constituents that are involved with the ewe's recognition of her own lamb's odour, hence the acceptances, and wool wax m a y contain constituents that are involved with recognition of alien lambs, hence the rejections. Such constituents could be maternally derived if maternal labelling, reported to occur in goats (Gubernick, 1981), also occurs in sheep. In an unpublished study (G. Alexander, D. Stevens and L.R. Bradley, 1982), an inhibitory effect of wool wax on acceptance of own lamb has also been observed with other Merinos (3/8 accepted), but n o t in Corriedales (9/10 accepted). Indeed with these ewes, whose own lambs had not been pre-treated, both wool wax and neatsfoot treatment of alien lambs resulted in 7/10 immediate acceptances by Corriedale ewes, whereas only 1/8 Merino ewes accepted wool-wax-treated aliens. These breed differences are consistent with results of other studies that assign Merinos a low rank in ease of fostering (Alexander et al., 1985; Alexander and Bradley, 1985). Consequently, the use of odorants in some other breeds could be highly successful. ACKNOWLEDGEMENTS

The authors gratefully acknowledge the help of Messrs. Neil Hinks and Colin Mills of the CSIRO, Division of Animal Production, for help with selection of odorants. The assistance of Bill Dwyer, of the same Division, was invaluable in managing the sheep.

REFERENCES Alexander, G. and Bradley, L.R., 1985. Fostering in sheep. IV. Use of restraint. Appl. Anita. Behav. Sci., 14: in press. Alexander, G. and Stevens, D., 1981. Recognition of washed lambs by Merino ewes. Appl. Anim. Ethol., 7: 77--86. Alexander, G. and Stevens, D., 1982. Failure to mask lamb odour with odoriferous substances. Appl. Anim. Ethol., 8: 253--260.

354 Alexander, G. and Stevens, D., 1985. Fostering in sheep. H. Use of hessian coats to foster an additional lamb on to ewes with single lambs. Appl. Anita. Behav. Sci., 14: in press. Alexander, G., Stevens, D. and Bradley, L.R., 1983. Washing lambs and confinement as aids to fostering. Appl. Anita. Ethol., 10: 251--261. Alexander, G., Stevens, D. and Bradley, L.D., 1985. Fostering in sheep. I. Facilitation by use of textile lamb coats. Appl. Anita. Behav. Sci., 14: in press. Gubernick, D.J., 1981. Parent and infant attachment in mammals. In: D.J. Gubernick and P.H. Klopfer (Editors), Parental Care in Mammals. Plenum Press, New York, pp. 243--305. Hulet, C.V., Dahmen, J.J., Shupe, W.L. and Doren, E., 1979. How to Graft Lambs. Current Information Series, No. 469, University of Idaho, College of Agriculture. Lamond, H.G., 1949. Mothering a lamb. Sheep Goat Raiser, San Angelo, TX, 29(9): 36--38. Lent, P.C., 1974. Mother--infant relationships in ungulates. In: V. Geist and F. Walther (Editors), The Behaviour of Ungulates and its Relation to Management. International Union for Conservation of Nature, Morges, Switzerland, pp. 14--55.