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The effect of planes of nutrition on growth and attainment of puberty in female wild boars raised in captivity
Animal Reproduction Science, 20 (1989) 71-77 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands
71
Short Communication
T h e E f f e c t of P l a n e s of N u t r i t i o n on G r o w t h and A t t a i n m e n t of P u b e r t y in F e m a l e Wild B o a r s R a i s e d in C a p t i v i t y D. PI~PIN1 and R. MAUGET ~ lInstitut de Recherche sur les Grands MammifSres, Institut National de la Recherche Agronomique, C.R.A. Toulouse, B.P. 27, 31326 Castanet Tolosan Cedex (France) 2Centre d'Etudes Biologiques des Animaux Sauvages, Centre National de la Recherche Scientifique, 79360 Beauvoir-sur-Niort (France)
(Accepted 9 January 1989)
ABSTRACT P~pin, D. and Mauget, R., 1989. The effect of planes of nutrition on growth and attainment of puberty in female wild boars raised in captivity. Anim. Reprod. Sci., 20" 71-77. Growth of wild boar females raised in captivity and fed with various amounts of the same diet was investigated from the age of 8-10 weeks until puberty. The spontaneous food intake of females fed ad libitum increased during autumn and decreased in winter. One-year-old animals weighed about 35 kg (vs only 26 kg for those having a restricted diet from the beginning of housing), and reached puberty at 21 months of age, with a body weight ranging between 50 and 59 kg. Restricted food intake throughout the growing period of the young, followed by an ad libitum diet, had drastic consequences on the weight at puberty (mean of 39 kg), but did not delay the onset of puberty. On the contrary, a short period of food restriction after the growing period of the young had no effect on weight at puberty, but led to precocious puberty. Females which received a very limited food supply showed delayed puberty and reduced body development.
INTRODUCTION O1off (1951) r e p o r t s t h a t , w h e n good o a k or b e e c h m a s t is available, t h e r a t e of r e p r o d u c t i o n o f f e m a l e wild b o a r ( S u s scrofa L.) i n c r e a s e s a n d t h a t m a n y y o u n g a n i m a l s m a y b r e e d for t h e f i r s t t i m e a t 8 - 1 0 m o n t h s o f age. T h i s is n o t so w h e n m a s t is poor. S i m i l a r o b s e r v a t i o n s w e r e m a d e b y M a t s c h k e (1964) w h o s p e a k s o f t h e " f l u s h i n g e f f e c t " o f food, as r e p o r t e d b y S o r e n s e n et al. (1961) for t h e d o m e s t i c sow. C o n s e q u e n t l y in wild b o a r , a f o o d excess or defic i e n c y i n d u c e s large v a r i a t i o n s in b o d y d e v e l o p m e n t , in t i m i n g o f t h e a n o e s t r u s - o e s t r u s t r a n s i t i o n in a u t u m n , or in age a t first o e s t r u s ( A c k e r k n e c h t , 1950; Asdell, 1964; B r i e d e r m a n n , 1971; Kozlo, 1975; S t u b b e a n d S t u b b e , 1977; M a u -
0378-4320/89/$03.50
© 1989 Elsevier Science Publishers B.V.
72 get, 1980; Auma~tre et al., 1984; Klein, 1984; Pdpin et al., 1987). However, while the domestic sow is continuously fertile, with some monthly fluctuations (Martinat-Bottd et al., 1981, 1984), the wild boar shows seasonal sexuality, independently of the availability of food (Mauget, 1980). Knowledge of the relationships between food, growth and reproduction in the wild boar is important for assessing the regulation of population dynamics, but it appears very difficult to study such relationships in the wild (Pdpin et al., 1987). Although some effects of confinement on the physiology of the animals may be suspected (Prunier and Etienne, 1984), the present study is based on observations collected with 8-10-week-old females kept in captivity. In order to complete a previous work presented elsewhere (Mauget and Pdpin, 1985), the aim of this study was to compare the effects on growth and age at sexual maturity of four experimental feeding patterns, simulating natural annual variations in food availability. MATERIALAND METHODS Young females, 8-10 weeks old, were captured in the Chizd Forest National Reservation Area (midwestern France) during June-July. The age of each animal was estimated using the tooth eruption schedule given by Matschke ( 1967 ). The animals were housed in pairs in 1.5 × 3.5 m pens in a farm building open to the east, under natural photoperiod conditions. They were fed together with a 15% crude protein diet in variable amounts and with water ad libitum. The following experimental feeding patterns were applied: (a) Group i (n -- 5 ), ad libitum (ideal natural conditions); (b) Group 2 (n--4), ad libitum during the first year, then restricted food supply (600 g/animal) from July to March to simulate extremely unfavourable conditions, usually observed from summer to the end of winter in the wild, and 900 g/individual from April until puberty, in order to restore m i n i m u m growth; (c) Group 3 (n-- 4) ad libitum during the first year, restricted food supply (600 g/individual) from mid-July to midOctober, and thereafter ad libitum again as in conditions in the wild; (d) Group 4 (n = 3), restricted food supply, adjusted monthly to about 60% of the spontaneous intake of ad-libitum-fed animals, from the beginning of housing until October of the second year (in order to keep constant the relative restriction), then ad libitum. All animals were weighed regularly, at least monthly. For females fed ad libitum, spontaneous food intake was measured by daily weighing, pen by pen. As the behavioural tests to detect oestrus in domestic pigs are not suitable for the female wild boar, ovarian activity was studied by radioimmunoassay evaluation of plasma progesterone concentration using RIA kits (Biomerieux, France; validation tests were previously performed for wild boar plasma Mauget, 1980). Blood samples were taken weekly by radial venipuncture. Cyclic activity was established when plasma progesterone increased above the baseline value (1 n g / m l ) in two consecutive samples, of which at least one was
73 above 5 ng/ml (validation by Mauget, 1980). Statistical significance of average values ( _+s.e.m. ) was tested with ANOVA; differences in the onset of puberty between groups were tested with the Mann-Whitney U test. RESULTS A seasonal change in spontaneous food intake was observed during the first year in females fed ad libitum, a minimum level occurring in August-September (74.9 ___4.6 g/day kg -°'75) followed by a significant increase in OctoberNovember (102.3 + 5.5 g/day kg- o.75); p < 0.01 ). During the second year, females fed continuously ad libitum (Group 1) exhibited a similar autumnal increase (95.3 _+4.2 g/day kg -°'75 in October vs 77.2 + 4.2 g/day kg -°'75 in August; P < 0 . 0 1 ) . In seasonally and long restricted animals (Groups 3 and 4) restoration of free feeding in October induced a sharp rise of food intake (from 41.6 to 104.0 + 3.5 g/day kg -°75 in October-November). The natural or imposed changes in food intake were correlated with changes in body weight. At the beginning of housing, the mean body weight of animals was 9.0 + 0.4 kg, without any significant differences between the four groups (P > 0.05). During the first year, the growth variation of females fed ad libitum followed a sigmoid curve which characterizes the dynamics of development of the young. At 1 year of age, there was no significant difference in their body mass ( m e a n = 3 5 . 5 + 0 . 8 kg). Females with a restricted diet weighed only 26.0 + 1.8 kg (P < 0.01 ). In the second year, females fed ad libitum (Group 1) exhibited a new growth period from the end of summer to the beginning of autumn. This stage of faster growth was suppressed in food-limited females of Group 2 and delayed for 2 months in summer food-restricted females of Groups 3 and 4. Data concerning age and weight at puberty of individual females are shown in Table 1. All females of Group 1 reached puberty synchronously at the beginning of February, i.e. at 21 months of age, with a body mass ranging between 50 and 59 kg. For the females fed with limited food from 14 months (Group 2), puberty was delayed (23 to 34 months of age, Mann-Whitney U test; U--0; P < 0.05 ), but their weight at puberty (39-50 kg) was not significantly lowered ( P > 0.05 ). Whereas a restricted feeding period in summer (Group 3) had no significant effect on weight at puberty ( P > 0.05), these animals were a little more precocious (puberty in mid-January, i.e. about 3 weeks earlier than females of Group 1; U= 0; P < 0.05). A long period of food restriction during the growing period of the young females (from 2 to 16 months, Group 4), followed later on by an ad libitum diet, did not delay the onset of puberty but had major consequences for their weight at puberty ( m e a n = 38.7 ___1.8 kg, see Table 1, P<0.01).
74 TABLE 1 Age and body weight at puberty of female wild boars at different planes of feeding Attainment of puberty Feeding planes
Age (month)
Body weight (kg) individual
mean
(±s.e.m.) Always ad lib±turn Ad libitum until 14 months old, then restricted food Ad lib±turn, except between 14 and 16 months old Restricted food until 16 months old, then ad lib±turn
21, 21, 21, 21, 21
50, 50, 52, 55, 59
53.2 ± 1.7
23, 25, 34
39, 49, 50
46.0 + 3.5
20, 20, 20, 20
46, 50, 55, 57
52.0 ± 2.5
21, 21, 21
36, 38, 42
38.7 ± 1.8
DISCUSSION
As reviewed by Kirkwood and Aherne (1985), a m i n i m u m threshold value for body weight seems to be necessary for the onset of puberty in the pig. In our study, the observed m i n i m u m weight at puberty was about 35 kg for restricted females (Group 4). This value is in good agreement with previous data from the wild (AumaRre et al., 1982), However, a m i n i m u m body development alone does not seem to be sufficient to induce puberty in wild boar. In our farming context, females fed ad libitum reached 35 kg in May-June, i.e. when the adults begin anoestrus (Mauget, 1982). In natural conditions, the renewal of ovarian activity in adult females depends on autumnal food resources (AumMtre et al., 1984) and could be correlated with an increase of body weight (Jezierski and Myrcha, 1975; Stubbe and Stubbe, 1977). In the present study, prepubertal females fed ad lib±turn exhibited an increase of body weight, but only before the end of the anoestrus period (in September-October). We delayed the period of body weight increase in females of Group 3 experimentally, and the onset of puberty was slightly earlier t h a n for females always fed ad libitum; however, puberty was not observed before January. In long restricted animals (2nd to 16th months), an autumnal increase i n food availability is enough to induce puberty at the same age as ad lib±rum females. These last two situations observed in captivity are reminiscent of the flushing effect described by Matschke (1964) in the wild. Therefore, autumnal variations of food availability, essentially characterized by fat storage in adults (Mauget et al., 1988), seem to be directly correlated with the beginning of sexual maturity of young females.
75
In the domestic sow, many studies concern the problem of onset of puberty, and results are often contradictory (review by Hughes, 1982; Kirkwood and Aherne, 1985). If young sows are subjected to major food deprivation just before puberty, their body development is slowed down and their first oestrus is delayed (Duncan and Lodge, 1960, in Sadleir, 1969; Zimmermann et al., 1960; Du~e and Etienne, 1974; Friend et al., 1981; Etienne et al., 1983). Den Hartog and Noordewier (1984) and Prunier et al. (1987) considered that age plays a predominant role. The effect of photoperiod is also debated: Prunier et al. (1987) consider photoperiod to have no effect, whereas Scanlon and Krishnamurthy (1974) and Mavrogenis and Robison (1976) noted earlier puberty for animals born in autumn. Some photoperiod experiments have been caried out, but they were not conclusive (Dufour and Bernard, 1968; Hacker et al., 1979). Such apparent contradictions show that many parameters are involved in the determination of onset of puberty in the domestic sow, including external and internal factors. In the case of wild boar, the seasonal pattern of reproduction represents an additional constraint to sexual maturation of young females, as demonstrated in other seasonal breeders, for instance the ewe, where sexual maturation of slowly growing lambs may be masked by transition to seasonal anoestrus (Foster and Yellon, 1985; Foster et al., 1985, 1988). ACKNOWLEDGEMENTS
Financial support was provided by the Institut National de la Recherche Agronomique (National Institu~ of Agronomic Research). We thank I, Pignot for technical assistance, Dr. A. Prunier for helpful comments on the manuscript, and Dr. R. Campan for checking the language.
REFERENCES Ackerknecht, E., 1950. Anatomische Unterschied zwischen Wild Schwein und Hauss Schwein. Z. Tierz. Zfichtungsbiol., 58: 465-472. Asdell, S.A., 1964. Patterns of Mammalian Reproduction. Cornell Univ. Press, New York, NY, 670 pp. Aumaltre, A., Morvan, C., Qudrd, J.P., Peiniau, J. and Valet, G., 1982. Productivitd potentielle et reproduction hivernale chez la laie (Sus scrofa scrofa) en milieu sauvage. Journ. Rech. Porcine France, 14: 109-124. Aumaltre, A., Qudrd, J.P. and Peiniau, J., 1984. Influence du milieu sur la reproduction hivernale et la prolificitd de la laie. In: F. Spitz and D. Pdpin (Editors), Symposium International sur le Sanglier. Colloq. INRA, 22: 69-78. Briedermann, L., 1971. Zur Reproduktion des Schwarzwildes in der D.D.R. Tagungsber. Dtsch. Akad. Landwirtschaftswiss. Berlin, 113: 169-186. Den Hartog, L.A. and Noordewier, G.J., 1984. The effect of energy intake on age at puberty in gilts. Neth. J. Agric. Sci., 32: 263-280. Dude, P.H. and Etienne, M., 1974. Influence de l'alimentation pendant la croissance de la truie
76 sur la maturit~ sexuelle et les performances de reproduction: r~sultats pr~liminaires. Journ. Rech. Porcine France, I.N.R.A., I.T.P., Paris, pp. 43-47. Dufour, J. and Bernard, C., 1968. Effect of light on the development of market pigs and breeding gilts. Can. J. Anita. Sci., 48: 425-430. Etienne, M., Camous, S. and Cuvillier, A., 1983. Effets de restrictions alimentaires pendant la croissance des truies sur leur maturit~ sexuelle et leur reproduction ult~rieure. Reprod. Nutr. D~v., 23: 309-319. Foster, D.L. and Yellon, S.M., 1985. Photoperiodic time measurement is maintained in undernourished lambs with delayed puberty. J. Reprod. Fertil., 75: 203-208. Foster, D.L., Yellon, S.M. and Olster, D.H., 1985. Internal and external determinants of the timing of puberty in the female. J. Reprod. Fertil., 75: 327-344. Foster, D.L., Ebling, J.P. and Claypool, L.E., 1988. Timing of puberty by photoperiod. Reprod. Nutr. D~v., 28(2B): 345-364. Friend, D.W., Lodge, G.A. and Elliot, J.I., 1981. Effects of energy and dry matter intake on age, body weight and backfat at puberty and on embryo mortality in gilts. J. Anita. Sci., 53: 118124. Hacker, R.R., King, G.J., Ntunde, B.N. and Narendran, R., 1979. Plasma oestrogen, progesterone and other reproductive responses of gilts to photoperiod. J. Reprod. Fertil., 57: 447-451. Hughes, P.E., 1982. Factors affecting the natural attainment of puberty in the gilt. In: D.J.A. Cole and G.R. Foxcroft (Editors), Control of Pig Reproduction. Butterworths, London, pp. 117138. Jezierski, W. and Myrcha, A., 1975. Food requirements of a wild boar population. Pol. Ecol. Stud., 1: 61-83. Kirkwood, R.N. and Aherne, F.X., 1985. Energy intake, body composition and reproductive performanceof the gilt. J. Anim. Sci., 60: 1518-1529. Klein, F., 1984. Contribution ~ l'6tude de la croissance du sanglier (Sus scro[a) par capture et recapture. In: F. Spitz and D. P~pin (Editors), Symposium International sur le Sanglier. Colloq. INRA, 22: 55-67. Kozlo, P.G., 1975. The Wild Boar. Uradzhaj, Minsk, pp. 1-224 (in Russian). Martinat-Bott~, F., Dando, P., Gautier, J. and Terqui, M., 1981. Variation saisonni&re de la taille de la pottle en relation avec celles du taux d'ovulation et de la mortalit~ embryonnaire chez la truie. Journ. Rech. Porcine France, 13: 269-276. Martinat-Bott~, F., Dagorn, J., Terqui, M. and Dando, P., 1984. Effect of confinement, climatic conditions and litter parity on the seasonal variations of the fertility rate and prolificacy. Ann. Rech. Vet., 15: 165-172. Matschke, G.H., 1964. The influence of oak mast on European wild hog reproduction. Trans. Annu. Conf. S.E. Assoc. Game Fish Comm., 18: 35-39. Matschke, G.H., 1967. Aging European wild hogs by dentition. J. Wildl. Manage., 31: 109-113. Mauget, R., 1980. R~gulations ~cologiques, comportementales et physiologiques (fonction de reproduction) de l'adaptation du sanglier au milieu. Th~se Doct. Etat, Univ. Tours, 299 pp. Mauget, R., 1982. Seasonality of reproduction in the wild boar. In: D.J.A. Cole and G.R. Foxcroft (Editors), Control of Pig Reproduction. Butterworths, London, pp. 509-526. Mauget, R. and P~pin, D., 1985. La pubert~ chez le sanglier: ~tude pr61iminaire du rSle de l'alimentation. In: S. de Combrudge (Editor), XVIIth Congr. Int. Union Game Biol. Ministery of Agriculture, Agricultural Research Administration, Brussels 1985, pp. 191-197. Mauget, R., Auma~tre, A. and Peignier, Y., 1988. Caract~risation de l'~tat trophique du sanglier, en milieu forestier, ~ partir du gras m6sent~rique et des param~tres sanguins. Reprod. Nutr. D~v., 28: 969-978. Mavrogenis, A.P. and Robison, O.W., 1976. Factors affecting puberty in swine. J. Anim. Sci., 42: 1251-1255. Oloff, H.B., 1951. Zur Biologie und ()kologie des Wildschweines. Beitr. Tierz., 2: 1-95.
77 PSpin, D., Spitz, F., Janeau, G. and Valet, G., 1987. Dynamics of reproduction and development of weight in the wild boar (Sus scrofa) in South-west France. Z. S~iugetierkd., 52: 21-30. Prunier, A. and Etienne, M., 1984. Effects of confinement on attainment of puberty in gilts. Ann. Rech. V~t., 15: 155-164. Prunier, A., Bonneau, M. and Etienne, M., 1987. Effects of age and live weight on the sexual development of gilts and boars fed two planes of nutrition. Reprod. Nutr. D~v., 27: 689-700. Sadleir, R..M.S., 1969. The Ecology of Reproduction in Wild and Domestic Animals. Methuen, London, 321 pp. Scanlon, P.F. and Krishnamurthy, S., 1974. Puberty attainment in slaughter-weight gilts in relation to month examined. J. Anita. Sci., 39:160 (abstr. 97). Sorensen, A.M., Jr., Thomas, W.B. and Gosset, J.W., 1961. A further study of the influence of level of energy intake and season on reproductive performance of gilts. J. Anim. Sci., 20: 347349. Stubbe, W. and Stubbe, M., 1977. Vergleichende Beitrage zur Reproduktions und Geburtsbiologie von Wild und Hausschwein Sus scrofa. Jagd Wildforsch., 10: 153-179. Zimmermann, D.R., Spies, H.G., Rigor, E.M., Self, H.L. and Casida, L.E., 1960. Effect of restricted feeding, cross breeding and season of birth on age at puberty in swine. J. Anim. Sci., 19: 687-694.
71
Short Communication
T h e E f f e c t of P l a n e s of N u t r i t i o n on G r o w t h and A t t a i n m e n t of P u b e r t y in F e m a l e Wild B o a r s R a i s e d in C a p t i v i t y D. PI~PIN1 and R. MAUGET ~ lInstitut de Recherche sur les Grands MammifSres, Institut National de la Recherche Agronomique, C.R.A. Toulouse, B.P. 27, 31326 Castanet Tolosan Cedex (France) 2Centre d'Etudes Biologiques des Animaux Sauvages, Centre National de la Recherche Scientifique, 79360 Beauvoir-sur-Niort (France)
(Accepted 9 January 1989)
ABSTRACT P~pin, D. and Mauget, R., 1989. The effect of planes of nutrition on growth and attainment of puberty in female wild boars raised in captivity. Anim. Reprod. Sci., 20" 71-77. Growth of wild boar females raised in captivity and fed with various amounts of the same diet was investigated from the age of 8-10 weeks until puberty. The spontaneous food intake of females fed ad libitum increased during autumn and decreased in winter. One-year-old animals weighed about 35 kg (vs only 26 kg for those having a restricted diet from the beginning of housing), and reached puberty at 21 months of age, with a body weight ranging between 50 and 59 kg. Restricted food intake throughout the growing period of the young, followed by an ad libitum diet, had drastic consequences on the weight at puberty (mean of 39 kg), but did not delay the onset of puberty. On the contrary, a short period of food restriction after the growing period of the young had no effect on weight at puberty, but led to precocious puberty. Females which received a very limited food supply showed delayed puberty and reduced body development.
INTRODUCTION O1off (1951) r e p o r t s t h a t , w h e n good o a k or b e e c h m a s t is available, t h e r a t e of r e p r o d u c t i o n o f f e m a l e wild b o a r ( S u s scrofa L.) i n c r e a s e s a n d t h a t m a n y y o u n g a n i m a l s m a y b r e e d for t h e f i r s t t i m e a t 8 - 1 0 m o n t h s o f age. T h i s is n o t so w h e n m a s t is poor. S i m i l a r o b s e r v a t i o n s w e r e m a d e b y M a t s c h k e (1964) w h o s p e a k s o f t h e " f l u s h i n g e f f e c t " o f food, as r e p o r t e d b y S o r e n s e n et al. (1961) for t h e d o m e s t i c sow. C o n s e q u e n t l y in wild b o a r , a f o o d excess or defic i e n c y i n d u c e s large v a r i a t i o n s in b o d y d e v e l o p m e n t , in t i m i n g o f t h e a n o e s t r u s - o e s t r u s t r a n s i t i o n in a u t u m n , or in age a t first o e s t r u s ( A c k e r k n e c h t , 1950; Asdell, 1964; B r i e d e r m a n n , 1971; Kozlo, 1975; S t u b b e a n d S t u b b e , 1977; M a u -
0378-4320/89/$03.50
© 1989 Elsevier Science Publishers B.V.
72 get, 1980; Auma~tre et al., 1984; Klein, 1984; Pdpin et al., 1987). However, while the domestic sow is continuously fertile, with some monthly fluctuations (Martinat-Bottd et al., 1981, 1984), the wild boar shows seasonal sexuality, independently of the availability of food (Mauget, 1980). Knowledge of the relationships between food, growth and reproduction in the wild boar is important for assessing the regulation of population dynamics, but it appears very difficult to study such relationships in the wild (Pdpin et al., 1987). Although some effects of confinement on the physiology of the animals may be suspected (Prunier and Etienne, 1984), the present study is based on observations collected with 8-10-week-old females kept in captivity. In order to complete a previous work presented elsewhere (Mauget and Pdpin, 1985), the aim of this study was to compare the effects on growth and age at sexual maturity of four experimental feeding patterns, simulating natural annual variations in food availability. MATERIALAND METHODS Young females, 8-10 weeks old, were captured in the Chizd Forest National Reservation Area (midwestern France) during June-July. The age of each animal was estimated using the tooth eruption schedule given by Matschke ( 1967 ). The animals were housed in pairs in 1.5 × 3.5 m pens in a farm building open to the east, under natural photoperiod conditions. They were fed together with a 15% crude protein diet in variable amounts and with water ad libitum. The following experimental feeding patterns were applied: (a) Group i (n -- 5 ), ad libitum (ideal natural conditions); (b) Group 2 (n--4), ad libitum during the first year, then restricted food supply (600 g/animal) from July to March to simulate extremely unfavourable conditions, usually observed from summer to the end of winter in the wild, and 900 g/individual from April until puberty, in order to restore m i n i m u m growth; (c) Group 3 (n-- 4) ad libitum during the first year, restricted food supply (600 g/individual) from mid-July to midOctober, and thereafter ad libitum again as in conditions in the wild; (d) Group 4 (n = 3), restricted food supply, adjusted monthly to about 60% of the spontaneous intake of ad-libitum-fed animals, from the beginning of housing until October of the second year (in order to keep constant the relative restriction), then ad libitum. All animals were weighed regularly, at least monthly. For females fed ad libitum, spontaneous food intake was measured by daily weighing, pen by pen. As the behavioural tests to detect oestrus in domestic pigs are not suitable for the female wild boar, ovarian activity was studied by radioimmunoassay evaluation of plasma progesterone concentration using RIA kits (Biomerieux, France; validation tests were previously performed for wild boar plasma Mauget, 1980). Blood samples were taken weekly by radial venipuncture. Cyclic activity was established when plasma progesterone increased above the baseline value (1 n g / m l ) in two consecutive samples, of which at least one was
73 above 5 ng/ml (validation by Mauget, 1980). Statistical significance of average values ( _+s.e.m. ) was tested with ANOVA; differences in the onset of puberty between groups were tested with the Mann-Whitney U test. RESULTS A seasonal change in spontaneous food intake was observed during the first year in females fed ad libitum, a minimum level occurring in August-September (74.9 ___4.6 g/day kg -°'75) followed by a significant increase in OctoberNovember (102.3 + 5.5 g/day kg- o.75); p < 0.01 ). During the second year, females fed continuously ad libitum (Group 1) exhibited a similar autumnal increase (95.3 _+4.2 g/day kg -°'75 in October vs 77.2 + 4.2 g/day kg -°'75 in August; P < 0 . 0 1 ) . In seasonally and long restricted animals (Groups 3 and 4) restoration of free feeding in October induced a sharp rise of food intake (from 41.6 to 104.0 + 3.5 g/day kg -°75 in October-November). The natural or imposed changes in food intake were correlated with changes in body weight. At the beginning of housing, the mean body weight of animals was 9.0 + 0.4 kg, without any significant differences between the four groups (P > 0.05). During the first year, the growth variation of females fed ad libitum followed a sigmoid curve which characterizes the dynamics of development of the young. At 1 year of age, there was no significant difference in their body mass ( m e a n = 3 5 . 5 + 0 . 8 kg). Females with a restricted diet weighed only 26.0 + 1.8 kg (P < 0.01 ). In the second year, females fed ad libitum (Group 1) exhibited a new growth period from the end of summer to the beginning of autumn. This stage of faster growth was suppressed in food-limited females of Group 2 and delayed for 2 months in summer food-restricted females of Groups 3 and 4. Data concerning age and weight at puberty of individual females are shown in Table 1. All females of Group 1 reached puberty synchronously at the beginning of February, i.e. at 21 months of age, with a body mass ranging between 50 and 59 kg. For the females fed with limited food from 14 months (Group 2), puberty was delayed (23 to 34 months of age, Mann-Whitney U test; U--0; P < 0.05 ), but their weight at puberty (39-50 kg) was not significantly lowered ( P > 0.05 ). Whereas a restricted feeding period in summer (Group 3) had no significant effect on weight at puberty ( P > 0.05), these animals were a little more precocious (puberty in mid-January, i.e. about 3 weeks earlier than females of Group 1; U= 0; P < 0.05). A long period of food restriction during the growing period of the young females (from 2 to 16 months, Group 4), followed later on by an ad libitum diet, did not delay the onset of puberty but had major consequences for their weight at puberty ( m e a n = 38.7 ___1.8 kg, see Table 1, P<0.01).
74 TABLE 1 Age and body weight at puberty of female wild boars at different planes of feeding Attainment of puberty Feeding planes
Age (month)
Body weight (kg) individual
mean
(±s.e.m.) Always ad lib±turn Ad libitum until 14 months old, then restricted food Ad lib±turn, except between 14 and 16 months old Restricted food until 16 months old, then ad lib±turn
21, 21, 21, 21, 21
50, 50, 52, 55, 59
53.2 ± 1.7
23, 25, 34
39, 49, 50
46.0 + 3.5
20, 20, 20, 20
46, 50, 55, 57
52.0 ± 2.5
21, 21, 21
36, 38, 42
38.7 ± 1.8
DISCUSSION
As reviewed by Kirkwood and Aherne (1985), a m i n i m u m threshold value for body weight seems to be necessary for the onset of puberty in the pig. In our study, the observed m i n i m u m weight at puberty was about 35 kg for restricted females (Group 4). This value is in good agreement with previous data from the wild (AumaRre et al., 1982), However, a m i n i m u m body development alone does not seem to be sufficient to induce puberty in wild boar. In our farming context, females fed ad libitum reached 35 kg in May-June, i.e. when the adults begin anoestrus (Mauget, 1982). In natural conditions, the renewal of ovarian activity in adult females depends on autumnal food resources (AumMtre et al., 1984) and could be correlated with an increase of body weight (Jezierski and Myrcha, 1975; Stubbe and Stubbe, 1977). In the present study, prepubertal females fed ad lib±turn exhibited an increase of body weight, but only before the end of the anoestrus period (in September-October). We delayed the period of body weight increase in females of Group 3 experimentally, and the onset of puberty was slightly earlier t h a n for females always fed ad libitum; however, puberty was not observed before January. In long restricted animals (2nd to 16th months), an autumnal increase i n food availability is enough to induce puberty at the same age as ad lib±rum females. These last two situations observed in captivity are reminiscent of the flushing effect described by Matschke (1964) in the wild. Therefore, autumnal variations of food availability, essentially characterized by fat storage in adults (Mauget et al., 1988), seem to be directly correlated with the beginning of sexual maturity of young females.
75
In the domestic sow, many studies concern the problem of onset of puberty, and results are often contradictory (review by Hughes, 1982; Kirkwood and Aherne, 1985). If young sows are subjected to major food deprivation just before puberty, their body development is slowed down and their first oestrus is delayed (Duncan and Lodge, 1960, in Sadleir, 1969; Zimmermann et al., 1960; Du~e and Etienne, 1974; Friend et al., 1981; Etienne et al., 1983). Den Hartog and Noordewier (1984) and Prunier et al. (1987) considered that age plays a predominant role. The effect of photoperiod is also debated: Prunier et al. (1987) consider photoperiod to have no effect, whereas Scanlon and Krishnamurthy (1974) and Mavrogenis and Robison (1976) noted earlier puberty for animals born in autumn. Some photoperiod experiments have been caried out, but they were not conclusive (Dufour and Bernard, 1968; Hacker et al., 1979). Such apparent contradictions show that many parameters are involved in the determination of onset of puberty in the domestic sow, including external and internal factors. In the case of wild boar, the seasonal pattern of reproduction represents an additional constraint to sexual maturation of young females, as demonstrated in other seasonal breeders, for instance the ewe, where sexual maturation of slowly growing lambs may be masked by transition to seasonal anoestrus (Foster and Yellon, 1985; Foster et al., 1985, 1988). ACKNOWLEDGEMENTS
Financial support was provided by the Institut National de la Recherche Agronomique (National Institu~ of Agronomic Research). We thank I, Pignot for technical assistance, Dr. A. Prunier for helpful comments on the manuscript, and Dr. R. Campan for checking the language.
REFERENCES Ackerknecht, E., 1950. Anatomische Unterschied zwischen Wild Schwein und Hauss Schwein. Z. Tierz. Zfichtungsbiol., 58: 465-472. Asdell, S.A., 1964. Patterns of Mammalian Reproduction. Cornell Univ. Press, New York, NY, 670 pp. Aumaltre, A., Morvan, C., Qudrd, J.P., Peiniau, J. and Valet, G., 1982. Productivitd potentielle et reproduction hivernale chez la laie (Sus scrofa scrofa) en milieu sauvage. Journ. Rech. Porcine France, 14: 109-124. Aumaltre, A., Qudrd, J.P. and Peiniau, J., 1984. Influence du milieu sur la reproduction hivernale et la prolificitd de la laie. In: F. Spitz and D. Pdpin (Editors), Symposium International sur le Sanglier. Colloq. INRA, 22: 69-78. Briedermann, L., 1971. Zur Reproduktion des Schwarzwildes in der D.D.R. Tagungsber. Dtsch. Akad. Landwirtschaftswiss. Berlin, 113: 169-186. Den Hartog, L.A. and Noordewier, G.J., 1984. The effect of energy intake on age at puberty in gilts. Neth. J. Agric. Sci., 32: 263-280. Dude, P.H. and Etienne, M., 1974. Influence de l'alimentation pendant la croissance de la truie
76 sur la maturit~ sexuelle et les performances de reproduction: r~sultats pr~liminaires. Journ. Rech. Porcine France, I.N.R.A., I.T.P., Paris, pp. 43-47. Dufour, J. and Bernard, C., 1968. Effect of light on the development of market pigs and breeding gilts. Can. J. Anita. Sci., 48: 425-430. Etienne, M., Camous, S. and Cuvillier, A., 1983. Effets de restrictions alimentaires pendant la croissance des truies sur leur maturit~ sexuelle et leur reproduction ult~rieure. Reprod. Nutr. D~v., 23: 309-319. Foster, D.L. and Yellon, S.M., 1985. Photoperiodic time measurement is maintained in undernourished lambs with delayed puberty. J. Reprod. Fertil., 75: 203-208. Foster, D.L., Yellon, S.M. and Olster, D.H., 1985. Internal and external determinants of the timing of puberty in the female. J. Reprod. Fertil., 75: 327-344. Foster, D.L., Ebling, J.P. and Claypool, L.E., 1988. Timing of puberty by photoperiod. Reprod. Nutr. D~v., 28(2B): 345-364. Friend, D.W., Lodge, G.A. and Elliot, J.I., 1981. Effects of energy and dry matter intake on age, body weight and backfat at puberty and on embryo mortality in gilts. J. Anita. Sci., 53: 118124. Hacker, R.R., King, G.J., Ntunde, B.N. and Narendran, R., 1979. Plasma oestrogen, progesterone and other reproductive responses of gilts to photoperiod. J. Reprod. Fertil., 57: 447-451. Hughes, P.E., 1982. Factors affecting the natural attainment of puberty in the gilt. In: D.J.A. Cole and G.R. Foxcroft (Editors), Control of Pig Reproduction. Butterworths, London, pp. 117138. Jezierski, W. and Myrcha, A., 1975. Food requirements of a wild boar population. Pol. Ecol. Stud., 1: 61-83. Kirkwood, R.N. and Aherne, F.X., 1985. Energy intake, body composition and reproductive performanceof the gilt. J. Anim. Sci., 60: 1518-1529. Klein, F., 1984. Contribution ~ l'6tude de la croissance du sanglier (Sus scro[a) par capture et recapture. In: F. Spitz and D. P~pin (Editors), Symposium International sur le Sanglier. Colloq. INRA, 22: 55-67. Kozlo, P.G., 1975. The Wild Boar. Uradzhaj, Minsk, pp. 1-224 (in Russian). Martinat-Bott~, F., Dando, P., Gautier, J. and Terqui, M., 1981. Variation saisonni&re de la taille de la pottle en relation avec celles du taux d'ovulation et de la mortalit~ embryonnaire chez la truie. Journ. Rech. Porcine France, 13: 269-276. Martinat-Bott~, F., Dagorn, J., Terqui, M. and Dando, P., 1984. Effect of confinement, climatic conditions and litter parity on the seasonal variations of the fertility rate and prolificacy. Ann. Rech. Vet., 15: 165-172. Matschke, G.H., 1964. The influence of oak mast on European wild hog reproduction. Trans. Annu. Conf. S.E. Assoc. Game Fish Comm., 18: 35-39. Matschke, G.H., 1967. Aging European wild hogs by dentition. J. Wildl. Manage., 31: 109-113. Mauget, R., 1980. R~gulations ~cologiques, comportementales et physiologiques (fonction de reproduction) de l'adaptation du sanglier au milieu. Th~se Doct. Etat, Univ. Tours, 299 pp. Mauget, R., 1982. Seasonality of reproduction in the wild boar. In: D.J.A. Cole and G.R. Foxcroft (Editors), Control of Pig Reproduction. Butterworths, London, pp. 509-526. Mauget, R. and P~pin, D., 1985. La pubert~ chez le sanglier: ~tude pr61iminaire du rSle de l'alimentation. In: S. de Combrudge (Editor), XVIIth Congr. Int. Union Game Biol. Ministery of Agriculture, Agricultural Research Administration, Brussels 1985, pp. 191-197. Mauget, R., Auma~tre, A. and Peignier, Y., 1988. Caract~risation de l'~tat trophique du sanglier, en milieu forestier, ~ partir du gras m6sent~rique et des param~tres sanguins. Reprod. Nutr. D~v., 28: 969-978. Mavrogenis, A.P. and Robison, O.W., 1976. Factors affecting puberty in swine. J. Anim. Sci., 42: 1251-1255. Oloff, H.B., 1951. Zur Biologie und ()kologie des Wildschweines. Beitr. Tierz., 2: 1-95.
77 PSpin, D., Spitz, F., Janeau, G. and Valet, G., 1987. Dynamics of reproduction and development of weight in the wild boar (Sus scrofa) in South-west France. Z. S~iugetierkd., 52: 21-30. Prunier, A. and Etienne, M., 1984. Effects of confinement on attainment of puberty in gilts. Ann. Rech. V~t., 15: 155-164. Prunier, A., Bonneau, M. and Etienne, M., 1987. Effects of age and live weight on the sexual development of gilts and boars fed two planes of nutrition. Reprod. Nutr. D~v., 27: 689-700. Sadleir, R..M.S., 1969. The Ecology of Reproduction in Wild and Domestic Animals. Methuen, London, 321 pp. Scanlon, P.F. and Krishnamurthy, S., 1974. Puberty attainment in slaughter-weight gilts in relation to month examined. J. Anita. Sci., 39:160 (abstr. 97). Sorensen, A.M., Jr., Thomas, W.B. and Gosset, J.W., 1961. A further study of the influence of level of energy intake and season on reproductive performance of gilts. J. Anim. Sci., 20: 347349. Stubbe, W. and Stubbe, M., 1977. Vergleichende Beitrage zur Reproduktions und Geburtsbiologie von Wild und Hausschwein Sus scrofa. Jagd Wildforsch., 10: 153-179. Zimmermann, D.R., Spies, H.G., Rigor, E.M., Self, H.L. and Casida, L.E., 1960. Effect of restricted feeding, cross breeding and season of birth on age at puberty in swine. J. Anim. Sci., 19: 687-694.