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Supplementation of Barbarine ewes with spineless cactus (Opuntia ficus-indica f. inermis) cladodes during late gestation-early suckling: Effects on mammary secretions, blood metabolites, lamb growth and postpartum ovarian activity
Small Ruminant Research 90 (2010) 53–57
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Supplementation of Barbarine ewes with spineless cactus (Opuntia ficus-indica f. inermis) cladodes during late gestation-early suckling: Effects on mammary secretions, blood metabolites, lamb growth and postpartum ovarian activity M. Rekik a,∗ , H. Ben Salem b , N. Lassoued b , H. Chalouati a , I. Ben Salem a a b
Ecole Nationale de Médecine Vétérinaire, 2020 Sidi Thabet, Tunisia INRA-Tunisie, Laboratoire des Productions Animales et Fourragères, Rue Hédi Karray, 2049 Ariana, Tunisia
a r t i c l e
i n f o
Article history: Received 28 February 2009 Received in revised form 21 December 2009 Accepted 23 December 2009 Available online 18 January 2010 Keywords: Ewes Cactus Mammary secretions Growth Ovarian activity
a b s t r a c t This trial investigated effects of cactus incorporation in the diet of the late pregnant-early suckling ewe on mammary gland secretions, blood metabolites, ovarian activity and lamb growth. Thirty-four single bearing ewes of the Barbarine breed aged 4.4 ± 1.7 years that were oestrus synchronised were selected. Animals were allocated to either barley treatment (n = 17) with daily feeding of 1.5 kg of oaten hay, 0.33 kg of barley and 0.11 kg of soybean meal per ewe or to a cactus treatment (n = 17), with feeding of 1.5 kg of oaten hay, 3 kg of cactus cladodes and 0.14 kg of soybean meal per ewe. The trial lasted approximately 60 days and started 4 weeks before lambing and continued until 30 days postpartum. Plasma concentrations of phosphorus, total protein, glucose and insulin before and after lambing slightly differed between ewes in both treatment groups and were more affected by time relative to lambing. Ewes fed cactus had higher (P < 0.05) plasma levels of calcium than their counterparts fed barley. Colostrum production did not differ between feeding regimes. The colostrum immunoglobulin G concentrations averaged 160 and 149 g/l (S.E.M. = 12.9) in the barley and cactus groups, respectively. Milk yield at day 10 and 30 from birth was not affected by treatment (P > 0.05). Milk yield at 30 days was 1030 and 1041 g/day (S.E.M. = 96.9) for barley and cactus, respectively. Lamb live weight at 10 days of age was, respectively, 6.2 and 6.8 kg (S.E.M. = 0.23) for barley and cactus and identical (9.5 kg) at 30 days of age. The feeding regime did not affect ovarian activity at 30 days from lambing. It is concluded that cactus can totally replace barley grain in the diet of late pregnant-early suckling Barbarine ewes without affecting mammary secretions, resumption of ovarian activity or lamb growth. © 2010 Elsevier B.V. All rights reserved.
1. Introduction In sheep, late pregnancy and early lactation are periods when nutrient demands are greatest. The challenge of adequately feeding the late pregnant-early suckling ewe is
∗ Corresponding author. Tel.: +216 71 552 200; fax: +216 71 552 441. E-mail address: [email protected] (M. Rekik). 0921-4488/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.smallrumres.2009.12.051
to sustain the accelerated growth of the foetus (Dawson et al., 1999), mammary gland development (Mellor and Murray, 1985), milk production (Mellor and Murray, 1985), colostrum yield and quality (Guinan et al., 2005; Ocak et al., 2005), and ultimately lamb survival (Ocak et al., 2005) and growth rate. In Tunisia as in many other countries of North Africa and West Asia, sheep breeds mate in the spring and lamb during late summer and fall, which is an extremely hot and dry season when growth of natural vegetation in
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pastures ceases (Rekik et al., 2005). To bridge this recurrent annual period of feed scarcity, farmers rely on supplemental feedstuffs such as conserved forages (hay, straw) or concentrates. Providing supplemental feedstuffs may not be cost-effective in low input systems of semi-arid and arid Tunisia (Ben Salem and Nefzaoui, 2003). In this respect, Ben Salem et al. (2005) hypothesised that shrubby vegetation could be a promising alternative fodder resource for ruminants. A typical example is spineless cactus (Opuntia ficus-indica f. inermis) that is widespread in Tunisia and many Mediterranean and Latin American countries. Several studies have addressed its effects on intake and digestion as well as on growth performance of lambs (Ben Salem and Smith, 2008) and meat quality (Atti et al., 2006). To our knowledge, data on the use of cactus to feed ewes in late pregnancy-early lactation are not available. The objective of this study was to investigate effects of total replacement of barley grain by cactus on mammary secretions, growth of lambs, blood metabolite levels and resumption of postpartum ovarian activity in singleton-bearing ewes of the Barbarine breed. 2. Materials and methods 2.1. Experimental location and animal management The trial lasted 60 days and was conducted between October and November at the experimental station of Bou Rebiaà of the National Institute of Agricultural Research (INRAT; latitude 36◦ 38 N; longitude 10◦ 07 E). Average annual rainfall is 350 mm and represents the mean of 30 years. A total of 34 pregnant adult ewes, all bearing single foetuses, of the Barbarine breed were used. The animals were 4.4 ± 1.70 years of age and had a body condition score (BCS) value based on the scale by Russel et al. (1969) of 1.7 ± 0.32 at the start of the experiment on day 120 of pregnancy. At all occasions, BCS of each animal was consecutively assessed by two trained persons and averaged. The ewes were drafted from a flock of 120 ewes that were oestrus synchronised in early June using progestagen intravaginal sponges for 14 days followed by introduction of rams. Oestrous manifestation and dates of mating were recorded individually. Until day 119 of pregnancy, ewes grazed cereal stubble and natural rangeland. On day 120 of pregnancy, animals were drenched against internal parasites using Oxfendazol (Medivet, Soliman, Tunisia) at a conventional dose of 5 mg/kg body weight. Animals were subdivided in relation to age and BCS into two experimental groups of 17 ewes each. One group subjected to a barley treatment receiving 1.5 kg of oaten hay, 0.33 kg of barley and 0.11 kg of soybean meal per ewe each day. Ewes on a cactus treatment received 1.5 kg of oaten hay, 3 kg of cactus cladodes (based on previous unpublished observations in our laboratory) and 0.14 kg of soybean meal per ewe each day. The feeding regimes were applied from 4 weeks before lambing until 30 days after. Diets were expected to provide the same quantity of energy and nitrogen. It was assumed that ME contents of barley, soybean meal, cactus and oaten hay were 12.6, 12.9, 8.4 and 8.9 MJ/kg DM, respectively (INRA, 1988; Nefzaoui and Chermiti, 1989; Le Houérou, 1996). Terminal and sub-terminal cactus cladodes were regularly harvested and cut into small slices using a manual chopper, then distributed to animals as fresh material. Animals were group-penned (2 m2 /animal) and fed according to treatment throughout the experimental period. Hay, concentrate feedstuffs and cactus were distributed in separate troughs. The size and the number of troughs placed in each pen were sufficient to prevent competition between animals. Animals were housed in a large enclosed barn with sufficient side openings to allow free circulation of air and exposure of the animals to natural photoperiod. Throughout the experimental period, animals had free access to water. Hay was subdivided into two equal parts that were distributed in the morning and evening. After the morning meal of hay, ewes in the barley group received a mixture of barley and soybean meal while their counterparts received the soybean meal alone then followed by cactus. Feed refusals were weighed daily.
2.2. Sampling and measurements Throughout the experimental period, weekly samples of the distributed feedstuffs were collected. Each sample was divided in two parts. One part was used for DM determination and the other one was also dried to determine the chemical composition (AOAC, 1984). BCS was determined at the start of the experiment, 1 week before lambing, 1 week after lambing and 30 days after lambing. Jugular blood was collected into 10-ml heparinised tubes immediately before the morning feeding at 0800 h. Blood samples were taken at 1 and 2 weeks prior to lambing and also at 1 and 2 weeks postpartum. The heparinised blood was centrifuged at 3000 × g for 15 min immediately after sampling. Equal volumes of plasma were poured into plastic tubes and stored at −20 ◦ C until being analysed for insulin and blood metabolites. In addition, luteal function was determined by assessing plasma progesterone level in jugular blood samples taken every 72 h between day 3 and 30 after lambing. When parturition was imminent, ewes were observed continuously. At lambing, the amount of colostrum accumulated was measured by handstripping one teat after an intramuscular injection of 10 i.u. of oxytocin to ensure complete milk letdown (Doney et al., 1979). The teat was then covered to prevent sucking. Milking was repeated at 1, 10 and 24 h postpartum with the recorded amount multiplied by 2 to calculate total udder production. At lambing, colostrum collected represented prenatal accumulation and subsequent yields represented quantities secreted since the previous milking (Banchero et al., 2004; Boland et al., 2005). At each occasion, the amount of colostrum was weighed and one sample of 40 ml was kept in a plastic vial containing potassium dichromate as a preservative. Vials were stored at −20 ◦ C for later determination of the fat and protein contents. For the accumulated colostrum at lambing, a further 5-ml sample was taken and frozen at −20 ◦ C for subsequent immunoglobulin G (IgG) analysis. At 10 and 30 days after lambing, milk yield was determined using the protocol described by Ricordeau et al. (1960). On each occasion of milk sampling, and after lambs were withdrawn, ewes received an intramuscular injection of oxytocin (10 i.u.) and then were hand-milked. The harvested milk was discarded. After 2 h, the ewe received a second intramuscular injection of oxytocin (10 i.u.) and milk collected was weighed. The yielded volume was then multiplied by 12 to calculate daily milk production. At birth, lambs were ear-tagged and weighed within 1 h. For the first 24 h after birth, lambs were allowed to suckle the teat that was not covered. Lambs were also weighed when they reached 10 and 30 days of age.
2.3. Laboratory analyses Ground samples of feeds were analysed for ash, calcium, phosphorus and crude protein according to procedures of AOAC (1984). Neutral detergent fibre was determined in feed as described by Van Soest et al. (1991). Oxalates were analysed following the procedure described by Moir (1953). Fat and protein contents of colostrum and milk were determined using an integrated milk analyser (Combifoss 5300, Foss Electric, Hillerød, Denmark). Colostrum samples taken at birth and at 1 h postpartum were diluted 4 times while those taken at 10 and 24 h postpartum were diluted 2 times. Colostral IgG concentration in the sample taken at birth was measured using single radial immunodiffusion kit (Bethyl Laboratories® , TX, USA) as described by Boland et al. (2005). For this purpose, samples of colostrum were diluted 20-fold. Plasma levels of total protein, glucose, Ca and P were all determined using commercially available kits (Biomaghreb® , Tunis, Tunisia). All kits were based on bio-chemically established procedures and concentrations were measured photometrically at specific wavelengths. Plasma insulin levels were measured by a specific sheep ELISA kit (Mercodia® , Uppsala, Sweden) as previously reported by Ben Salem et al. (2009). Sheep plasma was used undiluted, and inter- and intra-assay coefficients of variation were 8.7 and 4.2%, respectively. Plasma progesterone concentration was determined in duplicate using a Coat-A Count® , solid-phase radioimmunoassay kit (Diagnostic Products Corporation, Los Angeles CA, USA) as reported by Contreras-Solis et al. (2009). The limit of detection was 0.02 ng/ml. Inter- and intra-assay coefficients of variation were 5.6 and 3.8%, respectively.
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Table 1 Feedstuff chemical composition (g/kg dry matter ± S.D.). Oaten hay (n = 10) Dry matter (g/kg) Organic matter Crude protein Neutral detergent fibre Ca P Oxalates
896 916 48 603 5.4 1.1 1.4
± ± ± ± ± ± ±
30.8 8.8 11.6 42.1 0.8 0.7 0.1
Cactus cladodes (n = 10) 97 670 44 306 74.7 1.2 105.3
2.4. Statistical analysis Results, except for total colostrum yield, relative to colostrum and milk production as well as blood parameters were analysed using the MIXED models procedure (SAS Version 9.1, SAS Inst. Inc., Cary, NC, USA). Sources of variation included feeding regime, time, and feeding regime × time interaction. The random variable was ewe within treatment. Other continuous variables were analysed by the Proc GLM procedure of SAS with the feeding regime as a source of variation. The effect of the feeding regime was considered to be significant when level of probability less than 5% and Student’s t-test was then used to rank means. Differences in the numbers of animals having resumed ovarian activity were analysed using a 2 test. Unless otherwise stated, all the values are presented as mean ± S.E.M.
3. Results Chemical composition of the different feedstuffs used is presented in Table 1. Total DM intake averaged 1610 and 1650 g/day in barley and cactus ewes, respectively. Metabolizable energy and CP intakes averaged 15.8 MJ/day and 137 g, respectively by barley ewes and 15.0 MJ/day and 131 g/day, respectively by cactus ewes. Feeding regime had no effect on BCS (P > 0.05). At 4 weeks prior to lambing, BCS was 1.6 ± 0.06 and 1.7 ± 0.01 for barley and cactus ewes, respectively. After 1 month of suckling, BCS reached the lowest level (P < 0.01), being 1.2 ± 0.08 and 1.2 ± 0.16 for ewes of the barley and cactus groups, respectively. For colostrum and milk data, effects of both the feeding regime and the interaction between the feeding regime and time were not significant; only time had a significant effect. Data related to colostrum yield are summarised in Fig. 1. There was a wide variation in colostrum yield at each milking. Cactus-fed ewes tended to accumulate
Fig. 1. Mean weight (g) of colostrum accumulated at or secreted after parturition.
± ± ± ± ± ± ±
35.7 21.5 9.0 40.7 17.1 0.5 17.1
Barley (n = 4) 905 964 109 330 0.7 3.2 1.5
± ± ± ± ± ± ±
Soybean meal (n = 4)
31.4 5.4 8.0 26.1 0.1 0.3 0.0
894 909 470 158 5.5 4.4 1.3
± ± ± ± ± ± ±
40.7 11.7 17.3 10.7 1.9 0.9 0.0
more colostrum at birth and yielded more colostrum to 24 h than barley ewes but differences were not statistically significant (P > 0.05). Similarly, there were no differences between both treatments in IgG concentration in accumulated colostrum at lambing, which averaged 160 and 149 g/l (S.E.M. = 12.9) for barley and cactus, respectively. After partum and for ewes in both treatment groups, there was a rapid fall in concentration of protein in colostrum from 21.1 and 19.7% at birth to 8.1 and 7.8% at 24 h after birth for barley and cactus, respectively. Fat content for the period 0–1 h after lambing was high (14.7 ± 0.85% for ewes in both treatment groups) and then gradually declined to an overall concentration of 10.3 ± 0.82% at 24 h after lambing. For ewes receiving the barley and cactus regimes, milk yield at 10 days from lambing averaged 1441 and 1580 g/day (S.E.M. = 166.2), respectively. For both feeding regimes, milk yield decreased at 30 days to 1030 and 1041 g/day (S.E.M. = 96.9) for barley and cactus ewes, respectively.
Table 2 Mean concentrations of blood parameters in plasma of Barbarine ewes supplemented with barley or cactus. Treatment
Proteins (g/l) 2 weeks prepartum 1 week prepartum 1 week postpartum 2 weeks postpartum
S.E.M.
Barley
Cactus
77 66 71 85
84 69 64 80
Significance
5.9 4.3 1.6 4.6
Glucose (mmol/l) 2 weeks prepartum 1 week prepartum 1 week postpartum 2 weeks postpartum
2.4 2.8 2.5 3.1
2.9 2.8 2.7 2.7
0.12 0.15 0.20 0.16
Insulin (pmol/l) 2 weeks prepartum 1 week prepartum 1 week postpartum 2 weeks postpartum
42.1 42.6 40.5 38.3
43.0 49.7 41.2 40.0
3.15 4.66 5.74 3.30
Calcium (mmol/l) 2 weeks prepartum 1 week prepartum 1 week postpartum 2 weeks postpartum
2.3 2.2 2.3 2.5
2.5 2.5 2.3 2.9
0.10 0.09 0.07 0.09
Phosphorus (mmol/l) 2 weeks prepartum 1 week prepartum 1 week postpartum 2 weeks postpartum
1.6 1.1 1.5 1.6
1.7 1.4 1.4 1.8
0.22 0.11 0.09 0.16
** *
* *
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Fig. 2. Number of ovulating ewes in the first 30 days after lambing.
Throughout the 1st month of life, lambs born to barley and cactus ewes had a similar growth pattern. At 10 days of age, cactus lambs weighed 6.8 kg compared with 6.2 kg (S.E.M. = 0.23) for barley lambs. At 30 days of age, average BW of lambs of both treatments was 9.5 kg. For all blood parameters except glucose, the interaction between the feeding regime and time was not significant. Plasma concentrations of Ca, P, total protein, glucose and insulin before and after lambing are summarised in Table 2. Blood Ca concentration was affected by the feeding regime at 1 week prior to and at 2 weeks after lambing. At both occasions, ewes supplemented with cactus had a higher concentration of Ca than ewes supplemented with barley (P < 0.05). Time had no effect on plasma Ca. Phosphorus blood concentration was not affected by feeding regime at any stage before or after lambing (P > 0.05). Plasma P concentration tended to be lower immediately before and after lambing. The same tendency was observed for plasma total protein, with concentrations for ewes of both treatments being lower at 1 week before and 1 week after lambing than at 2 weeks after parturition. Glucose plasma concentrations at 2 weeks prior to lambing were higher in ewes that were supplemented with cactus (P < 0.05) and the situation was reversed 2 weeks after lambing, with ewes supplemented with barley having a higher concentration (P < 0.05). However, insulin concentration was low for ewes of both feeding regimes and not different at any sampling time, with no clear trend before or after lambing. Ovulation was considered to have occurred when there was a sustained increase in plasma progesterone level lasting for at least two consecutive samples and reaching not less than 0.8 ng/ml (Rekik, 1988). At 10, 20 and 30 days postpartum, the number of ewes having resumed their ovarian activity was not different (P > 0.05). At 30 days after lambing, respectively, 9 and 6 ewes in the cactus and barley groups had ovulated (Fig. 2). 4. Discussion Although ewes used in the current study were groupfed, complete consumption of concentrate feedstuffs and cactus and similar hay intake by barley and cactus ewes suggest that animals met their nutrient requirements dur-
ing late gestation and were slightly below requirements after lambing (INRA, 1988). Concentrations of blood metabolites were within ranges of physiological levels commonly reported for sheep (Kaneko, 1997) and within the figures reported by El-Sherif and Assad (2001), Antunovié et al. (2002) and Balikci et al. (2007) for pregnant and lactating sheep. No major effect of the diet was observed on the plasma mineral composition. The higher level of plasma Ca in cactus-fed ewes is most likely a consequence of the high level of Ca in cactus as was also reported previously (Ben Salem et al., 2004). However, Ca level in plasma is not considered a reliable indicator of Ca status and much of it can be unavailable because of presence of oxalates in cactus (Roque et al., 2007). The similar decrease in plasma total protein at the end of pregnancy for both treatments is a finding similar to that reported by Balikci et al. (2007) and El-Sherif and Assad (2001). This could be ascribed to the fact that foetal protein synthesis is all derived from the mother’s pool of amino acids (Jainudee and Hafez, 1994) and also to the production of globulin-rich colostrum (Davson and Segal, 1980). For both feeding regimes in this study, IgG concentration of the colostrum was higher than in other reports (Boland et al., 2005; Guinan et al., 2005). These two latter studies used the same analytical procedure as in the present work; differences are perhaps breed-related. As to practical implications, total replacement of barley by cactus maintained the same growth rate of lambs and also the proportion of ewes that reinitiated postpartum ovarian activity. The similar weight of lambs is backed by data on both colostrum and milk yields that were not affected by feeding regime, which is consistent with the similar energy and crude protein intakes by ewes. Energy balance during the postpartum period is one of the main factors determining reinitiation of reproductive activity and insulin appears to be the main modulator of effects of postpartum nutritional and energy balance on resumption of ovarian activity (Robinson et al., 2006). In the case of the present study, the nature of the supplement did not affect the proportion (53 and 35% for cactus and barley ewes, respectively) of ewes resuming postpartum ovarian activity. This result can be ascribed to similar energy balance for ewes on the two feeding regimes as indicated by the similar pattern of decline in body condition as well as the absence of differences in insulin level (Schlumbohm et al., 1997). The recorded proportions were lower than results for the same breed in the same season (Khaldi, 1984; Lassoued et al., 2004). Social and pheromonal interactions can account for the differences (Thimonier et al., 2000). In the two reported studies, the ewes were teased by rams, while in the present study, females were kept totally isolated from rams before and after lambing. 5. Conclusion Most of the measured physiological and productive traits in this experiment were unchanged or nonsignificantly improved when barley grain was totally replaced by cactus cladodes in the diet of late pregnant-early suckling ewes of the Barbarine breed. These results should contribute to the scientific basis to consider spineless cactus (O.
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ficus-indica f. inermis), the most extensively planted shrub for rangeland rehabilitation, as a strategic animal feedstuff in central Tunisia. Acknowledgements This work was supported by the International Atomic Energy Agency and the Tunisian Ministry of Scientific Research under the framework of the technical cooperation project TUN 5/021. References Antunovié, Z., Sencié, D., Speranda, M., Liker, B., 2002. Influence of the season and the reproductive status of ewes on blood parameters. Small Rumin. Res. 45, 39–44. Association of Official Analytical Chemists, 1984. Official Methods of Analysis, 14th ed. AOAC, Washington, DC. Atti, N., Mahouachi, M., Rouissi, H., 2006. The effect of spineless cactus (Opuntia ficus-indica f. inermis) supplementation on growth, carcass, meat quality and fatty acid composition of male goat kids. Meat Sci. 73, 229–235. Balikci, E., Yildiz, A., Gürdogan, F., 2007. Blood metabolite concentrations during pregnancy and postpartum in Akkaraman ewes. Small Rumin. Res. 67, 247–251. Banchero, G.E., Quintans, G., Martin, G.B., Milton, J.T.B., Lindsay, D.R., 2004. Nutrition and colostrum production in sheep. 2. Metabolic and hormonal responses to different energy sources in the final stages of pregnancy. Reprod. Fertil. Dev. 16, 645–653. Ben Salem, H., Abdouli, H., Nefzaoui, A., El-Mastouri, A., Ben Salem, L., 2005. Nutritive value, behaviour, and growth of Barbarine lambs fed on oldman saltbush (Atriplex nummularia L.) and supplemented or not with barley grains or spineless cactus (Opuntia ficus-indica f. inermis) pads. Small Rumin. Res. 59, 229–237. Ben Salem, H., Nefzaoui, A., 2003. Feed blocks as alternative supplements for sheep and goats. Small Rumin. Res. 49, 275–288. Ben Salem, H., Nefzaoui, A., Ben Salem, L., 2004. Spineless cactus (Opuntia ficus-indica f. inermis) and oldman saltbush (Atriplex nummularia L.) as alternative supplements for growing Barbarine lambs given strawbased diets. Small Rumin. Res. 51, 65–73. Ben Salem, H., Smith, T., 2008. Feeding strategies to increase small ruminant production in dry environments. Small Rumin. Res. 77, 174–194. Ben Salem, I., Rekik, Ben Hamouda, M., Lassoued, N., Blache, D., 2009. Live weight and metabolic changes and the associated reproductive performance in maiden ewes. Small Rumin. Res. 81, 70–74. Boland, T.M., Guinan, M., Brophy, P.O., Callan, J.J., Quinn, P.J., Nowakowski, P., Crosby, T.F., 2005. The effect of varying levels of mineral and iodine supplementation to ewes during late pregnancy on serum immunoglobulin G concentrations in their progeny. Anim. Sci. 80, 209–218. Contreras-Solis, I., Vasquez, B., Diaz, T., Letelier, C., Lopez-Sebastian, A., Gonzalez-Bulnes, A., 2009. Ovarian and endocrine responses in tropical sheep treated with reduced doses of cloprostenol. Anim. Reprod. Sci. 114, 384–392. Davson, H., Segal, M.B., 1980. Pregnancy: maintenance and prevention. In: Introduction to Physiology, vol. 5: Control of Reproduction. Academic Press, London, UK, pp. 258–288. Dawson, L.E.R., Carson, A.F., Kilpatrick, D.J., 1999. The effect of digestible undegradable protein concentration of concentrates and protein source offered to ewes in late pregnancy on colostrum production and lamb performance. Anim. Feed Sci. Technol. 82, 21–36. Doney, J.M., Pert, J.N., Smith, W.F., Louda, F., 1979. A consideration of the technique for estimation of milk yield and a comparison of estimates obtained by two methods in relation to effect of breed, level of production and stage of lactation. J. Agric. Sci. 92, 123–132. El-Sherif, M.M.A., Assad, F., 2001. Changes in some blood constituents of Barki ewes during pregnancy and lactation under semi arid conditions. Small Rumin. Res. 40, 269–277.
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Guinan, M., Harrison, G., Boland, T.M., Crosby, T.F., 2005. The effect of timing of mineral supplementation of the ewe diet in late pregnancy on immunoglobulin G absorption by the lamb. Anim. Sci. 80, 193–200. Institut National de la Recherche Agronomique (INRA), 1988. In: Jarrige, R. (Ed.), Alimentation des bovins, ovins et caprins. INRA, Paris, France, 476 p. Jainudee, M.R., Hafez, E.S.E., 1994. Gestation, prenatal physiology and parturition. In: Hafez, E.S.E. (Ed.), Reproduction in Farm Animals. Lea and Febiger, PA, USA, pp. 247–283. Kaneko, J.J., 1997. Clinical Biochemistry of Domestic Animals, 5th ed. Academic Press, San Diego, CA, pp. 661. Khaldi, G., 1984. Variations saisonnières de l’activité ovarienne, du comportement d’oestrus et de la durée de l’anoestrus post-partum des femelles ovines de race Barbarine: influence du niveau alimentaire et de la présence du mâle (Seasonal variations of ovarian activity, oestrus behaviour and the duration of post-partum anoestrus of ewes of the Barbarine breed: the effects of the level of feeding and the presence of males). Thèse de Doctorat d’état. Université des Sciences et Techniques du Languedoc, Montpellier, France, 168 pp. Lassoued, N., Naouali, M., Khaldi, G., Rekik, M., 2004. Influence of the permanent presence of rams on the resumption of sexual activity in postpartum Barbarine ewes. Small Rumin. Res. 54, 25–31. Le Houérou, H.N., 1996. The role of cacti (Opuntia spp.) in erosion control, land reclamation, rehabilitation and agricultural development in the Mediterranean Basin. J. Arid Environ. 33, 135–159. Mellor, D.J., Murray, L., 1985. Effects of maternal nutrition on udder development during the pregnancy and on colostrum production in Scottish Blackface ewes with twin lambs. Res. Vet. Sci. 39, 230–234. Moir, K.W., 1953. The determination of oxalic acid in plants. Queensland J. Agric. Sci. 10 (March (1)), 1–3. Nefzaoui, A., Chermiti, A., 1989. Composition chimique et valeur nutritive pour les ruminants des fourrages et concentrés d’origine tunisienne. Annales de l’Institut National de la Recherche Agronomique de Tunisie 62. Ocak, N., Cam, M.A., Kuran, M., 2005. The effect of high dietary protein levels during late gestation on colostrum yield and lamb survival rate in singleton-bearing ewes. Small Rumin. Res. 56, 89–94. Rekik, M., 1988. The effect of rams and pre-treatment with progesterone or melatonin upon gonadotrophin secretion, follicular development and reproductive performance of anoestrous adult ewes. Ph.D. Thesis, University of Reading, UK, 124 pp. Rekik, M., Aloulou, R., Ben Hamouda, M., 2005. Small ruminant breeds of Tunisia. In: Iniguez, L. (Ed.), Characterisation of Small Ruminant Breeds in West Asia and North Africa, vol. 2. International Centre for Agricultural Research in the Dry Areas (ICARDA), Aleppo, Syria, pp. 91–140. Ricordeau, G., Boccard, R., Denamus, R., 1960. Mesure de la production laitière des femelles ovines et bovines pendant la phase d’allaitement (Measurement of milk production by ovine and bovine females during the suckling phase). Ann. Zootech. 9, 98–120. Robinson, J.J., Ashworth, C.J., Rooke, J.A., Mitchell, L.M., McEvoy, T.G., 2006. Nutrition and fertility in ruminant livestock. Anim. Feed Sci. Technol. 126, 259–276. Roque, A.P., Dias, R.S., Silber Schmidt Vitti, D.M., da Silva Bueno, I.C., da Cunha, E.A., dos Santos, L.E., Sartori Bueno, M., 2007. True digestibility of calcium from sources used in finishing lamb diets. Small Rumin. Res. 71, 243–249. Russel, A.J.F., Doney, J.M., Gunn, R.J., 1969. Subjective assessment of body fat in live sheep. J. Agric. Sci. 72, 451–454. Schlumbohm, C., Sporleder, H.P., Gurtler, H., Harmeyer, J., 1997. The influence of insulin on metabolism of glucose, free fatty acids and glycerol in normo- and hypocalcaemic ewes during different reproductive states. Deutsch. Tierärztl. Wochenschr. 104, 359–365. Thimonier, J., Cognié, Y., Lassoued, N., Khaldi, G., 2000. L’effet mâle chez les ovins: une technique actuelle de maîtrise de la reproduction (The ram effect: an up-to-date method for the control of oestrus and ovulation in sheep). Prod. Anim. 13, 223–231. Van Soest, P.J., Robertson, J.B., Lewis, B.-A., 1991. Methods for dietary fibre, neutral detergent fibre, and nonstarch carbohydrates in relation to animal nutrition. J. Dairy Sci. 74, 3583–3597.
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Small Ruminant Research journal homepage: www.elsevier.com/locate/smallrumres
Supplementation of Barbarine ewes with spineless cactus (Opuntia ficus-indica f. inermis) cladodes during late gestation-early suckling: Effects on mammary secretions, blood metabolites, lamb growth and postpartum ovarian activity M. Rekik a,∗ , H. Ben Salem b , N. Lassoued b , H. Chalouati a , I. Ben Salem a a b
Ecole Nationale de Médecine Vétérinaire, 2020 Sidi Thabet, Tunisia INRA-Tunisie, Laboratoire des Productions Animales et Fourragères, Rue Hédi Karray, 2049 Ariana, Tunisia
a r t i c l e
i n f o
Article history: Received 28 February 2009 Received in revised form 21 December 2009 Accepted 23 December 2009 Available online 18 January 2010 Keywords: Ewes Cactus Mammary secretions Growth Ovarian activity
a b s t r a c t This trial investigated effects of cactus incorporation in the diet of the late pregnant-early suckling ewe on mammary gland secretions, blood metabolites, ovarian activity and lamb growth. Thirty-four single bearing ewes of the Barbarine breed aged 4.4 ± 1.7 years that were oestrus synchronised were selected. Animals were allocated to either barley treatment (n = 17) with daily feeding of 1.5 kg of oaten hay, 0.33 kg of barley and 0.11 kg of soybean meal per ewe or to a cactus treatment (n = 17), with feeding of 1.5 kg of oaten hay, 3 kg of cactus cladodes and 0.14 kg of soybean meal per ewe. The trial lasted approximately 60 days and started 4 weeks before lambing and continued until 30 days postpartum. Plasma concentrations of phosphorus, total protein, glucose and insulin before and after lambing slightly differed between ewes in both treatment groups and were more affected by time relative to lambing. Ewes fed cactus had higher (P < 0.05) plasma levels of calcium than their counterparts fed barley. Colostrum production did not differ between feeding regimes. The colostrum immunoglobulin G concentrations averaged 160 and 149 g/l (S.E.M. = 12.9) in the barley and cactus groups, respectively. Milk yield at day 10 and 30 from birth was not affected by treatment (P > 0.05). Milk yield at 30 days was 1030 and 1041 g/day (S.E.M. = 96.9) for barley and cactus, respectively. Lamb live weight at 10 days of age was, respectively, 6.2 and 6.8 kg (S.E.M. = 0.23) for barley and cactus and identical (9.5 kg) at 30 days of age. The feeding regime did not affect ovarian activity at 30 days from lambing. It is concluded that cactus can totally replace barley grain in the diet of late pregnant-early suckling Barbarine ewes without affecting mammary secretions, resumption of ovarian activity or lamb growth. © 2010 Elsevier B.V. All rights reserved.
1. Introduction In sheep, late pregnancy and early lactation are periods when nutrient demands are greatest. The challenge of adequately feeding the late pregnant-early suckling ewe is
∗ Corresponding author. Tel.: +216 71 552 200; fax: +216 71 552 441. E-mail address: [email protected] (M. Rekik). 0921-4488/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.smallrumres.2009.12.051
to sustain the accelerated growth of the foetus (Dawson et al., 1999), mammary gland development (Mellor and Murray, 1985), milk production (Mellor and Murray, 1985), colostrum yield and quality (Guinan et al., 2005; Ocak et al., 2005), and ultimately lamb survival (Ocak et al., 2005) and growth rate. In Tunisia as in many other countries of North Africa and West Asia, sheep breeds mate in the spring and lamb during late summer and fall, which is an extremely hot and dry season when growth of natural vegetation in
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pastures ceases (Rekik et al., 2005). To bridge this recurrent annual period of feed scarcity, farmers rely on supplemental feedstuffs such as conserved forages (hay, straw) or concentrates. Providing supplemental feedstuffs may not be cost-effective in low input systems of semi-arid and arid Tunisia (Ben Salem and Nefzaoui, 2003). In this respect, Ben Salem et al. (2005) hypothesised that shrubby vegetation could be a promising alternative fodder resource for ruminants. A typical example is spineless cactus (Opuntia ficus-indica f. inermis) that is widespread in Tunisia and many Mediterranean and Latin American countries. Several studies have addressed its effects on intake and digestion as well as on growth performance of lambs (Ben Salem and Smith, 2008) and meat quality (Atti et al., 2006). To our knowledge, data on the use of cactus to feed ewes in late pregnancy-early lactation are not available. The objective of this study was to investigate effects of total replacement of barley grain by cactus on mammary secretions, growth of lambs, blood metabolite levels and resumption of postpartum ovarian activity in singleton-bearing ewes of the Barbarine breed. 2. Materials and methods 2.1. Experimental location and animal management The trial lasted 60 days and was conducted between October and November at the experimental station of Bou Rebiaà of the National Institute of Agricultural Research (INRAT; latitude 36◦ 38 N; longitude 10◦ 07 E). Average annual rainfall is 350 mm and represents the mean of 30 years. A total of 34 pregnant adult ewes, all bearing single foetuses, of the Barbarine breed were used. The animals were 4.4 ± 1.70 years of age and had a body condition score (BCS) value based on the scale by Russel et al. (1969) of 1.7 ± 0.32 at the start of the experiment on day 120 of pregnancy. At all occasions, BCS of each animal was consecutively assessed by two trained persons and averaged. The ewes were drafted from a flock of 120 ewes that were oestrus synchronised in early June using progestagen intravaginal sponges for 14 days followed by introduction of rams. Oestrous manifestation and dates of mating were recorded individually. Until day 119 of pregnancy, ewes grazed cereal stubble and natural rangeland. On day 120 of pregnancy, animals were drenched against internal parasites using Oxfendazol (Medivet, Soliman, Tunisia) at a conventional dose of 5 mg/kg body weight. Animals were subdivided in relation to age and BCS into two experimental groups of 17 ewes each. One group subjected to a barley treatment receiving 1.5 kg of oaten hay, 0.33 kg of barley and 0.11 kg of soybean meal per ewe each day. Ewes on a cactus treatment received 1.5 kg of oaten hay, 3 kg of cactus cladodes (based on previous unpublished observations in our laboratory) and 0.14 kg of soybean meal per ewe each day. The feeding regimes were applied from 4 weeks before lambing until 30 days after. Diets were expected to provide the same quantity of energy and nitrogen. It was assumed that ME contents of barley, soybean meal, cactus and oaten hay were 12.6, 12.9, 8.4 and 8.9 MJ/kg DM, respectively (INRA, 1988; Nefzaoui and Chermiti, 1989; Le Houérou, 1996). Terminal and sub-terminal cactus cladodes were regularly harvested and cut into small slices using a manual chopper, then distributed to animals as fresh material. Animals were group-penned (2 m2 /animal) and fed according to treatment throughout the experimental period. Hay, concentrate feedstuffs and cactus were distributed in separate troughs. The size and the number of troughs placed in each pen were sufficient to prevent competition between animals. Animals were housed in a large enclosed barn with sufficient side openings to allow free circulation of air and exposure of the animals to natural photoperiod. Throughout the experimental period, animals had free access to water. Hay was subdivided into two equal parts that were distributed in the morning and evening. After the morning meal of hay, ewes in the barley group received a mixture of barley and soybean meal while their counterparts received the soybean meal alone then followed by cactus. Feed refusals were weighed daily.
2.2. Sampling and measurements Throughout the experimental period, weekly samples of the distributed feedstuffs were collected. Each sample was divided in two parts. One part was used for DM determination and the other one was also dried to determine the chemical composition (AOAC, 1984). BCS was determined at the start of the experiment, 1 week before lambing, 1 week after lambing and 30 days after lambing. Jugular blood was collected into 10-ml heparinised tubes immediately before the morning feeding at 0800 h. Blood samples were taken at 1 and 2 weeks prior to lambing and also at 1 and 2 weeks postpartum. The heparinised blood was centrifuged at 3000 × g for 15 min immediately after sampling. Equal volumes of plasma were poured into plastic tubes and stored at −20 ◦ C until being analysed for insulin and blood metabolites. In addition, luteal function was determined by assessing plasma progesterone level in jugular blood samples taken every 72 h between day 3 and 30 after lambing. When parturition was imminent, ewes were observed continuously. At lambing, the amount of colostrum accumulated was measured by handstripping one teat after an intramuscular injection of 10 i.u. of oxytocin to ensure complete milk letdown (Doney et al., 1979). The teat was then covered to prevent sucking. Milking was repeated at 1, 10 and 24 h postpartum with the recorded amount multiplied by 2 to calculate total udder production. At lambing, colostrum collected represented prenatal accumulation and subsequent yields represented quantities secreted since the previous milking (Banchero et al., 2004; Boland et al., 2005). At each occasion, the amount of colostrum was weighed and one sample of 40 ml was kept in a plastic vial containing potassium dichromate as a preservative. Vials were stored at −20 ◦ C for later determination of the fat and protein contents. For the accumulated colostrum at lambing, a further 5-ml sample was taken and frozen at −20 ◦ C for subsequent immunoglobulin G (IgG) analysis. At 10 and 30 days after lambing, milk yield was determined using the protocol described by Ricordeau et al. (1960). On each occasion of milk sampling, and after lambs were withdrawn, ewes received an intramuscular injection of oxytocin (10 i.u.) and then were hand-milked. The harvested milk was discarded. After 2 h, the ewe received a second intramuscular injection of oxytocin (10 i.u.) and milk collected was weighed. The yielded volume was then multiplied by 12 to calculate daily milk production. At birth, lambs were ear-tagged and weighed within 1 h. For the first 24 h after birth, lambs were allowed to suckle the teat that was not covered. Lambs were also weighed when they reached 10 and 30 days of age.
2.3. Laboratory analyses Ground samples of feeds were analysed for ash, calcium, phosphorus and crude protein according to procedures of AOAC (1984). Neutral detergent fibre was determined in feed as described by Van Soest et al. (1991). Oxalates were analysed following the procedure described by Moir (1953). Fat and protein contents of colostrum and milk were determined using an integrated milk analyser (Combifoss 5300, Foss Electric, Hillerød, Denmark). Colostrum samples taken at birth and at 1 h postpartum were diluted 4 times while those taken at 10 and 24 h postpartum were diluted 2 times. Colostral IgG concentration in the sample taken at birth was measured using single radial immunodiffusion kit (Bethyl Laboratories® , TX, USA) as described by Boland et al. (2005). For this purpose, samples of colostrum were diluted 20-fold. Plasma levels of total protein, glucose, Ca and P were all determined using commercially available kits (Biomaghreb® , Tunis, Tunisia). All kits were based on bio-chemically established procedures and concentrations were measured photometrically at specific wavelengths. Plasma insulin levels were measured by a specific sheep ELISA kit (Mercodia® , Uppsala, Sweden) as previously reported by Ben Salem et al. (2009). Sheep plasma was used undiluted, and inter- and intra-assay coefficients of variation were 8.7 and 4.2%, respectively. Plasma progesterone concentration was determined in duplicate using a Coat-A Count® , solid-phase radioimmunoassay kit (Diagnostic Products Corporation, Los Angeles CA, USA) as reported by Contreras-Solis et al. (2009). The limit of detection was 0.02 ng/ml. Inter- and intra-assay coefficients of variation were 5.6 and 3.8%, respectively.
M. Rekik et al. / Small Ruminant Research 90 (2010) 53–57
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Table 1 Feedstuff chemical composition (g/kg dry matter ± S.D.). Oaten hay (n = 10) Dry matter (g/kg) Organic matter Crude protein Neutral detergent fibre Ca P Oxalates
896 916 48 603 5.4 1.1 1.4
± ± ± ± ± ± ±
30.8 8.8 11.6 42.1 0.8 0.7 0.1
Cactus cladodes (n = 10) 97 670 44 306 74.7 1.2 105.3
2.4. Statistical analysis Results, except for total colostrum yield, relative to colostrum and milk production as well as blood parameters were analysed using the MIXED models procedure (SAS Version 9.1, SAS Inst. Inc., Cary, NC, USA). Sources of variation included feeding regime, time, and feeding regime × time interaction. The random variable was ewe within treatment. Other continuous variables were analysed by the Proc GLM procedure of SAS with the feeding regime as a source of variation. The effect of the feeding regime was considered to be significant when level of probability less than 5% and Student’s t-test was then used to rank means. Differences in the numbers of animals having resumed ovarian activity were analysed using a 2 test. Unless otherwise stated, all the values are presented as mean ± S.E.M.
3. Results Chemical composition of the different feedstuffs used is presented in Table 1. Total DM intake averaged 1610 and 1650 g/day in barley and cactus ewes, respectively. Metabolizable energy and CP intakes averaged 15.8 MJ/day and 137 g, respectively by barley ewes and 15.0 MJ/day and 131 g/day, respectively by cactus ewes. Feeding regime had no effect on BCS (P > 0.05). At 4 weeks prior to lambing, BCS was 1.6 ± 0.06 and 1.7 ± 0.01 for barley and cactus ewes, respectively. After 1 month of suckling, BCS reached the lowest level (P < 0.01), being 1.2 ± 0.08 and 1.2 ± 0.16 for ewes of the barley and cactus groups, respectively. For colostrum and milk data, effects of both the feeding regime and the interaction between the feeding regime and time were not significant; only time had a significant effect. Data related to colostrum yield are summarised in Fig. 1. There was a wide variation in colostrum yield at each milking. Cactus-fed ewes tended to accumulate
Fig. 1. Mean weight (g) of colostrum accumulated at or secreted after parturition.
± ± ± ± ± ± ±
35.7 21.5 9.0 40.7 17.1 0.5 17.1
Barley (n = 4) 905 964 109 330 0.7 3.2 1.5
± ± ± ± ± ± ±
Soybean meal (n = 4)
31.4 5.4 8.0 26.1 0.1 0.3 0.0
894 909 470 158 5.5 4.4 1.3
± ± ± ± ± ± ±
40.7 11.7 17.3 10.7 1.9 0.9 0.0
more colostrum at birth and yielded more colostrum to 24 h than barley ewes but differences were not statistically significant (P > 0.05). Similarly, there were no differences between both treatments in IgG concentration in accumulated colostrum at lambing, which averaged 160 and 149 g/l (S.E.M. = 12.9) for barley and cactus, respectively. After partum and for ewes in both treatment groups, there was a rapid fall in concentration of protein in colostrum from 21.1 and 19.7% at birth to 8.1 and 7.8% at 24 h after birth for barley and cactus, respectively. Fat content for the period 0–1 h after lambing was high (14.7 ± 0.85% for ewes in both treatment groups) and then gradually declined to an overall concentration of 10.3 ± 0.82% at 24 h after lambing. For ewes receiving the barley and cactus regimes, milk yield at 10 days from lambing averaged 1441 and 1580 g/day (S.E.M. = 166.2), respectively. For both feeding regimes, milk yield decreased at 30 days to 1030 and 1041 g/day (S.E.M. = 96.9) for barley and cactus ewes, respectively.
Table 2 Mean concentrations of blood parameters in plasma of Barbarine ewes supplemented with barley or cactus. Treatment
Proteins (g/l) 2 weeks prepartum 1 week prepartum 1 week postpartum 2 weeks postpartum
S.E.M.
Barley
Cactus
77 66 71 85
84 69 64 80
Significance
5.9 4.3 1.6 4.6
Glucose (mmol/l) 2 weeks prepartum 1 week prepartum 1 week postpartum 2 weeks postpartum
2.4 2.8 2.5 3.1
2.9 2.8 2.7 2.7
0.12 0.15 0.20 0.16
Insulin (pmol/l) 2 weeks prepartum 1 week prepartum 1 week postpartum 2 weeks postpartum
42.1 42.6 40.5 38.3
43.0 49.7 41.2 40.0
3.15 4.66 5.74 3.30
Calcium (mmol/l) 2 weeks prepartum 1 week prepartum 1 week postpartum 2 weeks postpartum
2.3 2.2 2.3 2.5
2.5 2.5 2.3 2.9
0.10 0.09 0.07 0.09
Phosphorus (mmol/l) 2 weeks prepartum 1 week prepartum 1 week postpartum 2 weeks postpartum
1.6 1.1 1.5 1.6
1.7 1.4 1.4 1.8
0.22 0.11 0.09 0.16
** *
* *
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Fig. 2. Number of ovulating ewes in the first 30 days after lambing.
Throughout the 1st month of life, lambs born to barley and cactus ewes had a similar growth pattern. At 10 days of age, cactus lambs weighed 6.8 kg compared with 6.2 kg (S.E.M. = 0.23) for barley lambs. At 30 days of age, average BW of lambs of both treatments was 9.5 kg. For all blood parameters except glucose, the interaction between the feeding regime and time was not significant. Plasma concentrations of Ca, P, total protein, glucose and insulin before and after lambing are summarised in Table 2. Blood Ca concentration was affected by the feeding regime at 1 week prior to and at 2 weeks after lambing. At both occasions, ewes supplemented with cactus had a higher concentration of Ca than ewes supplemented with barley (P < 0.05). Time had no effect on plasma Ca. Phosphorus blood concentration was not affected by feeding regime at any stage before or after lambing (P > 0.05). Plasma P concentration tended to be lower immediately before and after lambing. The same tendency was observed for plasma total protein, with concentrations for ewes of both treatments being lower at 1 week before and 1 week after lambing than at 2 weeks after parturition. Glucose plasma concentrations at 2 weeks prior to lambing were higher in ewes that were supplemented with cactus (P < 0.05) and the situation was reversed 2 weeks after lambing, with ewes supplemented with barley having a higher concentration (P < 0.05). However, insulin concentration was low for ewes of both feeding regimes and not different at any sampling time, with no clear trend before or after lambing. Ovulation was considered to have occurred when there was a sustained increase in plasma progesterone level lasting for at least two consecutive samples and reaching not less than 0.8 ng/ml (Rekik, 1988). At 10, 20 and 30 days postpartum, the number of ewes having resumed their ovarian activity was not different (P > 0.05). At 30 days after lambing, respectively, 9 and 6 ewes in the cactus and barley groups had ovulated (Fig. 2). 4. Discussion Although ewes used in the current study were groupfed, complete consumption of concentrate feedstuffs and cactus and similar hay intake by barley and cactus ewes suggest that animals met their nutrient requirements dur-
ing late gestation and were slightly below requirements after lambing (INRA, 1988). Concentrations of blood metabolites were within ranges of physiological levels commonly reported for sheep (Kaneko, 1997) and within the figures reported by El-Sherif and Assad (2001), Antunovié et al. (2002) and Balikci et al. (2007) for pregnant and lactating sheep. No major effect of the diet was observed on the plasma mineral composition. The higher level of plasma Ca in cactus-fed ewes is most likely a consequence of the high level of Ca in cactus as was also reported previously (Ben Salem et al., 2004). However, Ca level in plasma is not considered a reliable indicator of Ca status and much of it can be unavailable because of presence of oxalates in cactus (Roque et al., 2007). The similar decrease in plasma total protein at the end of pregnancy for both treatments is a finding similar to that reported by Balikci et al. (2007) and El-Sherif and Assad (2001). This could be ascribed to the fact that foetal protein synthesis is all derived from the mother’s pool of amino acids (Jainudee and Hafez, 1994) and also to the production of globulin-rich colostrum (Davson and Segal, 1980). For both feeding regimes in this study, IgG concentration of the colostrum was higher than in other reports (Boland et al., 2005; Guinan et al., 2005). These two latter studies used the same analytical procedure as in the present work; differences are perhaps breed-related. As to practical implications, total replacement of barley by cactus maintained the same growth rate of lambs and also the proportion of ewes that reinitiated postpartum ovarian activity. The similar weight of lambs is backed by data on both colostrum and milk yields that were not affected by feeding regime, which is consistent with the similar energy and crude protein intakes by ewes. Energy balance during the postpartum period is one of the main factors determining reinitiation of reproductive activity and insulin appears to be the main modulator of effects of postpartum nutritional and energy balance on resumption of ovarian activity (Robinson et al., 2006). In the case of the present study, the nature of the supplement did not affect the proportion (53 and 35% for cactus and barley ewes, respectively) of ewes resuming postpartum ovarian activity. This result can be ascribed to similar energy balance for ewes on the two feeding regimes as indicated by the similar pattern of decline in body condition as well as the absence of differences in insulin level (Schlumbohm et al., 1997). The recorded proportions were lower than results for the same breed in the same season (Khaldi, 1984; Lassoued et al., 2004). Social and pheromonal interactions can account for the differences (Thimonier et al., 2000). In the two reported studies, the ewes were teased by rams, while in the present study, females were kept totally isolated from rams before and after lambing. 5. Conclusion Most of the measured physiological and productive traits in this experiment were unchanged or nonsignificantly improved when barley grain was totally replaced by cactus cladodes in the diet of late pregnant-early suckling ewes of the Barbarine breed. These results should contribute to the scientific basis to consider spineless cactus (O.
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ficus-indica f. inermis), the most extensively planted shrub for rangeland rehabilitation, as a strategic animal feedstuff in central Tunisia. Acknowledgements This work was supported by the International Atomic Energy Agency and the Tunisian Ministry of Scientific Research under the framework of the technical cooperation project TUN 5/021. References Antunovié, Z., Sencié, D., Speranda, M., Liker, B., 2002. Influence of the season and the reproductive status of ewes on blood parameters. Small Rumin. Res. 45, 39–44. Association of Official Analytical Chemists, 1984. Official Methods of Analysis, 14th ed. AOAC, Washington, DC. Atti, N., Mahouachi, M., Rouissi, H., 2006. The effect of spineless cactus (Opuntia ficus-indica f. inermis) supplementation on growth, carcass, meat quality and fatty acid composition of male goat kids. Meat Sci. 73, 229–235. Balikci, E., Yildiz, A., Gürdogan, F., 2007. Blood metabolite concentrations during pregnancy and postpartum in Akkaraman ewes. Small Rumin. Res. 67, 247–251. Banchero, G.E., Quintans, G., Martin, G.B., Milton, J.T.B., Lindsay, D.R., 2004. Nutrition and colostrum production in sheep. 2. Metabolic and hormonal responses to different energy sources in the final stages of pregnancy. Reprod. Fertil. Dev. 16, 645–653. Ben Salem, H., Abdouli, H., Nefzaoui, A., El-Mastouri, A., Ben Salem, L., 2005. Nutritive value, behaviour, and growth of Barbarine lambs fed on oldman saltbush (Atriplex nummularia L.) and supplemented or not with barley grains or spineless cactus (Opuntia ficus-indica f. inermis) pads. Small Rumin. Res. 59, 229–237. Ben Salem, H., Nefzaoui, A., 2003. Feed blocks as alternative supplements for sheep and goats. Small Rumin. Res. 49, 275–288. Ben Salem, H., Nefzaoui, A., Ben Salem, L., 2004. Spineless cactus (Opuntia ficus-indica f. inermis) and oldman saltbush (Atriplex nummularia L.) as alternative supplements for growing Barbarine lambs given strawbased diets. Small Rumin. Res. 51, 65–73. Ben Salem, H., Smith, T., 2008. Feeding strategies to increase small ruminant production in dry environments. Small Rumin. Res. 77, 174–194. Ben Salem, I., Rekik, Ben Hamouda, M., Lassoued, N., Blache, D., 2009. Live weight and metabolic changes and the associated reproductive performance in maiden ewes. Small Rumin. Res. 81, 70–74. Boland, T.M., Guinan, M., Brophy, P.O., Callan, J.J., Quinn, P.J., Nowakowski, P., Crosby, T.F., 2005. The effect of varying levels of mineral and iodine supplementation to ewes during late pregnancy on serum immunoglobulin G concentrations in their progeny. Anim. Sci. 80, 209–218. Contreras-Solis, I., Vasquez, B., Diaz, T., Letelier, C., Lopez-Sebastian, A., Gonzalez-Bulnes, A., 2009. Ovarian and endocrine responses in tropical sheep treated with reduced doses of cloprostenol. Anim. Reprod. Sci. 114, 384–392. Davson, H., Segal, M.B., 1980. Pregnancy: maintenance and prevention. In: Introduction to Physiology, vol. 5: Control of Reproduction. Academic Press, London, UK, pp. 258–288. Dawson, L.E.R., Carson, A.F., Kilpatrick, D.J., 1999. The effect of digestible undegradable protein concentration of concentrates and protein source offered to ewes in late pregnancy on colostrum production and lamb performance. Anim. Feed Sci. Technol. 82, 21–36. Doney, J.M., Pert, J.N., Smith, W.F., Louda, F., 1979. A consideration of the technique for estimation of milk yield and a comparison of estimates obtained by two methods in relation to effect of breed, level of production and stage of lactation. J. Agric. Sci. 92, 123–132. El-Sherif, M.M.A., Assad, F., 2001. Changes in some blood constituents of Barki ewes during pregnancy and lactation under semi arid conditions. Small Rumin. Res. 40, 269–277.
57
Guinan, M., Harrison, G., Boland, T.M., Crosby, T.F., 2005. The effect of timing of mineral supplementation of the ewe diet in late pregnancy on immunoglobulin G absorption by the lamb. Anim. Sci. 80, 193–200. Institut National de la Recherche Agronomique (INRA), 1988. In: Jarrige, R. (Ed.), Alimentation des bovins, ovins et caprins. INRA, Paris, France, 476 p. Jainudee, M.R., Hafez, E.S.E., 1994. Gestation, prenatal physiology and parturition. In: Hafez, E.S.E. (Ed.), Reproduction in Farm Animals. Lea and Febiger, PA, USA, pp. 247–283. Kaneko, J.J., 1997. Clinical Biochemistry of Domestic Animals, 5th ed. Academic Press, San Diego, CA, pp. 661. Khaldi, G., 1984. Variations saisonnières de l’activité ovarienne, du comportement d’oestrus et de la durée de l’anoestrus post-partum des femelles ovines de race Barbarine: influence du niveau alimentaire et de la présence du mâle (Seasonal variations of ovarian activity, oestrus behaviour and the duration of post-partum anoestrus of ewes of the Barbarine breed: the effects of the level of feeding and the presence of males). Thèse de Doctorat d’état. Université des Sciences et Techniques du Languedoc, Montpellier, France, 168 pp. Lassoued, N., Naouali, M., Khaldi, G., Rekik, M., 2004. Influence of the permanent presence of rams on the resumption of sexual activity in postpartum Barbarine ewes. Small Rumin. Res. 54, 25–31. Le Houérou, H.N., 1996. The role of cacti (Opuntia spp.) in erosion control, land reclamation, rehabilitation and agricultural development in the Mediterranean Basin. J. Arid Environ. 33, 135–159. Mellor, D.J., Murray, L., 1985. Effects of maternal nutrition on udder development during the pregnancy and on colostrum production in Scottish Blackface ewes with twin lambs. Res. Vet. Sci. 39, 230–234. Moir, K.W., 1953. The determination of oxalic acid in plants. Queensland J. Agric. Sci. 10 (March (1)), 1–3. Nefzaoui, A., Chermiti, A., 1989. Composition chimique et valeur nutritive pour les ruminants des fourrages et concentrés d’origine tunisienne. Annales de l’Institut National de la Recherche Agronomique de Tunisie 62. Ocak, N., Cam, M.A., Kuran, M., 2005. The effect of high dietary protein levels during late gestation on colostrum yield and lamb survival rate in singleton-bearing ewes. Small Rumin. Res. 56, 89–94. Rekik, M., 1988. The effect of rams and pre-treatment with progesterone or melatonin upon gonadotrophin secretion, follicular development and reproductive performance of anoestrous adult ewes. Ph.D. Thesis, University of Reading, UK, 124 pp. Rekik, M., Aloulou, R., Ben Hamouda, M., 2005. Small ruminant breeds of Tunisia. In: Iniguez, L. (Ed.), Characterisation of Small Ruminant Breeds in West Asia and North Africa, vol. 2. International Centre for Agricultural Research in the Dry Areas (ICARDA), Aleppo, Syria, pp. 91–140. Ricordeau, G., Boccard, R., Denamus, R., 1960. Mesure de la production laitière des femelles ovines et bovines pendant la phase d’allaitement (Measurement of milk production by ovine and bovine females during the suckling phase). Ann. Zootech. 9, 98–120. Robinson, J.J., Ashworth, C.J., Rooke, J.A., Mitchell, L.M., McEvoy, T.G., 2006. Nutrition and fertility in ruminant livestock. Anim. Feed Sci. Technol. 126, 259–276. Roque, A.P., Dias, R.S., Silber Schmidt Vitti, D.M., da Silva Bueno, I.C., da Cunha, E.A., dos Santos, L.E., Sartori Bueno, M., 2007. True digestibility of calcium from sources used in finishing lamb diets. Small Rumin. Res. 71, 243–249. Russel, A.J.F., Doney, J.M., Gunn, R.J., 1969. Subjective assessment of body fat in live sheep. J. Agric. Sci. 72, 451–454. Schlumbohm, C., Sporleder, H.P., Gurtler, H., Harmeyer, J., 1997. The influence of insulin on metabolism of glucose, free fatty acids and glycerol in normo- and hypocalcaemic ewes during different reproductive states. Deutsch. Tierärztl. Wochenschr. 104, 359–365. Thimonier, J., Cognié, Y., Lassoued, N., Khaldi, G., 2000. L’effet mâle chez les ovins: une technique actuelle de maîtrise de la reproduction (The ram effect: an up-to-date method for the control of oestrus and ovulation in sheep). Prod. Anim. 13, 223–231. Van Soest, P.J., Robertson, J.B., Lewis, B.-A., 1991. Methods for dietary fibre, neutral detergent fibre, and nonstarch carbohydrates in relation to animal nutrition. J. Dairy Sci. 74, 3583–3597.