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Milk production and composition in reindeer (Rangifer tarandus): effect of lactational stage
Comparative Biochemistry and Physiology Part A 137 (2004) 649–656
Milk production and composition in reindeer (Rangifer tarandus): effect of lactational stage Hallvard Gjøstein*, Øystein Holand, Robert B. Weladji ˚ Norway Department of Animal Science, Agricultural University of Norway, P.O. Box 5025, N-1432 As, Received 13 August 2003; received in revised form 24 November 2003; accepted 6 January 2004
Abstract Milk yield and composition of major milk constituents were measured in captive, nursing reindeer. Registration of milk production was performed during two successive lactations (2001 and 2002). The milk yield was significantly affected by week of lactation (P-0.001) and by individual (P-0.001). The lactation curve had an asymmetrical peak 3 weeks postpartum and the milk yield at peak lactation was 983 gyday (range 595–1239). The length of lactation varied from 24 to 26 weeks and average total milk production was 99.5 kg. From peak lactation the milk production decreased linearly (P-0.001) until milk production was terminated. Mean values for content of major milk constituents were 15.5% fat, 9.9% protein and 2.5% lactose. The content of fat and protein increased markedly with the lactation stage (P-0.001), while lactose showed a slight decrease (P-0.001). The milk composition was significantly affected by stage of lactation (P-0.001). There was a marginally significant decrease in protein:fat ratio (Ps0.06) as protein was substituted by fat with stage of lactation. The caloric value of the milk averaged 8.7 kJyg and increased significantly with the stage of lactation (P-0.001). The overall increase in milk gross energy content during lactation was 67.6%. The energy output averaged 7996 kJyday at peak lactation and decreased significantly during the course of lactation (Ps0.002). 䊚 2004 Elsevier Inc. All rights reserved. Keywords: Lactation; Milk composition; Milk production; Rangifer tarandus; Reindeer
1. Introduction Lactation is the major energetic component of maternal investment in mammals (Sadleir, 1984), implying biological constraints and trade-offs influencing milk yield and chemical composition (Luick et al., 1974; Loudon and Kay, 1984; White and Luick, 1984; Landete-Castillejos et al., 2000) as well as reproductive (Clutton-Brock et al., 1989) and behavioural traits (Martin, 1984; Lavigueur and Barrette, 1992). Hence, knowledge of *Corresponding author. Tel.: q47-64948078; fax: q4764947960. E-mail address: [email protected] (H. Gjøstein).
milk production and composition is important when comparing different lactational strategies and levels of maternal effort in mammals (Oftedal, 1984). Reindeerycaribou (Rangifer tarandus) has a ‘follower’ type mother–young relationship characterised by great seasonal mobility (Geist, 1999). Calving occurs at the end of the northern winter and the lactation period usually terminates during the rutting season in October (Holand et al., 2002b). Reindeerycaribou have evolved in a harsh environment with a short summer season, indicating a rapid and affluent transmission of energy and protein from the mother to the calf to optimize
1095-6433/04/$ - see front matter 䊚 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.cbpb.2004.01.002
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lifetime reproductive success, typical for capital ¨ breeders (Jonsson, 1997). Calves are precocious and dependent on an adequate supply of maternal milk until rumen function is developed and while plants are partly encased in snow (Luick et al., 1974). Most of the pre-weaning mortality in cervids occurs within 1 month of birth (see review by Gaillard et al., 2000) and high intake of energy and protein during early lactation favours survival. The calves given an adequate nutritional supply during the first weeks are able to take advantage of the lush green summer vegetation at an early stage and the females are released earlier from the burden of lactation and can start their build up of reserves toward the next reproductive cycle. Rapid growth and fat deposition in neonates are also crucial for reaching a body mass in autumn, enabling the calves to survive the harsh winter. Reindeer milk has a high content of milk solids compared to other ungulates and undergoes great compositional changes during a relatively short lactation cycle (Luick et al., 1974; Robbins et al., 1987). Furthermore, the selective advantage of producing concentrated milk in reindeer is argued to be different from ‘hider’-species, presumably as a result of requirements for locomotion and predator avoidance, as well as thermoregulatory requirements of the young (White and Luick, 1984). Peak lactation in reindeer is reported to occur within 3–4 weeks postpartum followed by a gradual decline in production until weaning (White and Luick, 1984). The highly concentrated milk becomes more concentrated during late lactation because of an increase in fat and protein content, and it is suggested that the increase in milk solids partially compensate for declining rate of milk intake during late lactation (Luick et al., 1974). However, little information exists about the variability of milk composition in reindeer in relation to the milk production and hence the energetic consequences of lactation during different stages of lactation. In this article, we provide milk yield and composition from does nursing young during the lactation period. We further investigate the variation in the over time of milk production and milk composition during lactation. 2. Material and methods 2.1. Data collection Semi-domesticated reindeer of the experimental herd of Agricultural University of Norway were
used in the study. Registration of milk production was performed during two successive lactations (2001 and 2002). The animals were accustomed to machine milking. Animals were transferred from their winter range to the enclosures of the University 3 weeks postpartum in 2001 and were kept there until the end of the experiment in November 2002. Five and 6 does with calves were studied in 2001 and 2002, respectively. Four of the does were used in both years of the study. The animals were held in a 0.4 ha pen and had free access to water, hay and pelleted concentrate (Formel Favour 20, Felleskjøpet, containing 16.2% crude protein). Does were weighed at the end of May and August. Calves were weighed within 3 days from birth and then weekly until week 27 postpartum. The dominance among does was established by registration of agonistic interactions (Thomson, 1977). The dominance data were organised into a dominance hierarchy by the aid of the socio-behavioural data program, MatMan 1.0 for Windows (Noldus Information Technology, 1998). The daily milk production was estimated using timed milking, where milk production is measured during a period where the calf is separated from the mother (Oftedal, 1985). At the start of each separation interval, the does were milked to empty the udder. At the end, the does were milked again and the milk yield was measured. The milkings were carried out after an intramuscular injection of 10 IU of oxytocin to secure a complete emptying of the udder. The length of the separation interval was kept short in early stage of lactation, when the production rate is high, and was increased through the lactation. The time-interval does were separated from calves was 3 h in May, 4 h in June, 6 h in July–August and 8 h in September–October. From June to September the separation interval did not differ from the natural suckling frequency of does and calves (H. Gjøstein, Ø. Holand, R. Weladji, unpublished data). Daily milk production was calculated based on the milk secretion during the separation interval. Milk production was measured twice a week, from which an average daily milk production was estimated. The measurement of milk production started in week 3 and week 2 postpartum in 2001 and 2002, respectively. The milking equipment used was a specifically designed cluster with teat cups fitted to the reindeer udder, developed by SAC (S.A. Christensen & Co., Kolding, Denmark). The milking machine
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Table 1 Interannual comparison of means for mass (kg), age (years) and calving dates (days from 1 April) of the experimental animals (Rangifer tarandus) Year 2001 Body mass May Body mass August Age Calving day
66.8"2.6 78.7"1.9 4.6"1.0 35.8"5.8
2002 (5) (5) (5) (5)
78.1"2.6 82.5"1.7 5.3"0.9 47.0"5.3
(5) (6) (6) (6)
tsy3.10, tsy1.61, tsy0.94, tsy1.43,
d.f.s9, Ps0.02 d.f.s10, Ps0.14 d.f.s10, Ps0.37 d.f.s10, Ps0.18
Estimates "S.E.M. are provided and the sample size is given in brackets.
was set up to 40:60 massageymilking ratio, 100 pulsationsymin and 28 kPa vacuum. Milk samples were frozen immediately and stored at y20 8C until analysed. Milk samples from the lactation period of 2001 were analysed at the Department of Dairy Science, Agricultural University of Norway, for fat (Gerber), total protein (micro-Kjeldahl) and lactose (HPLC). Total milk yield was computed multiplying the midpoint between yields of consecutive weeks by the number of days between them and then adding the results for all trials (Landete-Castillejos et al., 2001). Production of fat, protein and lactose at different lactation stages was calculated multiplying the percent of nutrients with the milk yield during each stage. The gross energy content in the milk was calculated using the formula developed by Perrin (1958): Gross energy (kcalyg)sw(9.11=fat)q (5.86=true protein)q(3.95=sugar)q7.4= NPN)x%100. Taking into account the milk yield, the energy output during different stages of lactation was calculated. 2.2. Statistical analysis Descriptive statistics were used to present characteristics of the animals involved in the experiments (females and calves), while t-tests were performed to investigate differences between the 2 years in the reported characteristic. We used a linear model to test the effect of ‘year’ on milk yield, but also to generate means by ‘week’ for milk yield, fat, lactose, protein, protein:fat ratio, gross energy content and energy output. Variation in milk yield and milk composition (i.e. lactose, fat, protein, protein:fat ratio, milk energy, energy output) was analysed by mixed linear model with both fixed and random effects (Littell et al., 1996), using the Mixed procedure in SAS, version 8.01 (1999), with a 5% significance level. Due to the
repeated measurement on each female during the course of lactation, ‘female identity’ was fitted as a random effect in the models. Predictor variable was mainly ‘week’, but in the case of milk yield, we also controlled one after another for female mass, female age and female dominance rank. Due to the sexual size dimorphism in reindeer, calf sex was also entered as a covariate in our models. Data on milk composition were not available for all weeks and we used the available analyses to represent different stages of lactation. All variables except ‘calf sex’ and ‘female identity’ were continuous and all analyses were performed using SAS (1999). 3. Results 3.1. Characteristics of the experimental flocks Females involved in the experiment were on average heavier in May 2002 than in May 2001 (Table 1), and there was no significant difference in August mass, age or calving date (Table 1). On average, female mass gain from May to August was higher in 2001 as compared to 2002 (respectively, 11.9 and 4.6 kg; ts2.52; Ps0.036, d.f.s 8; see also Table 1). Average weekly gain in body mass of calves during the lactation period was 2.39 kg S.E.M."0.56 in 2001 and 1.61 kg S.E.M."0.43 in 2002 and did not differ between years (F1, 33s1.24, P)0.3; Fig. 1). 3.2. Milk production Weekly milk yield did not vary significantly between years (F1, 222s0.55, P)0.1), justifying that in further analyses; data from both years could be pooled. Milk yield varied significantly between weeks (F1, 222s403.84, P-0.001; regression coefficient"S.E.M. y35.45"1.76). The lactation
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milk production was only weakly explained by age (F1, 204s3.29, Ps0.07), and replacing the variable ‘mother age’ by either female body mass in May or female dominance rank did not yield significant results (mass of mother: F1, 204s1.23, P)0.1; female dominance rank: F1, 132s0.03, P) 0.1). 3.3. Milk composition
Fig. 1. Means of body mass of reindeer calves (Rangifer tarandus) at different weeks postpartum in 2001 (ns5) and 2002 (ns6).
curve had an asymmetrical peak in the third week of lactation where the does on average produced 983 gyday (range 595–1239; Fig. 2). From peak lactation there was a negative linear relationship between milk production and week of lactation (rsy0.98, P-0.001). Including a quadratic term for the variable ‘week’ did not yield significant results (P)0.1). Total milk production during lactation was 99.5 kg and lactation length varied from 24 to 26 weeks. Milk production varied significantly among individuals (F6, 223s3.17, Ps0.005). However, the variation in the weekly
Fat content averaged 15.5% (gy100 g) over the lactation period (Table 2) and increased significantly with stage of lactation (F1, 23s51.56, P0.001; regression coefficient"S.E.M. 0.41"0.06). The fat content increased from 11.4% in week 3 to 21.5% in week 24. Mean protein content was 9.9% (Table 2) and increased significantly with stage of lactation (F1, 23s68.01, P-0.001; regression coefficient"S.E.M. 0.19"0.02). Protein content increased from 7.7% in week 3 to 12.2% in week 24. Contrary to fat and protein, lactose decreased significantly with week of lactation (F1, 23s212.42, P-0.001; regression coefficient"S.E.M. y0.11"0.01) and averaged 2.5% over the lactation period. The decrease in lactose content was from 3.6% in week 3 to 1.2% in week 24. Corrected for lactational stage, there were no significant differences among females (P)0.05) regarding content of fat, protein or lactose in milk. There was a marginally significant decrease in
Fig. 2. Mean milk production (gyday) and total energy output (kJyday) during lactation in reindeer (Rangifer tarandus). The milk production data are based on mean values from both years of the study.
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protein:fat ratio with stage of lactation (F1, 22s 3.94, Ps0.06; regression coefficient"S.E.M. y 0.005"0.003) as protein was substituted by fat throughout the lactation period. There was a negative correlation between stage of lactation and total production of fat (rsy0.97, P-0.001), protein (rsy0.97, P-0.001) and lactose (rsy 0.95, P-0.001; see Fig. 3). The gross energy content in the milk increased significantly with the stage of lactation (F1, 22s66.62, P-0.001; regression coefficient"S.E.M. 0.18"0.02; Table 2). The overall increase in gross energy content was 67.6%. The energy output decreased significantly during the course of lactation (F1, 22s12.00, Ps0.002; regression coefficient"S.E.M. y168.72"48.70; see also Table 2 and Fig. 2).
Fig. 3. Daily production (gyday) of the major milk constituents at different stages of lactation in reindeer (Rangifer tarandus).
mann et al., 1975; White and Luick, 1976, 1984; Parker et al., 1990; Chan-McLeod et al., 1994) have been carried out using accurate isotope tracer techniques. However, this method is elaborate and hence lactation curves of reindeer have been based on measures of milk yield during a few selected stages during the lactation period. Machine milking is, when using trained animals, an accurate and labour-saving method of assessing milk production. To obtain valid milk secretion estimates by the timed milking method, the secretion rates must be unaffected by the separation interval and repeated milking and comparable and relative complete evacuation of the mammary gland must be accomplished. Furthermore, the milk volumes obtained by timed milking has to be representative of what the offspring consume (Oftedal, 1985). To satisfy the conditions necessary for the procedure, the separation interval was kept close to the natural suckling frequency of the young in this experi-
4. Discussion 4.1. Change in doe body mass and calf growth The average mass gain in does from May to August was higher in 2001 than in 2002 probably because the latter were fed concentrate during winter 2001y2002. Hence, the females had higher body reserves in spring 2002, as indicated by their higher body mass in May, and showed a lower mass gain during summer. The calves had similar growth patterns during both years, most likely because they were fed ad lib in both years. This explains why the condition of the calves was not related to maternal effort. 4.2. Milk yield Most studies of milk production in reindeer and caribou (McEvan and Whitehead, 1971; Holle-
Table 2 Milk composition (gy100 g) of fat, protein, lactose, protein:fat ratio, gross energy content (kJyg) and total energy output (kJyday) during lactation in reindeer (Rangifer tarandus) Week of lactation
N
3 6 8 12 17 20 24
3 4 5 5 4 4 3
Average Data are mean"S.E.M.
Composition Fat
Protein
Lactose
Protein:fat
Gross energy
Total energy
11.4"1.2 12.4"1.0 13.8"1.2 15.3"0.4 16.6"1.1 17.4"0.9 21.5"1.7
7.7"0.4 8.8"0.5 9.0"0.3 10.3"0.5 10.5"0.5 11.1"0.9 12.2"0.1
3.6"0.1 3.1"0.2 3.0"0.1 2.5"0.1 2.2"0.0 1.7"0.2 1.2"0.2
0.69"0.1 0.72"0.1 0.67"0.1 0.68"0.0 0.64"0.0 0.63"0.0 0.57"0.1
6.8"0.4 7.4"0.3 8.0"0.4 8.8"0.2 9.1"0.5 9.6"0.5 11.4"0.6
7996"820 5682"400 5041"758 4465"817 4457"821 3668"338 3321"2053
15.5
9.9
2.5
0.66
8.7
4947
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ment. A parallel study of the suckling behaviour using the same animals provided accurate data on the suckling frequency (H. Gjøstein, Ø. Holand, R. Weladji, unpublished data). Furthermore, milking was performed by the aid of exogenous administration of oxytocin. Variation in nutritional state may have a great effect on milk production (Lee et al., 1991; Landete-Castillejos et al., 2002, 2003), and milk yield at peak lactation may be markedly reduced during years with poor pastures (White and Luick, 1984). The impact of different quality pastures on milk production is also reported in red deer, Cervus elaphus (Loudon and Kay, 1984). In our study, the animals were in a good nutritional state and fed concentrate and hay ad libitum during the lactation period. This suggests that the feeding regime practised and the female body condition was unlikely to be a limiting factor for milk production in the experiment. The shape of the lactation curve (Fig. 1) agrees with a typical mammalian curve with a peak during week 2 to week 4 (Robbins et al., 1987). The peak lactation yield was lower than the 1590 g reported by McEvan and Whitehead (1971), and the 1792 g by Parker et al. (1990). This difference might partly be due to larger body mass of the animals in their studies. The estimated total milk yield during lactation was 99.5 kg, which is lower than the estimate (118 kg) of Oftedal (1985) based on data presented by White and Luick (1984). However, the total milk yield in the present study was higher than milk yields of does on a low level of nutrition (Oftedal, 1985), which equalled 57 kg. 4.3. Milk composition Our findings agree with both Luick et al. (1974) and Holand et al. (2002a), with an increase in fat and protein content as lactation progressed. A similar trend is reported in red deer (Loudon and Kay, 1984), Iberian red deer (Landete-Castillejos et al., 2000), moose, (Reese and Robbins, 1994), and for ungulates in general (Oftedal, 1984, 1985; Robbins et al., 1987). In the present study, both fat and protein content increased from week 3 and throughout the lactation while lactose content decreased. The rise in content of protein and fat during lactation is more pronounced in reindeer than in red deer species and the latter does not undergo a decrease in lactose content as lactation
proceeds (Robbins et al., 1987). However, decline in lactose content is reported in black-tailed deer (Mueller and Sadleir, 1977). In reindeer, lactose content has been reported to decrease by 20% during the lactation cycle (White and Luick, 1984), compared to 66.1% in our study. Lactose is suggested to be the most osmotically active component and to function as a regulator of the water content in milk (Rook and Wheelock, 1967). Increased concentration of osmotically active salt may have compensated for the decrease in the lactose content, as suggested by Jennes and Sloan (1970). Increased content of ash during lactation is reported by Luick et al. (1974) and Aikio et al. (2000). Furthermore, it seems unlikely that the use of exogenous oxytocin administration has influenced the milk composition as Holand et al. (2002a) found no difference in milk composition between does milked with and without exogenous oxytocin administration. As reviewed by Laben (1963) several factors influence the milk composition including age, stage of lactation, gestation, disease, nutrition as well as inherited factors. Stage of lactation had a highly significant effect on milk composition as reported in various species (Oftedal, 1984). The age of does did not significantly influence milk composition in our results, nor did body mass or dominance rank. However, this could be related to small sample size in our study. As mentioned above nutrition affects both milk yield and milk composition (Sutton, 1989). Hence, we must assume that the feeding regime affected milk composition in the present study (Landete-Castillejos et al., 2003). However, it is reasonable to assume that the changes in milk composition during the course of lactation also are a result of the lactational stage, as it occurs in red deer (Loudon and Kay, 1984; Landete-Castillejos et al., 2000) and in bovine milk (Auldist et al., 1998). The ratio of protein to fat decreased during the course of lactation (see Table 2), which also is reported for Iberian red deer (Landete-Castillejos et al., 2000). This is probably due to high protein demand for growth in precocial calves during early stage of life, as muscles are developed earlier than fat tissues (Hammond, 1961). Fat deposition to meet the harsh winter probably becomes more important as lactation progresses (Landete-Castillejos et al., 2000; Holand et al., 2002a). In contrast, stage of lactation had no effect on protein:fat ratio in bovine milk (Auldist et al., 1998). Although
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the content of fat and protein increased in the milk with stage of lactation, the total production of fat and protein decreased as a result of the decline in milk yield (Fig. 3). The gross energy content in milk (kJyg) increased 66.7% throughout the lactation compared to 51% in the study of Luick et al. (1974). The energy output at peak lactation was 7996"820 kJyday and comparable to the interspecific regression of ungulates with single young (Oftedal, 1984, 1985). From peak lactation, the energy output decreased markedly whereas from midlactation (week 12, Fig. 1) the energy output declined at a slower rate than the milk yield. The same trend has been reported in caribou while in muskox the energy output declines at the same rate as milk yield (Parker et al., 1990). Lack of comparative data on energy output during different lactational stages makes inter-species comparisons within wild ungulates difficult. For northern ungulates the development of a viable calf during the short summer is crucial. To survive the artic winter, reindeer have to endure climatic stress and limited food access in time and space (see, e.g. Weladji and Holand, 2003). The high protein and energy content in the milk probably represent an optimum to meet both the growth and energy requirements of the calf. However, the transfer (or production) of milk should be traded against own requirements to replenish body reserves to secure own survival and future reproductions (Trivers, 1974). Replenishment of maternal body reserves favours a short peak of lactation early in the summer (White and Luick, 1976; Holand et al., 2002b). Hence, it is in the mother’s interest to provide an affluent supply of nutrients in early lactation to maximize calf growth and secure calf survival during the early phase of life, and then restrict the milk transfer to encourage the calf to evolve the ability to achieve solid food on its own. Acknowledgments This research was supported by the Norwegian Research Council. References Aikio, P., Nieminen, M., Holand, Ø., Mossing, T., Alatossava, ¨ med mjolking ¨ T., Malinen, H.L., 2000. Forsok av vajor. Prosjektrapport Interreg. Sapmi. 54.
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Auldist, M.J., Wals, B.J., Thomsom, N.A., 1998. Seasonal and lactational influences on bovine milk in New Zealand. J. Dairy Res. 65, 401–411. Chan-McLeod, A.C.A., White, R.G., Holleman, D.F., 1994. Effects of protein energy intake, body condition, and season on nutrient partitioning and milk production in reindeer and caribou. Can. J. Zool. 72, 938–947. Clutton-Brock, T.H., Albon, S.D., Guiness, F.E., 1989. Fitness cost of gestation and lactation in wild mammals. Nature 337, 260–262. Gaillard, J.M., Festa-Bianchet, M., Yoccoz, N.G., Loison, A., ¨ Toıgo, C., 2000. Temporal variation in fitness components and population dynamics of large herbivores. Ann. Rev. Ecol. Syst. 31, 367–393. Geist, W., 1999. Reindeer and caribou. Deer of the World. Swan Hill Press, Shrewsbury, pp. 315–337. Hammond, J., 1961. Growth in size and body proportions in farm animals. In: Zarrow, M.X. (Ed.), Growth in Living Systems. Basoe Books, New York. Holand, Ø., Aikio, P., Gjøstein, H., Nieminen, M., Hove, K., White, R.G., 2002a. Modern reindeer farming—the influence on different milking regimes on udder health, milk yield and composition. Small Rum. Res. 44, 65–73. Holand, Ø., Gjøstein, H., Aikio, P., Nieminen, M., White, R.G., 2002b. Traditional reindeer milking and prospects of developing reindeer farming as a niche based production. Encycl. Dairy Sci. 637–643. Hollemann, D.F., White, R.G., Luick, J.R., 1975. New isotope method for estimating milk intake and yield. J. Dairy Sci. 58, 1814–1821. Jennes, R., Sloan, R.E., 1970. The composition of milks of various species: a comparative review. Dairy Sci. Abstr. 32, 599–612. ¨ Jonsson, K.I., 1997. Capital and income breeding as alternative tactics of resource use in reproduction. Oikos 78, 57–66. Laben, B.L., 1963. Factors responsible for variation in milk composition. J. Dairy Sci. 46, 1293–1301. Landete-Castillejos, T., Garcia, A., Gomez, J.A., Gallego, L., 2003. Lactation under food constraints in Iberian red deer (Cervus elaphus hispanicus). Wildl. Biol. 9, 131–139. Landete-Castillejos, T., Garcia, A., Gomez, J.A., Laborda, J., Gallego, L., 2002. Effect of nutritional stress during lactation on immunity costs and indices of future reproduction in Iberian red deer (Cervus elaphus hispanicus). Biol. Reprod. 67, 1613–1620. Landete-Castillejos, T., Garcia, A., Molina, P., Vergara, J., Garde, J., Gallego, L., 2000. Milk production and composition in captive Iberian red deer (Cervus elaphus hispanicus): effect of birth date. J. Anim. Sci. 78, 2771–2777. Landete-Castillejos, T., Garcia, A., Gallego, L., 2001. Calf growth in captive Iberian red deer (Cervus elaphus hispanicus): effects of birth date and hind milk production and composition. J. Anim. Sci. 79, 1085–1092. Lavigueur, L., Barrette, C., 1992. Suckling, weaning and growth in captive woodland caribou. Can. J. Zool. 70, 1753–1766. Lee, P.C., Majluf, P., Gordon, I.J., 1991. Growth, weaning and maternal investment from a comparative perspective. J. Zool. Lond. 225, 99–114. Littell, R.C., Milliken, G.A., Stroup, W.W., Wolfinger, R.D., 1996. SAS System for Mixed Models. SAS Institute Inc, Cary, NC, pp. 633.
656
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Loudon, A.S.I., Kay, R.N.B., 1984. Lactational constraints on a seasonally breeding mammal: the red deer. Symp. Zool. Soc. Lond. (51) 233–252. Luick, J.R., White, R.G., Gau, A.M., Jennes, R., 1974. Compositional changes in the milk secreted by grazing reindeer. I. Gross composition and ash. J. Dairy Sci. 57, 1325–1333. Martin, P., 1984. The meaning of weaning. Anim. Behav. 32, 1257–1258. McEvan, E.H., Whitehead, P.E., 1971. Measurement of the milk intake of reindeer and caribou calves using tritiated water. Can. J. Zool. 49, 443–447. Mueller, C.C., Sadleir, R.M.F.S., 1977. Changes in the nutrient composition of black-tailed deer during lactation. J. Mammal. 58, 421–423. Noldus Information Technology, 1998. Reference Manual MatMan 1.0 for Windows. Wageningen, Netherlands, 91 p. Oftedal, O.T., 1984. Milk composition, milk yield and energy output at peak lactation: a comparative review. Symp. Zool. Soc. Lond. 51, 33–85. Oftedal, O.T., 1985. Pregnancy and lactation. In: Hudson, R.J., White, R.G. (Eds.), The Bioenergetics of Wild Herbivores. CRC Press, Boca Raton, FL, pp. 215–238. Parker, K.L., White, R.G., Gillingham, M.P., Holleman, D.F., 1990. Comparison of energy metabolism in relation to daily activity and milk consumption by caribou and muskox neonates. Can. J. Zool. 68, 106–114. Perrin, D.R., 1958. The caloric value of milk in different species. J. Dairy Res. 25, 215–220.
Reese, E.O., Robbins, C.T., 1994. Characteristics of moose lactation and neonatal growth. Can. J. Zool. 72, 953–957. Robbins, C.T., Oftedal, O.T, O’Rourke, K.I., 1987. Lactation, early nutrition and hand-rearing of wild ungulates, with special reference to deer. In: Wemmer, C.M. (Ed.), Biology and Management of the Cervidae: A Conference held at the Conservation and Research Centre. Smithsonian Inst. Press, National Zoological Park, Washington DC, pp. 429–442. Rook, J.A.F., Wheelock, J.V., 1967. The secretion of water and of water-soluble constituents in milk. J. Dairy Res. 34, 273–287. Sadleir, P.M.F.S., 1984. Ecological consequences of lactation. Acta Zool. Fenn. 171, 179–182. SAS Inc, 1999. The SAS system for Windows, version 8.01. SAS Inc, Cary, NC. Sutton, J.D., 1989. Altering milk composition by feeding. J. Dairy Sci. 72, 2801–2814. Thomson, B.R., 1977. The behaviour of wild reindeer in Norway, Ph.D. Thesis, University of Edinburgh, UK. Trivers, R.L., 1974. Parent-offspring conflict. Amer. Zool. 14, 249–264. Weladji, R.B., Holand, Ø., 2003. Global climate change and reindeer: effects of winter weather on the autumn weight and growth of calves, Oecologia: in press. White, R.G., Luick, J.R., 1976. Glucose metabolism in lactating reindeer. Can. J. Zool. 54, 55–64. White, R.G., Luick, J.R., 1984. Plasticity and constraints in the lactational strategy of reindeer and caribou. Symp. Zool. Soc. Lond. 51, 215–232.
Milk production and composition in reindeer (Rangifer tarandus): effect of lactational stage Hallvard Gjøstein*, Øystein Holand, Robert B. Weladji ˚ Norway Department of Animal Science, Agricultural University of Norway, P.O. Box 5025, N-1432 As, Received 13 August 2003; received in revised form 24 November 2003; accepted 6 January 2004
Abstract Milk yield and composition of major milk constituents were measured in captive, nursing reindeer. Registration of milk production was performed during two successive lactations (2001 and 2002). The milk yield was significantly affected by week of lactation (P-0.001) and by individual (P-0.001). The lactation curve had an asymmetrical peak 3 weeks postpartum and the milk yield at peak lactation was 983 gyday (range 595–1239). The length of lactation varied from 24 to 26 weeks and average total milk production was 99.5 kg. From peak lactation the milk production decreased linearly (P-0.001) until milk production was terminated. Mean values for content of major milk constituents were 15.5% fat, 9.9% protein and 2.5% lactose. The content of fat and protein increased markedly with the lactation stage (P-0.001), while lactose showed a slight decrease (P-0.001). The milk composition was significantly affected by stage of lactation (P-0.001). There was a marginally significant decrease in protein:fat ratio (Ps0.06) as protein was substituted by fat with stage of lactation. The caloric value of the milk averaged 8.7 kJyg and increased significantly with the stage of lactation (P-0.001). The overall increase in milk gross energy content during lactation was 67.6%. The energy output averaged 7996 kJyday at peak lactation and decreased significantly during the course of lactation (Ps0.002). 䊚 2004 Elsevier Inc. All rights reserved. Keywords: Lactation; Milk composition; Milk production; Rangifer tarandus; Reindeer
1. Introduction Lactation is the major energetic component of maternal investment in mammals (Sadleir, 1984), implying biological constraints and trade-offs influencing milk yield and chemical composition (Luick et al., 1974; Loudon and Kay, 1984; White and Luick, 1984; Landete-Castillejos et al., 2000) as well as reproductive (Clutton-Brock et al., 1989) and behavioural traits (Martin, 1984; Lavigueur and Barrette, 1992). Hence, knowledge of *Corresponding author. Tel.: q47-64948078; fax: q4764947960. E-mail address: [email protected] (H. Gjøstein).
milk production and composition is important when comparing different lactational strategies and levels of maternal effort in mammals (Oftedal, 1984). Reindeerycaribou (Rangifer tarandus) has a ‘follower’ type mother–young relationship characterised by great seasonal mobility (Geist, 1999). Calving occurs at the end of the northern winter and the lactation period usually terminates during the rutting season in October (Holand et al., 2002b). Reindeerycaribou have evolved in a harsh environment with a short summer season, indicating a rapid and affluent transmission of energy and protein from the mother to the calf to optimize
1095-6433/04/$ - see front matter 䊚 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.cbpb.2004.01.002
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lifetime reproductive success, typical for capital ¨ breeders (Jonsson, 1997). Calves are precocious and dependent on an adequate supply of maternal milk until rumen function is developed and while plants are partly encased in snow (Luick et al., 1974). Most of the pre-weaning mortality in cervids occurs within 1 month of birth (see review by Gaillard et al., 2000) and high intake of energy and protein during early lactation favours survival. The calves given an adequate nutritional supply during the first weeks are able to take advantage of the lush green summer vegetation at an early stage and the females are released earlier from the burden of lactation and can start their build up of reserves toward the next reproductive cycle. Rapid growth and fat deposition in neonates are also crucial for reaching a body mass in autumn, enabling the calves to survive the harsh winter. Reindeer milk has a high content of milk solids compared to other ungulates and undergoes great compositional changes during a relatively short lactation cycle (Luick et al., 1974; Robbins et al., 1987). Furthermore, the selective advantage of producing concentrated milk in reindeer is argued to be different from ‘hider’-species, presumably as a result of requirements for locomotion and predator avoidance, as well as thermoregulatory requirements of the young (White and Luick, 1984). Peak lactation in reindeer is reported to occur within 3–4 weeks postpartum followed by a gradual decline in production until weaning (White and Luick, 1984). The highly concentrated milk becomes more concentrated during late lactation because of an increase in fat and protein content, and it is suggested that the increase in milk solids partially compensate for declining rate of milk intake during late lactation (Luick et al., 1974). However, little information exists about the variability of milk composition in reindeer in relation to the milk production and hence the energetic consequences of lactation during different stages of lactation. In this article, we provide milk yield and composition from does nursing young during the lactation period. We further investigate the variation in the over time of milk production and milk composition during lactation. 2. Material and methods 2.1. Data collection Semi-domesticated reindeer of the experimental herd of Agricultural University of Norway were
used in the study. Registration of milk production was performed during two successive lactations (2001 and 2002). The animals were accustomed to machine milking. Animals were transferred from their winter range to the enclosures of the University 3 weeks postpartum in 2001 and were kept there until the end of the experiment in November 2002. Five and 6 does with calves were studied in 2001 and 2002, respectively. Four of the does were used in both years of the study. The animals were held in a 0.4 ha pen and had free access to water, hay and pelleted concentrate (Formel Favour 20, Felleskjøpet, containing 16.2% crude protein). Does were weighed at the end of May and August. Calves were weighed within 3 days from birth and then weekly until week 27 postpartum. The dominance among does was established by registration of agonistic interactions (Thomson, 1977). The dominance data were organised into a dominance hierarchy by the aid of the socio-behavioural data program, MatMan 1.0 for Windows (Noldus Information Technology, 1998). The daily milk production was estimated using timed milking, where milk production is measured during a period where the calf is separated from the mother (Oftedal, 1985). At the start of each separation interval, the does were milked to empty the udder. At the end, the does were milked again and the milk yield was measured. The milkings were carried out after an intramuscular injection of 10 IU of oxytocin to secure a complete emptying of the udder. The length of the separation interval was kept short in early stage of lactation, when the production rate is high, and was increased through the lactation. The time-interval does were separated from calves was 3 h in May, 4 h in June, 6 h in July–August and 8 h in September–October. From June to September the separation interval did not differ from the natural suckling frequency of does and calves (H. Gjøstein, Ø. Holand, R. Weladji, unpublished data). Daily milk production was calculated based on the milk secretion during the separation interval. Milk production was measured twice a week, from which an average daily milk production was estimated. The measurement of milk production started in week 3 and week 2 postpartum in 2001 and 2002, respectively. The milking equipment used was a specifically designed cluster with teat cups fitted to the reindeer udder, developed by SAC (S.A. Christensen & Co., Kolding, Denmark). The milking machine
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Table 1 Interannual comparison of means for mass (kg), age (years) and calving dates (days from 1 April) of the experimental animals (Rangifer tarandus) Year 2001 Body mass May Body mass August Age Calving day
66.8"2.6 78.7"1.9 4.6"1.0 35.8"5.8
2002 (5) (5) (5) (5)
78.1"2.6 82.5"1.7 5.3"0.9 47.0"5.3
(5) (6) (6) (6)
tsy3.10, tsy1.61, tsy0.94, tsy1.43,
d.f.s9, Ps0.02 d.f.s10, Ps0.14 d.f.s10, Ps0.37 d.f.s10, Ps0.18
Estimates "S.E.M. are provided and the sample size is given in brackets.
was set up to 40:60 massageymilking ratio, 100 pulsationsymin and 28 kPa vacuum. Milk samples were frozen immediately and stored at y20 8C until analysed. Milk samples from the lactation period of 2001 were analysed at the Department of Dairy Science, Agricultural University of Norway, for fat (Gerber), total protein (micro-Kjeldahl) and lactose (HPLC). Total milk yield was computed multiplying the midpoint between yields of consecutive weeks by the number of days between them and then adding the results for all trials (Landete-Castillejos et al., 2001). Production of fat, protein and lactose at different lactation stages was calculated multiplying the percent of nutrients with the milk yield during each stage. The gross energy content in the milk was calculated using the formula developed by Perrin (1958): Gross energy (kcalyg)sw(9.11=fat)q (5.86=true protein)q(3.95=sugar)q7.4= NPN)x%100. Taking into account the milk yield, the energy output during different stages of lactation was calculated. 2.2. Statistical analysis Descriptive statistics were used to present characteristics of the animals involved in the experiments (females and calves), while t-tests were performed to investigate differences between the 2 years in the reported characteristic. We used a linear model to test the effect of ‘year’ on milk yield, but also to generate means by ‘week’ for milk yield, fat, lactose, protein, protein:fat ratio, gross energy content and energy output. Variation in milk yield and milk composition (i.e. lactose, fat, protein, protein:fat ratio, milk energy, energy output) was analysed by mixed linear model with both fixed and random effects (Littell et al., 1996), using the Mixed procedure in SAS, version 8.01 (1999), with a 5% significance level. Due to the
repeated measurement on each female during the course of lactation, ‘female identity’ was fitted as a random effect in the models. Predictor variable was mainly ‘week’, but in the case of milk yield, we also controlled one after another for female mass, female age and female dominance rank. Due to the sexual size dimorphism in reindeer, calf sex was also entered as a covariate in our models. Data on milk composition were not available for all weeks and we used the available analyses to represent different stages of lactation. All variables except ‘calf sex’ and ‘female identity’ were continuous and all analyses were performed using SAS (1999). 3. Results 3.1. Characteristics of the experimental flocks Females involved in the experiment were on average heavier in May 2002 than in May 2001 (Table 1), and there was no significant difference in August mass, age or calving date (Table 1). On average, female mass gain from May to August was higher in 2001 as compared to 2002 (respectively, 11.9 and 4.6 kg; ts2.52; Ps0.036, d.f.s 8; see also Table 1). Average weekly gain in body mass of calves during the lactation period was 2.39 kg S.E.M."0.56 in 2001 and 1.61 kg S.E.M."0.43 in 2002 and did not differ between years (F1, 33s1.24, P)0.3; Fig. 1). 3.2. Milk production Weekly milk yield did not vary significantly between years (F1, 222s0.55, P)0.1), justifying that in further analyses; data from both years could be pooled. Milk yield varied significantly between weeks (F1, 222s403.84, P-0.001; regression coefficient"S.E.M. y35.45"1.76). The lactation
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milk production was only weakly explained by age (F1, 204s3.29, Ps0.07), and replacing the variable ‘mother age’ by either female body mass in May or female dominance rank did not yield significant results (mass of mother: F1, 204s1.23, P)0.1; female dominance rank: F1, 132s0.03, P) 0.1). 3.3. Milk composition
Fig. 1. Means of body mass of reindeer calves (Rangifer tarandus) at different weeks postpartum in 2001 (ns5) and 2002 (ns6).
curve had an asymmetrical peak in the third week of lactation where the does on average produced 983 gyday (range 595–1239; Fig. 2). From peak lactation there was a negative linear relationship between milk production and week of lactation (rsy0.98, P-0.001). Including a quadratic term for the variable ‘week’ did not yield significant results (P)0.1). Total milk production during lactation was 99.5 kg and lactation length varied from 24 to 26 weeks. Milk production varied significantly among individuals (F6, 223s3.17, Ps0.005). However, the variation in the weekly
Fat content averaged 15.5% (gy100 g) over the lactation period (Table 2) and increased significantly with stage of lactation (F1, 23s51.56, P0.001; regression coefficient"S.E.M. 0.41"0.06). The fat content increased from 11.4% in week 3 to 21.5% in week 24. Mean protein content was 9.9% (Table 2) and increased significantly with stage of lactation (F1, 23s68.01, P-0.001; regression coefficient"S.E.M. 0.19"0.02). Protein content increased from 7.7% in week 3 to 12.2% in week 24. Contrary to fat and protein, lactose decreased significantly with week of lactation (F1, 23s212.42, P-0.001; regression coefficient"S.E.M. y0.11"0.01) and averaged 2.5% over the lactation period. The decrease in lactose content was from 3.6% in week 3 to 1.2% in week 24. Corrected for lactational stage, there were no significant differences among females (P)0.05) regarding content of fat, protein or lactose in milk. There was a marginally significant decrease in
Fig. 2. Mean milk production (gyday) and total energy output (kJyday) during lactation in reindeer (Rangifer tarandus). The milk production data are based on mean values from both years of the study.
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protein:fat ratio with stage of lactation (F1, 22s 3.94, Ps0.06; regression coefficient"S.E.M. y 0.005"0.003) as protein was substituted by fat throughout the lactation period. There was a negative correlation between stage of lactation and total production of fat (rsy0.97, P-0.001), protein (rsy0.97, P-0.001) and lactose (rsy 0.95, P-0.001; see Fig. 3). The gross energy content in the milk increased significantly with the stage of lactation (F1, 22s66.62, P-0.001; regression coefficient"S.E.M. 0.18"0.02; Table 2). The overall increase in gross energy content was 67.6%. The energy output decreased significantly during the course of lactation (F1, 22s12.00, Ps0.002; regression coefficient"S.E.M. y168.72"48.70; see also Table 2 and Fig. 2).
Fig. 3. Daily production (gyday) of the major milk constituents at different stages of lactation in reindeer (Rangifer tarandus).
mann et al., 1975; White and Luick, 1976, 1984; Parker et al., 1990; Chan-McLeod et al., 1994) have been carried out using accurate isotope tracer techniques. However, this method is elaborate and hence lactation curves of reindeer have been based on measures of milk yield during a few selected stages during the lactation period. Machine milking is, when using trained animals, an accurate and labour-saving method of assessing milk production. To obtain valid milk secretion estimates by the timed milking method, the secretion rates must be unaffected by the separation interval and repeated milking and comparable and relative complete evacuation of the mammary gland must be accomplished. Furthermore, the milk volumes obtained by timed milking has to be representative of what the offspring consume (Oftedal, 1985). To satisfy the conditions necessary for the procedure, the separation interval was kept close to the natural suckling frequency of the young in this experi-
4. Discussion 4.1. Change in doe body mass and calf growth The average mass gain in does from May to August was higher in 2001 than in 2002 probably because the latter were fed concentrate during winter 2001y2002. Hence, the females had higher body reserves in spring 2002, as indicated by their higher body mass in May, and showed a lower mass gain during summer. The calves had similar growth patterns during both years, most likely because they were fed ad lib in both years. This explains why the condition of the calves was not related to maternal effort. 4.2. Milk yield Most studies of milk production in reindeer and caribou (McEvan and Whitehead, 1971; Holle-
Table 2 Milk composition (gy100 g) of fat, protein, lactose, protein:fat ratio, gross energy content (kJyg) and total energy output (kJyday) during lactation in reindeer (Rangifer tarandus) Week of lactation
N
3 6 8 12 17 20 24
3 4 5 5 4 4 3
Average Data are mean"S.E.M.
Composition Fat
Protein
Lactose
Protein:fat
Gross energy
Total energy
11.4"1.2 12.4"1.0 13.8"1.2 15.3"0.4 16.6"1.1 17.4"0.9 21.5"1.7
7.7"0.4 8.8"0.5 9.0"0.3 10.3"0.5 10.5"0.5 11.1"0.9 12.2"0.1
3.6"0.1 3.1"0.2 3.0"0.1 2.5"0.1 2.2"0.0 1.7"0.2 1.2"0.2
0.69"0.1 0.72"0.1 0.67"0.1 0.68"0.0 0.64"0.0 0.63"0.0 0.57"0.1
6.8"0.4 7.4"0.3 8.0"0.4 8.8"0.2 9.1"0.5 9.6"0.5 11.4"0.6
7996"820 5682"400 5041"758 4465"817 4457"821 3668"338 3321"2053
15.5
9.9
2.5
0.66
8.7
4947
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ment. A parallel study of the suckling behaviour using the same animals provided accurate data on the suckling frequency (H. Gjøstein, Ø. Holand, R. Weladji, unpublished data). Furthermore, milking was performed by the aid of exogenous administration of oxytocin. Variation in nutritional state may have a great effect on milk production (Lee et al., 1991; Landete-Castillejos et al., 2002, 2003), and milk yield at peak lactation may be markedly reduced during years with poor pastures (White and Luick, 1984). The impact of different quality pastures on milk production is also reported in red deer, Cervus elaphus (Loudon and Kay, 1984). In our study, the animals were in a good nutritional state and fed concentrate and hay ad libitum during the lactation period. This suggests that the feeding regime practised and the female body condition was unlikely to be a limiting factor for milk production in the experiment. The shape of the lactation curve (Fig. 1) agrees with a typical mammalian curve with a peak during week 2 to week 4 (Robbins et al., 1987). The peak lactation yield was lower than the 1590 g reported by McEvan and Whitehead (1971), and the 1792 g by Parker et al. (1990). This difference might partly be due to larger body mass of the animals in their studies. The estimated total milk yield during lactation was 99.5 kg, which is lower than the estimate (118 kg) of Oftedal (1985) based on data presented by White and Luick (1984). However, the total milk yield in the present study was higher than milk yields of does on a low level of nutrition (Oftedal, 1985), which equalled 57 kg. 4.3. Milk composition Our findings agree with both Luick et al. (1974) and Holand et al. (2002a), with an increase in fat and protein content as lactation progressed. A similar trend is reported in red deer (Loudon and Kay, 1984), Iberian red deer (Landete-Castillejos et al., 2000), moose, (Reese and Robbins, 1994), and for ungulates in general (Oftedal, 1984, 1985; Robbins et al., 1987). In the present study, both fat and protein content increased from week 3 and throughout the lactation while lactose content decreased. The rise in content of protein and fat during lactation is more pronounced in reindeer than in red deer species and the latter does not undergo a decrease in lactose content as lactation
proceeds (Robbins et al., 1987). However, decline in lactose content is reported in black-tailed deer (Mueller and Sadleir, 1977). In reindeer, lactose content has been reported to decrease by 20% during the lactation cycle (White and Luick, 1984), compared to 66.1% in our study. Lactose is suggested to be the most osmotically active component and to function as a regulator of the water content in milk (Rook and Wheelock, 1967). Increased concentration of osmotically active salt may have compensated for the decrease in the lactose content, as suggested by Jennes and Sloan (1970). Increased content of ash during lactation is reported by Luick et al. (1974) and Aikio et al. (2000). Furthermore, it seems unlikely that the use of exogenous oxytocin administration has influenced the milk composition as Holand et al. (2002a) found no difference in milk composition between does milked with and without exogenous oxytocin administration. As reviewed by Laben (1963) several factors influence the milk composition including age, stage of lactation, gestation, disease, nutrition as well as inherited factors. Stage of lactation had a highly significant effect on milk composition as reported in various species (Oftedal, 1984). The age of does did not significantly influence milk composition in our results, nor did body mass or dominance rank. However, this could be related to small sample size in our study. As mentioned above nutrition affects both milk yield and milk composition (Sutton, 1989). Hence, we must assume that the feeding regime affected milk composition in the present study (Landete-Castillejos et al., 2003). However, it is reasonable to assume that the changes in milk composition during the course of lactation also are a result of the lactational stage, as it occurs in red deer (Loudon and Kay, 1984; Landete-Castillejos et al., 2000) and in bovine milk (Auldist et al., 1998). The ratio of protein to fat decreased during the course of lactation (see Table 2), which also is reported for Iberian red deer (Landete-Castillejos et al., 2000). This is probably due to high protein demand for growth in precocial calves during early stage of life, as muscles are developed earlier than fat tissues (Hammond, 1961). Fat deposition to meet the harsh winter probably becomes more important as lactation progresses (Landete-Castillejos et al., 2000; Holand et al., 2002a). In contrast, stage of lactation had no effect on protein:fat ratio in bovine milk (Auldist et al., 1998). Although
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the content of fat and protein increased in the milk with stage of lactation, the total production of fat and protein decreased as a result of the decline in milk yield (Fig. 3). The gross energy content in milk (kJyg) increased 66.7% throughout the lactation compared to 51% in the study of Luick et al. (1974). The energy output at peak lactation was 7996"820 kJyday and comparable to the interspecific regression of ungulates with single young (Oftedal, 1984, 1985). From peak lactation, the energy output decreased markedly whereas from midlactation (week 12, Fig. 1) the energy output declined at a slower rate than the milk yield. The same trend has been reported in caribou while in muskox the energy output declines at the same rate as milk yield (Parker et al., 1990). Lack of comparative data on energy output during different lactational stages makes inter-species comparisons within wild ungulates difficult. For northern ungulates the development of a viable calf during the short summer is crucial. To survive the artic winter, reindeer have to endure climatic stress and limited food access in time and space (see, e.g. Weladji and Holand, 2003). The high protein and energy content in the milk probably represent an optimum to meet both the growth and energy requirements of the calf. However, the transfer (or production) of milk should be traded against own requirements to replenish body reserves to secure own survival and future reproductions (Trivers, 1974). Replenishment of maternal body reserves favours a short peak of lactation early in the summer (White and Luick, 1976; Holand et al., 2002b). Hence, it is in the mother’s interest to provide an affluent supply of nutrients in early lactation to maximize calf growth and secure calf survival during the early phase of life, and then restrict the milk transfer to encourage the calf to evolve the ability to achieve solid food on its own. Acknowledgments This research was supported by the Norwegian Research Council. References Aikio, P., Nieminen, M., Holand, Ø., Mossing, T., Alatossava, ¨ med mjolking ¨ T., Malinen, H.L., 2000. Forsok av vajor. Prosjektrapport Interreg. Sapmi. 54.
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Auldist, M.J., Wals, B.J., Thomsom, N.A., 1998. Seasonal and lactational influences on bovine milk in New Zealand. J. Dairy Res. 65, 401–411. Chan-McLeod, A.C.A., White, R.G., Holleman, D.F., 1994. Effects of protein energy intake, body condition, and season on nutrient partitioning and milk production in reindeer and caribou. Can. J. Zool. 72, 938–947. Clutton-Brock, T.H., Albon, S.D., Guiness, F.E., 1989. Fitness cost of gestation and lactation in wild mammals. Nature 337, 260–262. Gaillard, J.M., Festa-Bianchet, M., Yoccoz, N.G., Loison, A., ¨ Toıgo, C., 2000. Temporal variation in fitness components and population dynamics of large herbivores. Ann. Rev. Ecol. Syst. 31, 367–393. Geist, W., 1999. Reindeer and caribou. Deer of the World. Swan Hill Press, Shrewsbury, pp. 315–337. Hammond, J., 1961. Growth in size and body proportions in farm animals. In: Zarrow, M.X. (Ed.), Growth in Living Systems. Basoe Books, New York. Holand, Ø., Aikio, P., Gjøstein, H., Nieminen, M., Hove, K., White, R.G., 2002a. Modern reindeer farming—the influence on different milking regimes on udder health, milk yield and composition. Small Rum. Res. 44, 65–73. Holand, Ø., Gjøstein, H., Aikio, P., Nieminen, M., White, R.G., 2002b. Traditional reindeer milking and prospects of developing reindeer farming as a niche based production. Encycl. Dairy Sci. 637–643. Hollemann, D.F., White, R.G., Luick, J.R., 1975. New isotope method for estimating milk intake and yield. J. Dairy Sci. 58, 1814–1821. Jennes, R., Sloan, R.E., 1970. The composition of milks of various species: a comparative review. Dairy Sci. Abstr. 32, 599–612. ¨ Jonsson, K.I., 1997. Capital and income breeding as alternative tactics of resource use in reproduction. Oikos 78, 57–66. Laben, B.L., 1963. Factors responsible for variation in milk composition. J. Dairy Sci. 46, 1293–1301. Landete-Castillejos, T., Garcia, A., Gomez, J.A., Gallego, L., 2003. Lactation under food constraints in Iberian red deer (Cervus elaphus hispanicus). Wildl. Biol. 9, 131–139. Landete-Castillejos, T., Garcia, A., Gomez, J.A., Laborda, J., Gallego, L., 2002. Effect of nutritional stress during lactation on immunity costs and indices of future reproduction in Iberian red deer (Cervus elaphus hispanicus). Biol. Reprod. 67, 1613–1620. Landete-Castillejos, T., Garcia, A., Molina, P., Vergara, J., Garde, J., Gallego, L., 2000. Milk production and composition in captive Iberian red deer (Cervus elaphus hispanicus): effect of birth date. J. Anim. Sci. 78, 2771–2777. Landete-Castillejos, T., Garcia, A., Gallego, L., 2001. Calf growth in captive Iberian red deer (Cervus elaphus hispanicus): effects of birth date and hind milk production and composition. J. Anim. Sci. 79, 1085–1092. Lavigueur, L., Barrette, C., 1992. Suckling, weaning and growth in captive woodland caribou. Can. J. Zool. 70, 1753–1766. Lee, P.C., Majluf, P., Gordon, I.J., 1991. Growth, weaning and maternal investment from a comparative perspective. J. Zool. Lond. 225, 99–114. Littell, R.C., Milliken, G.A., Stroup, W.W., Wolfinger, R.D., 1996. SAS System for Mixed Models. SAS Institute Inc, Cary, NC, pp. 633.
656
H. Gjøstein et al. / Comparative Biochemistry and Physiology Part A 137 (2004) 649–656
Loudon, A.S.I., Kay, R.N.B., 1984. Lactational constraints on a seasonally breeding mammal: the red deer. Symp. Zool. Soc. Lond. (51) 233–252. Luick, J.R., White, R.G., Gau, A.M., Jennes, R., 1974. Compositional changes in the milk secreted by grazing reindeer. I. Gross composition and ash. J. Dairy Sci. 57, 1325–1333. Martin, P., 1984. The meaning of weaning. Anim. Behav. 32, 1257–1258. McEvan, E.H., Whitehead, P.E., 1971. Measurement of the milk intake of reindeer and caribou calves using tritiated water. Can. J. Zool. 49, 443–447. Mueller, C.C., Sadleir, R.M.F.S., 1977. Changes in the nutrient composition of black-tailed deer during lactation. J. Mammal. 58, 421–423. Noldus Information Technology, 1998. Reference Manual MatMan 1.0 for Windows. Wageningen, Netherlands, 91 p. Oftedal, O.T., 1984. Milk composition, milk yield and energy output at peak lactation: a comparative review. Symp. Zool. Soc. Lond. 51, 33–85. Oftedal, O.T., 1985. Pregnancy and lactation. In: Hudson, R.J., White, R.G. (Eds.), The Bioenergetics of Wild Herbivores. CRC Press, Boca Raton, FL, pp. 215–238. Parker, K.L., White, R.G., Gillingham, M.P., Holleman, D.F., 1990. Comparison of energy metabolism in relation to daily activity and milk consumption by caribou and muskox neonates. Can. J. Zool. 68, 106–114. Perrin, D.R., 1958. The caloric value of milk in different species. J. Dairy Res. 25, 215–220.
Reese, E.O., Robbins, C.T., 1994. Characteristics of moose lactation and neonatal growth. Can. J. Zool. 72, 953–957. Robbins, C.T., Oftedal, O.T, O’Rourke, K.I., 1987. Lactation, early nutrition and hand-rearing of wild ungulates, with special reference to deer. In: Wemmer, C.M. (Ed.), Biology and Management of the Cervidae: A Conference held at the Conservation and Research Centre. Smithsonian Inst. Press, National Zoological Park, Washington DC, pp. 429–442. Rook, J.A.F., Wheelock, J.V., 1967. The secretion of water and of water-soluble constituents in milk. J. Dairy Res. 34, 273–287. Sadleir, P.M.F.S., 1984. Ecological consequences of lactation. Acta Zool. Fenn. 171, 179–182. SAS Inc, 1999. The SAS system for Windows, version 8.01. SAS Inc, Cary, NC. Sutton, J.D., 1989. Altering milk composition by feeding. J. Dairy Sci. 72, 2801–2814. Thomson, B.R., 1977. The behaviour of wild reindeer in Norway, Ph.D. Thesis, University of Edinburgh, UK. Trivers, R.L., 1974. Parent-offspring conflict. Amer. Zool. 14, 249–264. Weladji, R.B., Holand, Ø., 2003. Global climate change and reindeer: effects of winter weather on the autumn weight and growth of calves, Oecologia: in press. White, R.G., Luick, J.R., 1976. Glucose metabolism in lactating reindeer. Can. J. Zool. 54, 55–64. White, R.G., Luick, J.R., 1984. Plasticity and constraints in the lactational strategy of reindeer and caribou. Symp. Zool. Soc. Lond. 51, 215–232.