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Reproduction in female reindeer
E. Ropstad
)Department of Reproduction and Forensic Medicine, Norwegian School of Veterinary Science, P.O. Box 8146, Dep., N-0033 Oslo, Norway
Abstract
Reindeer are either wild or kept under very extensive farming systems. They are seasonal breeders, with mating coinciding with the decreasing photoperiod in the autumn, and with calving in the spring. Little is known regarding the factors that influence reproduction in reindeer or of their reproductive physiology. Studies carried out to date have mainly focused on issues related to the population dynamics of wild populations and semi-domestic herds, and to a limited extent on the reproductive physiology of the female. Nor is much known about reproductive disorders and their medical treatment, or of the possibilities to manipulate or control reproduction by the use of hormones. Modern reproductive techniques such as artificial insemination and in vitro fertilisation, maturation and transfer of embryos have so far received scant attention.
In the future, it is possible that reindeer under certain conditions might be kept in more intensive production systems. Limited access to high-quality winter pastures and increased demands for productivity have resulted in artificial feeding becoming a common practice in various reindeer herding areas in Scandinavia. In efforts to enhance the productivity of reindeer herds, attention has been focused on factors affecting reproduction in the female and survival of the offspring. Further knowledge on these issues seems necessary when developing strategies for optimalization of meat production in domestic herds and the harvesting of wild populations. This paper puts a broad focus on various aspects of reproduction, including factors influencing the fecundity of reproductively active females. In order to understand these effects it is important also to have a basic understanding of the reproductive physiology of these animals.q2000 Published
by Elsevier Science B.V. All rights reserved.
Keywords: Reindeer; Reproduction; Oestrous cycle; Pregnancy
)Tel.:q47-229-64857; fax:q47-225-97081.
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E-mail address: erik.ropstad@veths.no E. Ropstad .
0378-4320r00r$ - see front matterq2000 Published by Elsevier Science B.V. All rights reserved.
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1. Introduction
Reindeer, like most temperate cervids, are seasonal breeders, with mating coinciding with the decreasing photoperiod in the autumn, and with fawning in the spring. The fact that reindeer are kept under very extensive farming conditions and generally have a high fecundity chiefly explains why little interest has been shown in their reproductive physiology.
Reindeer are kept mainly for meat production. One of the most important factors of significance for productivity is the proportion of fertile females that have a calf at foot in
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the autumn. Both in caribou Miller and Broughton, 1974 and reindeer Eloranta and .
Nieminen, 1986; Lenvik and Aune, 1988 , calf losses ranging from 30% to 50% have been found between birth in the spring and slaughter in the autumn. Investigations by
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Lenvik and Aune 1988 indicate a strong relationship between calf losses and the maternal body weight, suggesting that significant reductions in calf losses could be obtained simply by increasing the body weight of females that become mated.
In the future, it is likely that reindeer will be managed more intensively and in closer contact with the herdsmen, which implies that there will be an increased need for knowledge on reproduction in this species. Thus, there is a need to expand our knowledge of normal reproductive physiology during the breeding season. Also, there may be benefits from development of methods to control reproduction by hormonal treatment. Little information is currently available about the control of ovarian function during the breeding season and the oestrous cycle.
The aim of this paper is to present current knowledge on reproduction in female reindeer with special emphasis on reproductive physiology and the interactions between environmental factors and fecundity. As most reindeer are free ranging and given little supplementary feeding, information based on wild-animal populations is highly relevant to the semi-domestic situation.
2. The breeding season
The plasma progesterone pattern over repeated oestrous cycles during the reproduc-Ž
tive season has been described in only a few reports McEwan and Whitehead, 1980, .
Rangifer tarandus caribou; Ropstad et al., 1995, Rangifer tarandus tarandus . Both
these studies indicate that cyclic ovarian activity occurs from September until February. As a result, the potential reproductive season is considerably longer than is indicated by
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the rut, which, is confined to about 2–3 weeks in SeptemberrOctober Lenvik, 1988b .
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Reindeer, as sheep Ryan et al., 1991 and other ruminants, are dependent on temporary elevations in progesterone concentration for initiation of regular oestrous cycles. Patterns of short periods of elevated progesterone concentrations were observed
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prior to the ordinary luteal phases Ropstad et al., 1995 . These consisted of one or more periods of elevated progesterone concentrations lasting 4–9 days. These results support
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findings in caribou McEwan and Whitehead, 1972, 1980 and in reindeer Eloranta et .
ovulations took place prior to these brief luteal phases. The shape of the progesterone
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curves was, as also found in sheep, highly variable Ryan et al., 1991 .
The fact that some females were still reproductively active in mid-February could explain the fact that late pregnancies can occasionally be seen at slaughter in August.
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McEwan and Whitehead 1972, 1980 documented that the reproductive seasons in reindeer and caribou may last up to150 days. These results are in accordance with those reported in various deer species and reindeer where the cyclical production of
proges-Ž
terone has been found to last for about 4–5 months Asher, 1985; Curlewis et al., 1988; .
Knox et al., 1988; Ropstad et al., 1995 .
3. The oestrous cycle
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In the experiment described by Ropstad et al. 1995 the overall average oestrous
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cycle length was 19.4"5.7 days "SD, range:13–33 days . The average length of the
Ž y1.
follicular phase plasma progesterone -1.6 nmol l remained fairly constant at about
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3 days over the same period overall mean"SDs3.0"1.6 days . An average oestrous
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cycle length of about 20 days was found also in adult females Ropstad, 1998 . The detailed endocrine profiles of the oestrous cycle in reindeer are generally in
Ž . accordance with those found in the ewe, extensively reviewed by Goodmann 1993 .
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15-Ketodihydro-PGF2a was secreted in a pulsatile manner Ropstad et al., 1995 . The first pulse was recorded before progesterone declined to basal levels, suggesting that PGF2a is the main luteolytic factor also in reindeer. In two animals the preovulatory LH Ž y1. peak occurred 66 and 42 h after progesterone had reached basal levels -1.6 nmol l .
Ž y1.
In both animals the maximal oestradiol level 16–18 pmol l preceded the preovula-tory LH peak. The duration of the LH peak was 12 and 15 h, respectively. Plasma
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progesterone concentrations were found to be higher than baseline levels )1.6 nmol y1.
l 99 and 78 h after LH maximum in two females.
3.1. Effect of cloprostenol in nonpregnant females
Treatment of nonpregnant females with cloprostenol resulted in an immediate and
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rapid decrease in plasma progesterone concentrations Ropstad et al., 1996a . The
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plasma progesterone remained low for a varying period of time 100–150 h until the onset of a new luteal phase. The fall in plasma progesterone was associated with increases in 15-ketodihydro-PGF . Generally, the concentrations of 15-ketodihydro-2a
Ž y1.
PGF2a were lower than during normal luteolysis 400–600 pool l and a pulsatile secretion pattern was not seen. The fall in progesterone was accompanied by rises in
Ž y1.
plasma oestradiol peak values: 16–31 pool l . A preovulatory rise in plasma LH was seen immediately after the increases in plasma oestradiol. The time elapsing between cloprostenol treatment and the preovulatory LH peak ranged from 48 to 72 h.
3.2. Oestrous symptoms
Oestrus, indicated by standing behaviour, was observed in three females as a result of
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luteolysis till the first observed oestrous symptoms was 56 and 60 h in one female and
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69 h in another. The average duration of standing behaviour oestrus was 27 h range: .
24–30 h . General interest in the observer, and lifting of the tail in response to touching the perineal regionrvulva, were seen for a somewhat longer period, usually 3–6 h prior to and after the standing behaviour. No vaginal discharge or swelling of the vulva was observed during oestrus.
4. Pregnancy
The gestation period in reindeer and caribou is reported to be approximately 225–235
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days Skjenneberg and Slagsvold, 1968; Bergerud, 1975; unpublished results .The reproductive endocrinology of pregnancy is poorly investigated. Only a few animals have been blood-sampled repeatedly throughout pregnancy, and detailed individual hormone profiles for hormones other than progesterone are not available. Progesterone concentrations show great variation during pregnancy, both within and between animals ŽMcEwan and Whitehead, 1980; Rehbinder et al., 1981; Blom et al., 1983, Ropstad et
.
al., 1999 . Generally there is an increase from conception until around 1–3 months of pregnancy after which the concentration stabilises or a slight decrease is seen. Prior to parturition a further increase in progesterone takes place. Progesterone detected during early pregnancy is probably secreted by the corpus luteum. However, during later pregnancy progesterone secretion most likely occurs both in the ovaries and the
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foeto-placental unit Sjaastad et al., 1990 .
4.1. Pregnancy diagnosis
For use in population studies measurement of plasma progesterone and pregnancy Ž .
specific proteins PSPB has proven efficient for pregnancy diagnosis when performed
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in January or later in pregnancy Russell et al., 1998; Ropstad et al., 1999 . Although reindeer are seasonally polyoestrous, it is unlikely that a large proportion of high progesterone concentrations at this stage originate from corpora lutea of the oestrous
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cycle Ropstad et al., 1999 . In early stages of pregnancy, progesterone has proven
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superior to PSPB in pregnancy diagnosis Russell et al., 1998 . Preliminary results indicate that rectal ultrasound investigation can be useful for early pregnancy diagnosis. When rectal ultrasound was performed in later stages of pregnancy the agreement with progesterone was good for positive diagnoses but not for negative diagnoses. This probably reflects a high rate of false negative diagnoses by the ultrasound method rather
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than false positives in the progesterone analysis Ropstad et al., 1999 .
4.2. Cloprostenol treatment during pregnancy
In other cattle, prostaglandin can be used to cause luteolysis and induce abortion, and
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have been used to control pregnancy in extensive production systems Roche, 1976 . It is questionable, however, whether the use of cloprostenol can be a useful method
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.
1996b . Treatment may be unreliable and can cause undesirable side effects. Preliminary data indicate that resumption of cyclic ovarian activity after induced abortion by
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cloprostenol is not common Ropstad et al., 1996a; Ropstad, 1998 .
5. Factors affecting reproduction
Traditionally, the basic idea behind reindeer herding has been to utilise the ability of these animals to grow and reproduce using pasture as their only food resource. As a result, the productivity of reindeer herds is extremely vulnerable to changes in the environment with food limitation as the major threat. In this context, the degree of access to nourishment in summer and shortage in winter and their interrelationship is of prime concern. The production potential of individuals is to a large extent determined by the carrying capacity of the pastures, and by the composition of the herds and the culling policy. In this context, the fertility of animals kept through the winter and the survival of
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their offspring are the most important factors Lenvik, 1988a .
5.1. Population density
An increase in population density will usually cause a rapid reduction of winter range quality, and thus decrease the amount of food available per capita in winter. This will cause decreases in reproduction rates and body mass of reindeer, and increases in
Ž
mortality rates within the population Klein, 1968; Skogland 1983, 1985; Kojola et al., .
1995 , but it can also expose populations to the risk of crashes during extreme winter conditions.
5.2. Age
The probability of pregnancy and a surviving autumn calf is related to maternal age in a curvilinear manner. The probability of pregnancy in a semi-domestic herd in Finnmark, northern Norway, increased from 18.8% in yearlings to 81.8% in females approaching 3 years of age. The highest probabilities of pregnancy were in the age
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classes between 4 and 9 years around 90% . Older females showed a lower fertility Žunpublished data . These figures are slightly lower than those reported in wild Alaskan.
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caribou Adams, 1998 but in agreement with findings in Finland Eloranta and
. Ž .
Nieminen, 1991 and in wild Svalbard reindeer Stien et al., 1999 . There was also a significant effect of age on the relationship between maternal body weight and calf
Ž .
autumn weight Lenvik et al., 1988 . Within the same maternal weight classes, mean calf autumn weight increased by 1.1 kgryear with increasing maternal age up to the age
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of five years, after which there was no significant age effect Lenvik et al., 1988 .
5.3. Between-yearÕariation
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Recent findings in Svalbard reindeer Rangifer tarandus plathrynchus indicate that in this particular subspecies, between-year variation in fecundity is mainly due to
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variation in foetal survival rather than variation in ovulation rate Stien et al., 1999 , suggesting that winter nutrition can be an important factor determining reproductive
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success in female reindeer and caribou Gates et al., 1986 . Low calf production follows harsh winters. On Nordenskjøldland on Svalbard calf production was only 5.9%
Ž
following severely restricted access to forage in late winter 1974 Alendal and Byrk-.
jedal, 1976 . In the same area the late winter pregnancy rate varied considerably
Ž . Ž .
between 1979 and 1982 Tyler, 1987 and between 1996 and 1998 Stien et al., 1999 . In 1996 only 50% of the adult females were pregnant. Of those diagnosed as being pregnant, 49% proved to be carrying a dead foetus. In 1998 the pregnancy rate was 90%
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and only one female carried a dead foetus Ropstad et al., 1996b; Stien et al., 1999 . No studies have as yet demonstrated any relationship between autumn weather conditions and pregnancy andror ovulation rate, although preliminary findings show a negative correlation between precipitation in October and the probability of pregnancy
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the following winter in a semi-domestic herd in Finnmark unpublished data . Within the same herd winter pregnancy rate ranged between 62.6% and 82.8% in the period from 1992 to 1998. The probability of calf loss ranged between 7.9% and 22.6%, and was correlated positively with snow depth in April and negatively with May temperature.
5.4. Body weight
Ž . The meat production potential of a herd is mainly dependent on three factors: 1
Ž . Ž .
fecundity, 2 losses, and 3 the potential for growth in young animals. All these factors are correlated with the body weight of sexually mature females in the herd. Studies in southern Norway and Finland showed that optimal criteria for calf production and reproduction could not be met unless live body weight in females becoming pregnant
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exceeded 60 kg Lenvik 1988a; Eloranta and Nieminen, 1986 .
Parturition rate is closely linked to autumn body weight, in general agreement with previous reports of direct relationships between pregnancy or parturition rate and live or
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dressed weight of female barren-ground caribou Daupine, 1976 , wild reindeer
Reim-. Ž .
ers, 1983a and semi-domestic reindeer Eloranta and Nieminen, 1986 in autumn. Similarly, pregnancy rates based on data collected at winter gatherings have been shown
Ž .
to vary directly with the intact or dressed weight of caribou Cameron et al., 1993 ,
Ž . Ž .
semi-domestic reindeer Lenvik et al., 1988 and Svalbard reindeer Stien et al., 1999 . Ž
Body fat, rather than body weight itself, may influence breeding success Thomas, 1982;
. Ž
Adamczewski et al., 1987; Allaye-Chan, 1991 through an effect on ovulation Leader-.
Williams and Rosser, 1983; Ropstad et al., 1992 , although the metabolic mechanism is largely unknown.
Body condition at or near breeding may alter calving date via an effect on conception
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time Baskin, 1970; Reimers, 1983b . Based on data from reindeer slaughtered approxi-Ž .
Ž .
by Cameron et al. 1993 and several other studies suggest that the date of calving is mainly a function of the nutritional status of the pregnant female, but the possibility of condition-related differences in the onset of ovulation cannot be discounted. Logically, female condition prior to the rut andror during late gestation could be implicated,
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depending on the timing of food limitation Skogland, 1984 .
The consequences of late calving are potentially serious. Late-born calves have less Ž
opportunity for growth before the onset of winter Baskin, 1970; Bergerud, 1975; .
Skogland, 1983 and are therefore more likely to suffer mortality due to predation and
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undernutrition Dauphine and McClure, 1974; Bergerud, 1975 . Finally, females calving late might be unable to complete lactation in time to replenish body reserves by autumn,
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thereby reducing chances of conceiving that year Skogland, 1985 .
5.5. Calf surÕiÕal
Several reports show that maternal weight or food intake of Rangifer is positively Ž
correlated with calf birth weight Bergerud, 1975; Rognmo et al., 1983; Cameron et al.,
. Ž
1993 and early survival Rognmo et al., 1983; Skogland, 1984; Eloranta and Nieminen, .
1986; Adamczewski et al., 1987 . The effect of calf birth weight on survival apparently extends beyond the perinatal stage. Domestic reindeer calves that survive to the end of
Ž
the calving season are heavier at birth than those that die Eloranta and Nieminen,
. Ž . Ž .
1986 . Low weight at birth may Espmark, 1980 or may not Rognmo et al., 1983 be sustained through summer, depending upon both milk production and the quality of the
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summer pasture White, 1991 .
5.6. PreÕious pregnancy
As indicated before, factors controlling the birth rate in a population of caribou are to a large extent of nutritional origin. The number of adult parturient females is to some
Ž
extent dependent on the body condition of the animals the previous season Allaye-Chan, .
1991; Cameron et al., 1993; Dauphine, 1976 , indicating that a decline in body condition due to the demands of reproduction may result in reproductive pauses andror delayed breeding. The incidence of reproductive pauses has been reported to be between 11% to
Ž
33% in wild caribou populations with higher incidences in young animals Dauphine, .
1976; Cameron, 1994 . In semi-domestic Norwegian reindeer, a lower percentage was
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found in adult females 4.8%; unpublished results . Yearlings diagnosed as pregnant had a 73.9% chance of becoming pregnant the following year as compared to 89.5% in older females.
5.7. Cohort effects
Significant cohort effects in reindeer have not as yet been reported in the literature. However, preliminary findings indicate that effects of early development on reproduc-tive performance in adulthood exist in reindeer and this effect might be related to
Ž .
Ž implications not only for the understanding of the population biology of reindeer Albon
.
et al., 1987 , but also for the understanding of environmental effects on the developmen-tal competence of gonadal cells.
6. Conclusions
Reindeer are seasonally polyoestrous with average oestrous cycle duration of about 20 days. Studies of reproductive hormones during the oestrous cycle and throughout the reproductive season indicate that reindeer show the same hormonal fluctuations as several other ruminants. Because reindeer are managed very extensively, environmental factors interact markedly with fecundity. Present knowledge suggests that management of these factors, of which nutrition and herd composition seem to be the most important, will enable the productivity of reindeer herds to be significantly improved.
Present knowledge on reindeer reproduction is still limited. Further insight both into the reproductive physiology and the population dynamics of these animals is needed to develop and evaluate new management strategies better suited to optimise their produc-tion potential.
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