Chapter III. Prenatal wastage

Fertilization failure
Fertilization failure due to lack or quality of stud male
Fertilization failure due to high temperature
Fertilization failure due to light body weight
Embryo mortality
High temperatures as cause of embryo mortality
Effect of genotype on embryo mortality
Effect of undernutrition on embryo mortality
Foetal losses
Estimates of foetal losses
Causes of abortions and stillbirths
References for chapter III

Confusion over the identity of prenatal mortality seems to remain a problem despite the clear definitions provided in earlier reports by Hanley (1961) and Edey (1969). According to Edey (1969), prenatal mortality refers to "deaths occurring over the full period of pregnancy". In other reports (Suleiman, 1976; Singh et al., 1986), however, such mortality is expressed as the sum of abortions and stillbirths. In this review, prenatal mortality will be referred to as the total losses occurring from ovulation to parturition including death of the ovum, be it fertilized or not. Prenatal losses will, therefore, encompass fertilization failure, embryo mortality and fetal death.

Fertilization involves the successful fusion of the sperm and the ovum. The embryo is the conceptus from the moment of syngamy to the time of implantation and the foetus is the conceptus from implantation to parturition (Wilmut et al., 1985). Pregnancy has three periods which are the period of ovum, that of the embryo and that of the foetus (Winters et al., 1942; Green and Winters, 1945). The period of ovum also known as pre-attachment or pre-implantation period is the time from fertilization to the first loose attachment of the blastocyst to the endometrium and is thought to last until about Day 14-15 in sheep (Edgy, 1969; Kelly, 1984). The embryonic period lasts until about Day 40 when the differentiation of the embryonic parts and placenta is concluded (Edey, 1976). The foetal period corresponds to the rest of the pregnancy which, according to Kelly (1986) begins on Day 30-40. Death during the period of ovum can be reasonably referred to as early embryonic loss whilst that occurring during the embryonic period can be named late embryonic loss. A ewe will have a cycle of normal length if the embryos die before Day 12 when maternal recognition of pregnancy occurs (Moor & Rowson, 1964). Edey (1967) pointed out that embryo mortality occurring before this recognition day is unlikely to be distinguished from failure of fertilization.

It appears from the preceding that embryo mortality should refer to death of fertilized ova (or embryos) before the completion of organogenesis and foetal mortality to deaths occurring from the end of organogenesis to birth.

While fertilization failure and embryo mortality are probably equally important in both sheep and goats, studies have concentrated on sheep which are always the preferred experimental animals. It is, therefore, within this constraint, that these two components (i.e. fertilization failure and embryo mortality) of reproductive losses will be discussed.

Fertilization failure

There is no published report on fertilization failure in sheep and goats of SSA, perhaps because this source of losses is costly and time consuming to measure. Reproduction in sheep is, however, a very wasteful process in view of the large difference between potential production and progenies produced. Kelly (1986) stated that while a ewe can only produce five to ten offsprings in her lifetime, she "could produce about 4,000 lambs if all the potential eggs in her ovaries developed". Restall et al. (1976) quoted in Willingham et al. (1986) found that 30 per cent of infertility in adult ewes and 34 per cent in maiden ewes were ascribed to a failure of the ewe to mate. A fertilization failure rate of 30 per cent has been assumed for sheep and goats in Africa (Charray et al., 1980) and may result from lack of breeding rams and bucks, high temperature and/or low live-weight of ewes and does.

Fertilization failure due to lack or quality of stud male

That flocks under the traditional production system often lack males of breeding age is overwhelmingly acknowledged (Wilson and Wagenaar, 1982; Branckaert et al., 1986; Dubois and Hardouin, 1987; von Kaufmann et al., 1986). Bayer (1986) reported that in the sub-humid zone of Nigeria, crop farmers may keep their small flocks for several months without a fertile male. Hendy (1980) found in Makonde Plateau of Tanzania that 56 per cent of goat flocks had no male over one year of age and in some cases, access to breeding males was a constraint to reproductive performance. In the highlands of Cameroon, Dubois and Hardouin (1987) observed that the long parturition interval (14 months) prevailing in goat flocks was ascribed not to abortions or temporary barrenness but to lack of a buck. Does under these conditions are put to bucks only during certain periods of the year when the farmers' financial resources permit. It is generally accepted that the early removal of males from the flocks is a means whereby producers minimize the risk of having them stolen or damaging neighbours' crops. However, farmers assume that bucks and rams will always be available in the communal grazing system, and this may be the major reason for the lack of stud males in the traditional production systems.

Moreover, there are indications that rams and bucks in SSA's traditional production systems are very fertile (ILCA, 1983). However, male fertility can be low due to immaturity or be lowered by chronic morbidity due to various pathologies or seasonal environment changes which may affect sperm quality and quantity. In this case and particularly when fewer than required breeding males are available, the fertilization process could be adversely affected. Lack of stud males appears to be a particular problem of these production systems.

It could be concluded that where the above situations prevail, failure to mate will undoubtedly play an important role in reproductive losses.

Fertilization failure due to high temperature

The depressive effect of high temperature on the behaviour and mating activities of both females and males has been reported as source of fertilization failure elsewhere in the tropics (Braden and Mattner, 1970; Devendra and Burns, 1983; Kelly, 1986). It has also been reported elsewhere that ram fertility is affected most severely 2-3 weeks later after he is exposed to high ambient temperatures (Waites and Setchell 1969; Braden and Mattner 1970; Smith, 1971). In SSA where research on the subject is neglected, a few reports (Wilson, 1976; Reynolds, 1979) claimed no adverse effects of temperature on male libido. Wilson (1976) working in southern Darfur of Sudan reported that ram libido appeared to be high at all times. Studies on fertility of Peul ewes in the semi-arid zone of Niger showed, however, that during the period of increasing temperature, silent ovulations are frequent and complete anestrus common (Yenikoye, 1984). In this case, the studies reveal, that native ewes and does do not exhibit oestrus in spite of the evidence that they ovulate. Behavioral oestrus is shown and reproductive activity is maximal only during parts of the year.

More evidence from on-farm studies of both male and female reproductive performance is needed to confirm the above suggestion that temperature has no depressive effect on male libido in SSA. Further, should the total lack of such adverse effects become established, which is unlikely, chances are that fertilization failure remains a problem in parts of SSA where widespread nutritional and housing constraints prevail and where temperature depresses the female's reproductive activity. Under village conditions and particularly in sahelian and arid zones of SSA, the temperature's depressive role on reproductive performance may involve an important reduction in the proportion of ewes in oestrous throughout the year (Guerra et al., 1972), an increase in the anestrus period (Haresign, 1981) and a failure to mate due to absence of behavioral oestrus.

Fertilization failure due to light body weight

Poor body weight of ewes and does can be a source of fertilization failure. Kelly (1986) reported that the number of ewes that fail to lamb increases as their bodyweight decreases. Weight loss, however, is a common feature of growth pattern of individual animals in the tropics in general and in SSA in particular. Its magnitude is highly affected by the degree of morbidity in the flocks and varies with the seasonal availability of forage resources, the nutritional and health statue, and the general management practices. Van Vlaenderen (1985) observed that adult sheep raised under the traditional system of the sub-humid Northern Togo lose 22 per cent of their body weight during the first half of the rainy season. During this period which also corresponds to the cropping season, animals are tethered. At Bunda stations of Malawi, lactating ewes lose 13.6 to 15.6 per cent of their live weight during the dry season (Kamwanja et al., 1985) which is far beyond the tolerable level of 5-7 per cent suggested by Scott (1975). It is unlikely that, under village conditions, such excessive losses are followed by a fast recovery and successful mating after weaning or after the tethering season has ended.

It could be concluded that research activities into the adverse effects of inadequate female weight along with heat stress and lack or questionable quality of stud male on sheep and goat productivity in the sub-Saharan Africa region have been poor or inexistent. Where such effects prevail, however, failure of fertilization may continue to play a silent role in lowering the reproductive efficiency of the region's small ruminants. Whether this role is to be assumed negligible because of the all-year round breeding system prevailing in the region is yet to be investigated.

Embryo mortality

The failure of a fertilized egg to develop normally has been investigated by many authors (Hammond, 1921; Corner, 1923; Crew, 1925; Overall, 1955; Hanley, 1961; Bishop, 1964; Quinlivan et al., 1966; Mattner and Braden, 1967; Edey 1969; Wilkins et al., 1984). Edey (1969), supported later by Wilkins et al. (1984) summarized estimates of prenatal loss (Table 3.1) and concluded that 20-30 per cent of embryos are normally lost during pregnancy with most losses occurring in the first 30 days. The normally occurring embryonic death is called basal embryonic mortality. It is the loss that occurs under normal and stress-free conditions. The questions as to why such loss occurs even in well managed flocks and why no factor or combination of factors investigated and controlled have not been able to eliminate it, remain unanswered. Bishop (1964) stated that the basal embryonic death may be a "perfectly normal way of eliminating unfit genotypes at low biological cost". It could be that asynchrony between ewe and embryo causes the latter to become abnormal (Wilmut and Sales, 1981) and be expelled from the uterus which is unable to prevent luteolysis (Lawson et al., 1983). For Hanley (1961), there is some "universally active factor" which seems to be responsible for the relatively constant residual death of fertilized ova. Edey (1969) concluded that until such a factor is discovered, many embryos will continue to die within the first 30 days of pregnancy in their native environment, the uterus.

It is now generally accepted, however, that identifiable factors exist which cause embryo death rate to rise beyond the basal limit. These factors which include ovulation rate, dam age, nutrition, hormonal conditions, site of ovulation, litter size, temperature and genotype have been well documented (Macfarlane et al., 1959; Edey, 1970; Braden, 1971; Gunn et al., 1972; Scalon, 1972; Lindsay, 1976; Brien et al., 1981; White et al., 1981; Hanrahan, 1983; Wilmut et al., 1985). Periods of particular vulnerability for the embryo are also well documented (Robinson, 1951; Moor et al., 1960; Edgar, 1962; Dutt, 1963; Quinlivan et al., 1966; Mattner and Braden, 1967; Edey, 1969). These are the early cleavage stage (Dust, 1963), the time of maternal recognition or Day 12 (Edey, 1969), and about Day 18 when the transfer from yolk sea to allantoic placentation occurs (Robinson, 1951; Moor et al., 1960; Quinlivan et al., 1966). Generally, more than half of the loss occurs before Day 13 and most of the remainder by Day 18 (Edey, 1967; 1969; 1976). Loss after commencement of implantation may simply be a continuation of a process initiated long before (Robinson, 1951).

No elaborated study has been carried out on embryo mortality in sheep and goats of SSA. In one of the two available reports, Wilson and Traore (1988) using abattoir material in Mali claimed that "although it is not possible to establish exactly the rate of embryo mortality by the method used, indications are that these were not very high". The authors did not specify what these indications were but reported early embryo deaths of 6.6 per cent in goats and none in sheep. In the second and more reliable report, Pathiraja and Oyedipe (unpublished data), using the abattoir material, found that about 30 per cent of fertilized ova in Yankasa ewes failed to be represented as lambs at birth. The abattoir material, however, has many shortfalls. Among these, are the impossibility to distinguish between failure of fertilization and early embryo death and the resulting underestimation of the latter. Where early embryonic mortality and resorption have occurred, a corpus luteum might still be seen and such cases cannot be differentiated from cyclic corpora in unmated ewes (Edey, 1969).

It can be concluded that, at this point, we have a poor knowledge of the extent of embryo death in sheep and goats in SSA, the factors that affect it when they do and the resulting effects on flock fertility. Some of the controllable factors investigated elsewhere and which may be associated with embryo loss in the region will now be discussed.

High temperatures as cause of embryo mortality

That high temperatures can lead to the death of a large proportion of embryos in newly mated ewes is well established (Dust et al., 1956; 1959; Alliston and Ulberg, 1961; Dutt, 1963; 1964; Boyd, 1965; Thwaites, 1967; 1971; Lindsay et. al., 1975; Sayer, 1979; Kelly, 1986). It is also established from field observations that embryonic deaths do occur in hot environments (Morley, 1954; Moule, 1954; Shelton, 1964; Moule, 1966; all cited in Edey 1969). The timing of heat stress seems more critical than its duration. Alliston and Ulberg (1961) and Dutt (1963, 1964) supported by Thwaites (1967; 1971), Lindsay et al. (1975), and Sayer (1979) showed that the sheep embryo is highly susceptible to continuously applied material heat stress during early cleavage stages while it is in the fallopian tube, i.e. during the first three days after conception. There are indications that acclimatization and diurnal variations in temperature can modify the adverse effects of such a stress (Thwaites, 1967b) but all embryos will usually die when continuous exposure to high temperatures raises ewe rectal temperature by 0.76 to 1.13°C (Thwaites, 1967c). Thwaites (1971) working with a room temperature of 40.6°C suggested that short-term heat waves of the kind that occur in the field can increase embryo mortality rates only in ewes that have recently ovulated. A field study carried out under summer conditions where mean ambient temperatures were between 32 and 40°C showed negative correlations between these temperatures at the time of mating and lambing performance, a situation ascribed to embryo mortality (Lindsay et al., 1975). Since prolonged heat stress due to high ambient temperatures within or above the indicated range prevails during dry seasons in many areas of SSA where housing facilities are lacking, it is likely that embryo death may be more than a minor component of reproductive losses in the region.

Effect of genotype on embryo mortality

Animal genotype is the second possible factor affecting embryo loss. Many authors elsewhere have generally agreed that significant differences in embryo mortality exist between breeds and lines of sheep (Foote et al., 1959; Bellows et al., 1963; Cumming et al., 1975; Edey 1976 and Meyer et al., 1983). However, according to Hanrahan (quoted in Kelly, 1984) who found low repeatability estimates (0.11 ±0.04 and 0.06 ±0.07) for the trait in Merino ewes, the potential for direct selection for higher embryonic survival may be small. Undoubtedly, variations in the trait among individuals within and between breeds exist and do need to be explored in SSA. This may require an understanding of the relationship between the ability of native does and ewes to withstand SSA's stressful environment and the degree to which survival of their fertilized ova is sustained.

Effect of undernutrition on embryo mortality

The effect of undernourishment on early embryo death has also been the subject of many investigations. However, there is a considerable variation in published results on the issue. While a number of studies have shown a decrease in embryo survival due to nutritional restriction (Bennet et al., 1964; Edey, 1966; 1970a; Cumming, 1972a; 1972b; Blockey et al., 1974), others have reported no such effects (Killeen, 1967; Edey, 1970b; 1970c; Bennet et al., 1970; Parr et al., 1982; Smith et al., 1983). Blockey et al. (1974) investigating the suggestion of Van Niekerk et al. (1968) that a few days of fasting could kill embryos, found that three days of fasting killed up to 10 per cent of single embryos during the first ten days after mating but had no effect on twin embryos. The authors concluded that there would normally be little effect on lambing percentage since deaths occurred early and ewes returning to service could mate again. Edey (1976) reviewed the available literature and pointed out that:

1. "when detected, levels of induced mortality have usually been less than 15 per cent, so fairly sensitive experimental designs are required to decide if loss is occurring";

2. "with rare exceptions, positive results have been associated only with severe undernutrition for periods of 7 to 21 days during the first month of pregnancy".

The above observations together with the findings of Parr et al. (1982) and Smith et al. (1983), led Kelly (1984) to conclude that "under normal farming conditions, it is unlikely that such severe changes in nutrition will occur".

From what precedes, it may be doubtful that embryonic death due to undernutrition represents an important source of embryo mortality in small ruminants under the normal drought-free conditions of SSA although nutrition is one of the major constraints to increased ruminant productivity in the region. Selenium deficiency may, however, be a problem in the highlands of SSA in view of the fact that this deficiency has been found to result in deaths of embryos of about four weeks old elsewhere (Hartley, 1963; Mudd and Mackie, 1973 quoted in Egan, 1974; Kelly, 1986) and that blood selenium in sheep and goats have been shown to be below minimum required levels in Kenya (Mbwiria et al., 1984).

Foetal losses

Under normal conditions, loss of conceptus from the end of organogenesis (Day 30-40) through to parturition (foetal period), is small (i.e. less or equal to 6 per cent) (Robinson, 1951; Quinlivan et al., 1966; Edey, 1969; 1976; Kelly 1984; 1986). Foetal loss entails abortion and stillbirth. Abortion is the expulsion before full term of a conceptus unable to sustain independent life (Dennis, 1969, quoted in Osuagwuh, 1985) or death in utero prior to the start of normal birth process (Woolliams et al., 1983). Stillbirth is the expulsion of a dead conceptus which is fully developed and might normally be expected to survive outside the uterus if born alive (Woolliams et al., 1983).

Unlike embryo mortality for which no estimate is available in SSA, foetal death is quite documented though available data are limited. Oftentimes, however, published reports fail to distinguish abortions from stillbirths. Where possible, the two components of reproductive losses will be discussed separately in this review.

Estimates of foetal losses

Estimates of abortions found in the literature are collated in table 3.2. There is a considerable variation on the basis of their expression. Some authors expressed them rightly on the basis as percent of total breeding females (Bertaudière, 1977; Lefèvre et al., 1979; Berger and Ginisty, 1980; Bourzat, 1980; Dumas, 1980; Adesiyun et al., 1983; Okoh, 1986; Armbruster, 1988), others as percent of total lambs/kids born (Reynolds, 1979; Wilson and Traore, 1988), or as percent of parturitions (Haumesser and Poutrel, 1973; 1980; Murayi et al., 1985) or as percent of livebirths (Adesiyun et al., 1983). In one report, abortions and stillbirths were expressed as percent of all foetuses (Suleiman, 1976) while in another, they were estimated as percent of pregnancies (Akakpo, 1988). Many estimates have no declared specification basis (Sarr et al., 1988; Shavulimo et al., 1984; Branckaert, 1987; El-Naim, 1979; Rutagwenda et al., 1985). The paucity of data coupled with the above varying classification will not permit meaningful comparisons between breeds, species and management conditions within ecological zones. However, estimates expressed as percent of breeding females of Bertaudière (1977), Dumas (1980), Lefèvre et al. (1979), Bourzat (1980) which range from 13 to 40 per cent for goats appear very high compared with those ranging from 3.7 to 13.65 per cent reported for sheep by Okoh (1986), Dumas (1980), Armbruster (1988) and Bourzat (1980). The above ranges could be applicable in the semi-arid zone as well. In the humid and sub-humid zones, abortions have been estimated at 25 per cent of breeding does and 3.7 to 6.5 per cent of breeding ewes (Dumas, 1980; Armbruster, 1988). Overall, most abortion rates are higher than the estimate of 9 per cent of breeding females proposed by Charray et al. (1980) for the western and central African sheep and goats.

Available estimates on stillbirths are fewer than those on abortions in SSA (table 3.2) and offer no basis for comparisons. However, the values of 10.3, 14.9 and 10.64 per cent reported by Wilson and Traore (1988), Suleiman (1976) and Osuagwuh et al. (1980) are high when approximated to estimates of 3.8 and 4 per cent obtained for sheep in Cameroon and Mali (Branckaert, 1987; Wilson and Traore, 1988) and to those of 4 and 7.39 per cent reported in Sudan (El-Naim, 1979) and Nigeria, respectively (Osuagwuh and Akpokodje, 1981).

It appears that losses due to foetal death in general have rarely been investigated and that stillbirths have been neglected or generally recorded as abortions. Among ewes and does in SSA, abortion rates are likely to be high and considerably variable (3.7 to 40 per cent of breeding females). Goats are more prone to abortions than sheep. Except in a few cases, the rates are exceedingly high when compared with the tolerable level of 1-5 per cent proposed in earlier work by Watson (1952).

Causes of abortions and stillbirths

Abortifacient diseases
Nutrition and season
Dam age, litter size, parturition interval and genotype
Embryonic and foetal loss due to slaughter of pregnant females

Published information on the causes of abortions is shown in Table 3.3. These causes can be partitioned in two groups of components which are of environmental (abortion-induced diseases, nutrition, season, dam age, litter size, management) and genetic origins. Such components interact within and between groups.

Abortifacient diseases

Reports on clinically diagnosed diseases responsible for abortions are rare in the literature. One of the few cases observed is concerned with enzootic abortion which was detected in most ecological zones (Lefèvre et al., 1979; Okoh, 1986; Armbruster, 1988). Two out of the three reports on this disease were under village management conditions. The highest abortion rate (26.5 per cent) was obtained under these same conditions where the introduction of controlled breeding as a management device was said to have been tested (Armbruster, 1988). In the semi-arid zone of Chad, incidence of chlamydial abortion was highest in the dry cool season (Lefèvre et al., 1979). Brucellosis, another abortifacient disease, was also clinically diagnosed. Losses due to Brucella ovis in sheep were estimated at 64.3 per cent of live births ³ in a rainy month on a state owned ranch in the sub-humid zone of Nigeria by Adesiyun et al. (1983). The authors suggested that inappropriate management played an important role contributing to these losses. Okoh (1980) observed a 'storm' of abortions due to Brucella abortus in sheep kept with cattle showing very high incidence of Brucellosis near Kano (Nigeria). The positive reactor rate was estimated at 14.5 per cent but the magnitude of the related abortion rate was not mentioned. Finally, the devastating growing effect of Rift Valley Fever (RVF) has been pointed out by Akakpo et al. (1988) in West Africa where they found that in the semi-arid zone of Burkina Faso, pregnancy rate interruptions due to RVF jumped from 29.62 per cent in sheep and 41.1 per cent in goats in 1985-86 to 78.3 and 52.1 per cent in 1987, respectively. High incidence of RVF was also reported in Mauritania, Senegal and The Gambia where cases of human death have occurred (Jouan, 1988 cited in OIE, 1988). Sarr et al. (1988) reported that abortions due to RVF virus are now common among small ruminants in the Senegal river valley following their occurrence in Mali, Madagascar, The Gambia, Sudan and Guinea Conakry. The latter authors indicated that abundant seasonal rains, swamps and a hot climate coupled with high concentration of animals and mosquitos, are responsible for the spread of the disease. Rats and migratory birds may have played an important role as vectors. It is worthwhile noting that RVF virus has existed in West Africa since its first presence was reported more than three decades ago (Ferguson, 1959). It is also worthwhile noting that many other disease conditions can cause abortions in small ruminants. Among these is PPR which was reported to have been associated with 41.2 per cent abortions in does raised under village management in the humid zone of Nigeria.

³ This is the specification basis used by the authors.

Nutrition and season

Nutritionally induced abortions have long been acknowledged particularly in does in Southern Africa (Van Rensburg, 1971; Wentzel et al., 1974) and suspected under the semi-arid village conditions of Niger (Haumesser and Poutrel, 1973) and Burkina Faso (Bourzat, 1980). In Niger, 75 per cent of the reported abortions in goats occurred towards the end of the dry season. In Burkina Faso, 21.6 per cent of abortions took place in the rainy season, 29.9 per cent in the dry cool season and 48.5 per cent in dry hot season. It was estimated that 23.6 to 87.5 per cent of breeding ewes and 27.3 to 72.2 per cent of breeding does joined in the dry hot season lost their foetuses before term. Both the reports by Bourzat (1980), Haumesser and Poutrel (1973) incriminated the scarcity of feed resources during the dry season, agreeing with evidence presented by Rutagwenda et al., (1985) in the semi-arid zone of Kenya. The latter authors obtained 22 and 0 per cent abortion rates when females were mated at the end of long dry season and prior to the long rains, respectively. In the humid zone of Côte d'Ivoire, the detrimental effect of season seems to be more important in the first months of the long rainy season (April-May) where more than 50 per cent of breeding females lost their foetuses before term (Armbruster, 1988). In general, management practices found in crop producing areas of the humid and sub-humid zones are thought to be responsible for losses of this kind. In these zones, small ruminants are tethered during rainy seasons to prevent them from damaging crops (Lagemann, 1977; Mack et al., 1984). This leads to under-nourishment which results in weight losses and poor reproductive performance occurring ironically during the very period when feed resources are abundant.

The period of high vulnerability when nutritionally induced abortions occurred in goats was found to be between 90 to 110 days of foetal life (Wentzel et al., 1974; Shelton and Groft, 1974). This was confirmed by Osuagwuh and Akpokodje (1985) who found that abortions are the prominent response of WAD does to undernourishment and that most of these abortions occurred during the period of accelerated foetal growth i.e. 90-120 days of foetal life.

Dam age, litter size, parturition interval and genotype

Very high rates of abortion and stillbirth were found among twin or triplet bearers (Suleiman, 1976; Osuagwuh, 1984), females with short parturition intervals (Haumesser, 1975, Rombaut and van Vlaenderen, 1976) and when primiparous and immature females were bred (Rombaut and van Vlaenderen, 1976; Ojo, 1980). In the humid zone of Côte d'Ivoire, Rombaut and van Vlaenderen (1976) observed that ewe lambs bred between four and eight months of age not only suffered from higher abortions and stillbirths (55 per cent) than adult ewes (14.6 per cent), but also lost 89 per cent of their progenies before one year of age. They strongly recommended that immature females be protected in the traditional system where breeding is not controlled. Osuagwuh (1984) who reported 70.5 per cent abortion among does carrying two or three foetuses and 61.1 per cent among first kidders, suggested that the high abortion rates among young and/or multiple pregnancy bearing does may be due to inadequate nourishment of both the foetuses and the young growing dam.

Certainly, the overall level of decrease in productivity due to foetal deaths under the traditional production system of SSA will remain unknown for a long time. However, there is a risk that this decrease is high in some areas of the region. For example, more than 50 per cent of both sheep and goats usually abort before three years of age in many areas of the semi-arid zone of Chad (Dumas, 1980). Perhaps, one of the most urgent needs is to identify the least susceptible breeds or genotypes among sheep and goats found in every ecological zone. In this regard, the data presented by Bourzat (1980) for the semi-arid zone of Burkina Faso is quite interesting. Mossi type animals in this zone aborted more during the hot season than Peul type breeds. Mossi goats and sheep are southern types of small ruminants closely related to the WAD breeds (Charray et al., 1980). That these animals tend to have lower performance than Peul types due to the environmental challenge may be an indication of their lower degree of adaptation to that environment. Evidence that some genotypes of native breeds may do better than others in a given environment has also been presented by Osuagwuh et al. (1980). In a crossbreeding trial involving WAD, Yankasa and Uda sheep, the authors observed higher stillbirths for Yankasa x WAD (22 per cent) and Uda x WAD (23 per cent) than for pure breed WAD (0 per cent). Where breed or genotype differences and genotype by environment interactions are detected, possibilities for improvement exist and must be used to reduce prenatal losses.

It can be concluded that many sheep and goat flocks in SSA may not be free of abortifacient diseases. As indicated by Okoh (1986), infectious abortions are probably among the highest economic problems facing the small stock industry of the region. Their association with particular seasons and mismanagement may be real and warrants more investigation. Undoubtedly, Rift Valley Fever appears to be the most dangerous abortion causing disease of our time as evidenced by its rapid spread and growing destructive effect among flocks and human populations between and within countries of SSA. Foetal losses tend to be related to dry season undernourishment in both sheep and goats raised in the semi-arid zone while the start of rainy season seems to be a period of high vulnerability in humid and sub-humid zones. In most cases, losses are highest in multiple foetus bearers, primiparous and immature females, and when parturition intervals are exceedingly short. Underfed does will be expected to respond with high abortion rates. Overall, there are no guidelines for proper specification of published estimates; such a situation is misleading and prevents sound comparisons to be made.

Embryonic and foetal loss due to slaughter of pregnant females

Wastage of conceptus through the slaughter of pregnant females is probably one of the most destructive practices man has ever used against his own production endeavour. While early pregnancy diagnosis may not be possible in most production systems of SSA, there can be no doubt that slaughter of three to four months pregnant does/ewes has some motives other than ignorance. It may be that farmers sell pregnant females because they look heavier and consequently sell at better prices than others. It may also be that because of financial resource limitations, females are indiscriminately sold for slaughter in time of crisis. It may further be that farmers wait for well-known poor producing females to be pregnant and so acquire apparent good condition before they sell them. Whatever the reason, it is most likely that many pregnancies are diagnosed before females are put to death. As shown in Table 3.4, 20 to over 70 per cent of does and ewes slaughtered at various slaughter houses of SSA were pregnant females. Furthermore, there is some evidence to suggest that the proportion of slaughtered pregnant females is highest when these are in their third to fifth months of gestation. Mukasa-Mugerwa and Tekelye (1988) found that of the conceptuses killed, 9.7, 21, 33.3 and 31.9 were in their first, second, third and forth months of age, respectively. In Mali, the average ages of foetuses when their dams were slaughtered were 3.1 months in goats and 3.6 months in sheep (Wilson and Traore, 1988). In Senegal, out of the 138 pregnant foetuses collected at the slaughter house in Dakar, 7.19, 13.66 and 79.13 per cent were 1-2, 2-3 and 3-5 months old, respectively (Nsekanyarenze, 1988). In Nigeria's Enugu and Nsukka abattoirs, pregnancy losses that could be avoided (i.e., 12-20 weeks old pregnancy) were estimated at 31.0 per cent in does and 33.9 per cent in ewes (Wosu and Dibua, 1992). The above figures suggest that slaughter of pregnant does and ewes is one of the most important causes of prenatal losses in the region. It remains to be seen, however, if the overall profit accruing to the farmers who intentionally sell pregnant females, compensates for the above expected loss.

Table 3.1. Basal Embryo Loss

Author(s)	Type of Estimate	% Mortality	Size of Sample		Breed	Age	Location
			Ewes	Ova
Dutt (1954)	Slaughter day 3-lambing	32.7	180	264	Mixed	Yearling	U.S.A.
Quinlivan et. al. (1966)	Slaughter day 2, 18, 40, 140-lambing	22.1	676	1,017	Romney	2.5 yr	N.Z.
Averill (1955)	Slaughter day 3 and 18-24	22.5	131	262	Suffolk		U.K.
Laffey and Hart (1959)	Slaughter day 3-4	40	60	85	N.Z. Halfbred		N.Z.
Hasnain (1964)	Slaughter day 18	43.3	14	30			U.K.
Mattner and Braden (1967)	Slaughter day 2 and 20	20.8	100		Merino	5 yr	Aust.
Hulet et. al. (1956)	Slaughter and returns to service	28.6 9.9	603 ewe-years		Hampshire and Shropshire		U.S.A.
Edgar (1962)	Slaughter day 24 and returns to service	10.8 0	276 328		Romney Romney	1.5 yr	N.Z.
Watson and Radford (1966)	Returns to service and slaughter on day 28	24	127	155	Merino	1.5 yr	Aust.
Dolling and Nicolson (1967)	Returns to service and slaughter on day 28	4.7-5.7 18.6-20.6	183 158	193 194	Merino Merino	1.5 yr 8.5-11.5 yr	Aust.
Morley (1954)	Indirect estimate	25-30	716		Merino		Aust.
Mullaney (1966)	Indirect estimate	22.8	7,304 ewe-years		Merino, Polwarth and Corriedal	4-9 yr	Aust.
Mullaney (1966)	Indirect estimate	24	2,451 ewe-years		Merino, Polwarth and Corriedal	2-3 yr	Aust.

Table 3.2. Some Estimates of Abortion/Stillbirth in Small Ruminants in Sub-Saharan Africa

Country	Breed/Species	Ecozone	Management Conditions	Type of Loss	Specification	% Loss	Author(s)
Malawi	Small East African goats	Highlands	Village	Abortion	As 70 of viable births	5.6	Karua, 1989
Nigeria	Balami & Yankasa sheep	Highlands	Station	Abortion	As % of breeding females	3	Okoh, 1986
Rwanda	African long-fat tailed sheep	Highlands	Station	Abortion	As % of parturitions	2.9	Murayi et al., 1985
Côte d'Ivoire	WAD goats	Humid	Village	Abortion	As % of breeding	5.3	Armbruster, 1988
Cameroon	WAD sheep	Humid	Station	Stillbirth	No specification	3.8	Branckaert, 1987
Côte d'Ivoire	WAD sheep	Humid	Village	Abortion	As % of breeding females	3.7	Armbruster, 1988
Nigeria	WAD, Udah, Yankasa & Permer cross-breed sheep	Humid	Station	Stillbirth	As % of parturitions	10.64	Osuagwnh et. al., 1980
Burkina Faso	Mossi goats	Semi-arid	Village	Abortion	As % of breeding females	30.5	Bourzat, 1980
Burkina Faso	Peul goats	Semi-arid	Village	Abortion	As 70 of breeding females	22.15	Bourzat, 1980
Chad	Sahel goats	Semi-arid	Village	Abortion	As % of breeding females	35	Bertaudière, 1977 cited in Lefèvre et al., 1979
Chad	Sahel goats	Semi-arid	Village	Abortion	As % of breeding	17.92	Lefèvre et al., 1979
Chad	Sahel goats	Semi-arid	Village	Abortion	As % of parturitions	28	Lefèvre et. al., 1979
Mali	Sahel goats	Semi-arid	Village	Abortion	As 70 of total kids born	12.6	Wilson & Traore, 1988
Mali	Sahel goats	Semi-arid	Village	Stillbirth	As 70 of total kids born	10.3	Wilson & Traore, 1988
Niger	Sokoto goats	Semi-arid	Village	Abortion	As 70 of parturitions	6.5	Haumesser & Poutrel, 1973
Senegal	Sheep & goats	Semi-arid	Village	Abortion	No specification	12.5	Sarr et al., 1988
Chad	Sahel goats	Semi-arid	Village	Abortion	No specification	5	Dumas, 1980
Somalia	While Somali goats	Semi-arid	Village	Abortion	As % of parturitions	1-7	Bouzat et al., 1992
Burkina Faso	Mossi sheep	Semi-arid	Village	Abortion	As % of breeding females	10.75	Bourzat, 1980
Burkina Faso	Peul sheep	Semi-arid	Village	Abortion	As % of breeding females	13.65	Bourzat, 1980
Chad	Sahel sheep	Semi-arid	Village	Abortion	No specification	4.6	Dumas, 1980
Mali	Sahel sheep	Semi-arid	Village	Abortion	As 70 of total lambs born	5.1	Wilson & Traore, 1988
Mali	Sahel sheep	Semi-arid	Village	Stillbirth	As 70 of total lambs	4	Wilson & Traore, 1988
Sudan	Sugor & Burog sheep	Semi-arid	Station	Abortion & Stillbirth	As % of all foetuses	14.9	Suleiman, 1976
Somalia	Black-headed Somali-sheep	Semi-arid	Village	Abortion	As % of parturitions	3-5	Bouzat et al., 1992
Chad	Kirdi goats	Sub-humid	Village	Abortion	No specification	10	Dumas, 1980
Kenya	East African x Exotic goats	Sub-humid	Village	Abortion	No specification	10	Shavulimo et. al., 1984
Malawi	Malawi goats	Sub-humid	Station	Abortion	As % of total kids born	11.76	Reynolds, 1979
Malawi	Small East African goats	Sub-humid	Ranch	Abortion	As % of viable births	9.5	Karua, 1989
Chad	Mayo-Kebbi & Kirdi sheep	Sub-humid	Village	Abortion	No specification	6.5	Dumas, 1980

Table 3.3. Causes of Abortion/Stillbirth in Small Ruminants in Sub-Saharan Africa

Country	Breed/Species	Ecozone	Management Conditions	Cause		Type of Loss	Specification	% Loss	Author(s)
				Main	Secondary
Rwanda	Small East African goat	Highlands	Station		Station 1	Abortion	% of parturition	1.28	Murayi et. al., 1987
Rwanda	Small East African goat	Highlands	Station		Station 2	Abortion	% of parturitions	20.6	Murayi et. al., 1987
Nigeria	Balami & Yankasa sheep	Highlands	Station	Chlamydiosis		Abortion	% of breeding females	3	Okoh, 1986
Nigeria	WAD goat	Humid	Station		Multiple birth and dry season	Abortion	% of total abortions	70.5	Osuagwuh, 1984
Nigeria	WAD goat	Humid	Station		First kidders	Abortion	% of total abortions	61	Osuagwuh, 1984
Cote d'Ivoire	WAD sheep	Humid	Village		Part. Int < 7 months	Abortion & Stillbirth	% of total abortions	22	Rombaut & Van Vlaenderen, 1976
Cote d'Ivoire	WAD sheep	Humid	Village		Breeding females aged 4-8 months	Abortion & Stillbirth	% of total abortions	56	Rombaut & Van Vlaenderen, 1976
Cote d'Ivoire	WAD sheep	Humid	Village		Breeding adult females	Abortion & Stillbirth	% of total abortions	15	Rombaut & Van Vlaenderen, 1976
Cote d'Ivoire	WAD sheep	Humid	Station		Rainy season	Abortion	% of breeding females	50-52.6	Berger & Ginistry, 1980
Cote d'Ivoire	WAD sheep	Humid	Station		Dry season	Abortion	% of breeding females	3.12	Berger & Ginistry, 1980
Nigeria	WAD sheep	Humid	Station		Early rains	Stillbirth	% of total kids/lambs born	0	Osuagwuh et. al., 1980
Nigeria	Permer x WAD sheep	Humid	Station		Dry season	Stillbirth	% of total kids/lambs born	19.23	Osuagwuh et. al., 1980
Nigeria	Sahel x WAD sheep	Humid	Station		Dry season	Stillbirth	% of total kids/lambs born	22.22	Osuagwuh et. al., 1980
Nigeria	Permer x WAD	Humid	Station		Early rains	Stillbirth	% of total lambs born sheep	0	Osuagwuh et al., 1980
Nigeria	Uda x WAD	Humid	Station		Early rains	Stillbirth	% of total lambs born sheep	0	Osuagwuh et al., 1980
Nigeria	Yankasa X WAD sheep	Humid	Station		Early rains	Stillbirth	% of total lambs born	0	Osuagwuh et al., 1980
Nigeria	Sahel x WAD sheep	Humid	Station		Dry season	Stillbirth	% of total kids/lambs born	23.08	Osuagwuh et. al., 1980
Cote d'Ivoire	WAD sheep	Humid	Village	Chlamydiosis		Abortion	% of breeding females	26.5	Armbruster 1988
Niger	Sokoto goat	Semi-arid	Village	Malnutrition		Abortion	% of parturitions	6.5	Haumesser & Poutrel, 1973
Chad	Sahel goat	Semi-arid	Village	Chlamydiosis		Abortion	% of breeding females	17.92	Lefèvre et. al., 1979
Burkina Faso	Mossi goat	Semi-arid	Village		Rainy season	Abortion	% of breeding females	11.2	Bourzat, 1980
Burkina Faso	Mossi goat	Semi-arid	Village		Dry cool season	Abortion	% of breeding females	16.2	Bourzat, 1980
Burkina Faso	Mossi goat	Semi-arid	Village		Dry hot season	Abortion	% of breeding females	72.2	Bourzat, 1980
Burkina Faso	Peul goat	Semi-arid	Village		Rainy season	Abortion	% of breeding females	13.4-40.9	Bourzat, 1980
Burkina Faso	Peul goat	Semi-arid	Village		Dry cool season	Abortion	% of breeding females	20-31.8	Bourzat, 1980
Burkina Faso	Peul goat	Semi-arid	Village		Dry hot season	Abortion	% of breeding females	27.3-66.6	Bourzat, 1980
Kenya	Small East African goat	Semi-arid	Station		Kidding at the onset of long rains	Abortion	No specification	22	Rutagwenda et al., 1985
Kenya	Small East African goat	Semi-arid	Station		Mated prior to long rains	Abortion	No specification	0	Rutagwenda et al., 1985
Kenya	Small East African goat	Semi-arid	Station		Kidding prior to short rains	Abortion	No specification	0	Rutagwenda et al., 1985
Kenya	Small East African goat	Semi-arid	Station		Kidding during short dry season	Abortion	No specification	11	Rutagwenda et al., 1985
Burkina Faso	Sahel type goat	Semi-arid	Village	Rift Valley Fever	1985-86	Abortion	% of pregnancies	41.17	Akakpo et. al., 1988
Burkina Faso	Sahel type goat	Semi-arid	Village	Rift Valley Fever	1987	Abortion	% of pregnancies	52.1	Akakpo et. al., 1988
Sudan	Sugor & Burog sheep	Semi-arid	Station		Single	Abortion + Stillbirth	70 of all foetus	11.3	Suleiman, 1976
Sudan	Sugor & Burog sheep	Semi-arid	Station		Twins	Abortion + Stillbirth	% of all foetus	16.36	Suleiman, 1976
Sudan	Sugor & Burog sheep	Semi-arid	Station		Triplet	Abortion + Stillbirth	% of all foetus	100	Suleiman, 1976
Burkina Faso	Mossi sheep	Semi-arid	Village		Rainy season	Abortion	% of breeding females	33.3	Bourzat, 1980
Burkina Faso	Mossi sheep	Semi-arid	Village		Dry cool season	Abortion	% of breeding females	12.5-33.3	Bourzat, 1980
Burkina Faso	Mossi sheep	Semi-arid	Village		Dry hot season	Abortion	% of breeding females	33.3-87.5	Bourzat, 1980
Burkina Faso	Peul sheep	Semi-arid	Village		Rainy season	Abortion	% of breeding females	17.6-25	Bourzat, 1980
Burkina Faso	Peul sheep	Semi-arid	Village		Dry cool season	Abortion	% of breeding females	25-58.8	Bourzat, 1980
Burkina Faso	Peul sheep	Semi-arid	Village		Dry hot season	Abortion	% of breeding females	23.6-50	Bourzat, 1980
Niger	Uda sheep	Semi-arid	Village		Peul Nomad	Abortion	% of Parturitions	2.45	Haumesser & Gerbaldi, 1980
Niger	Uda sheep	Semi-arid	Village		Hausa sedentary	Abortion	% of Parturitions	0.3	Haumesser & Gerbaldi, 1980
Burkina Faso	Sahel sheep	Semi-arid	Village	Rift Valley Fever	1985-86	Abortion	% of pregnancies	29.62	Akakpo et. al., 1988
Burkina Faso	Sahel sheep	Semi-arid	Village	Rift Valley Fever	1987	Abortion	% of pregnancies	78.3	Akskpo et. al., 1988
Nigeria	Uda, Balami & Yankasa crosses	Sub-humid	Station	Brucellosis		Abortion	% of breeding females	1.0	Adesiyun et al., 1983
Nigeria	Uda, Balami & Yankasa crosses	Sub-humid	Station	Brucellosis		Abortion	% of breeding females	1.9	Adesiyun et al., 1983

Table 3.4. Examples of losses due to slaughter of pregnant does and ewes - Slaughter house data

Country	Location	Month/year	Number of females slaughtered			Number of pregnant females slaughtered			% pregnant females slaughtered			Authors
			Sheep	Goats	Sheep + Goats	Sheep	Goats	Sheep + Goats	Sheep	Goats	Sheep + Goats
Ethiopia	Addis Ababa	July 1985 June 1986	608	-	-	426	-	-	70	-	-	Mukasa-Mugerwa and Tekelye, 1988
Mali	Niono	1983-86	469	3,166	-	94	1,004	-	20	32	-	Wilson and Traore, 1988
Senegal	Dakar	1987	-	-	79,805	-	-	21,301	-	-	27	Abassa and Tine, 1987
Chad	Bokoto	July & August 1988	16	215	-	7	154	-	44	72	-	Gongnet and Abassa, 1988
Togo	Lome	1982-85	17,847	14,631	-	7,139	5,755	-	40	39	-	Kombate and Abassa, 1987

References for chapter III

Abassa, K.P. and A. Tine. 1988. Loss of conceptuses due to the slaughter of pregnant does and ewes in Senegal. Unpublished data. EISMV; Dakar, Senegal.

Adesiyun, A.A., Ezeokoli, C.D., Kumi-Diaka, J. and A.L. Udechukwu. 1983. Brucella ovis as a possible cause of infertility and abortion on two sheep ranches in Nigeria. Bull. Anim. Hlth. Prod. Afr. 33: 11-16.

Akakpo, A.J., Jouan, A., Some M., Bada, R., Saluzzo, J.F., Bornarel, P., Sarradin, P. and J.P. Digoutte. 1988. Epidémiologie de la fièvre de la vallée du rift en Afrique de l'Ouest: Etude sérologique au Niger et au Burkina Faso. Article présenté à la réunion sur la fièvre de la vallée du rift en Afrique de l'Ouest. Dakar, Senegal.

Alliston, C.W. and L.C. Ulberg. 1961. Early pregnancy loss in sheep at ambient temperatures of 70 and 90°F as determined by embryo transfer. J. Anim. Sci. 20: 608.

Armbruster, T. 1988. La productivité de l'élevage ovin dans la région forestière de la Côte d'Ivoire. Rapport provisoire. CIPEA, Addis Ababa, Ethiopia.

Overall, R.L.W. 1955. Fertility of the ewe. Proc. Sec. Study Fert., 7:139-148. (A.B.A., 24, No. 691).

Bayer, W. 1986. Traditional Small Ruminant Production in the sub-humid zone of Nigeria. In: Von Kaufmann R., Chater S. and Blench R. (eds). Livestock systems research in Nigeria's sub-humid zone. Proceedings of the second ILCA/NAPRI symposium held in Kaduna, ILCA, Kaduna, Nigeria.

Bellows, R.W., Pope A.L., Chapman A.B. and L.E. Casida. 1963. Effect of level and sequence of feeding and breed on ovulation rate, embryo survival and fetal growth in the mature ewe. J. Anim. Sci., 22: 101-108 (A.B.A. 31, No. 2149).

Bennet, D., Axelsen A. and H.W. Chapman. 1964. The effect of nutritional restriction during early pregnancy on numbers of lambs born. Proceedings of the Australian Society of Animal Production. 5: 70.

Bennet, D., Nadin, J.B. and A. Axelsen. 1970. The effect of undernutrition during early pregnancy in Merino ewes. proceedings of the Australian Society of Animal Production 8: 362.

Berger, Y. and L. Ginisty. 1980. Bilan de 4 années d'étude de la race ovine Djallonké en Côte d'Ivoire. Rev. Elev. Med. Vet. Pays Trop. 33(1): 71-78.

Bertaudière, L. 1977. Aspects de la reproduction et aptitude laitière chez la chèvre du Sahel (Chèvre de Masskory). Rapport annuel. Laboratoire de Farcha. Tchad.

Bertaudière,, S. 1979. Région de recherches d'Afrique Centrale. Rapport d'activité 1978. Institut d'Elevage et de Médecine Vétérinaire des Pays Tropicaux. Maisons-Alfort. France.

Bishop, M.W.H. 1964. Paternal contribution to embryonic death. J. Reprod. Fert., 7: 383-396 (A.B.A., 32, No. 2689).

Blockey, M.A. de B., Cumming, I.A. and R.W. Blaxter. 1974. The effect of short-term fasting in ewes on early embryonic survival. Proceedings of the Australian Society of Animal Production 10: 265:269.

Bourzat, D. 1980. Paramètres zootechniques des espèces ovines et caprines de type "Mossi" et de type "Peul". IEMVT. Maisons-Alfort, France.

Bourzat, D., K.D. Gautsch, M.P.O. Baumann and K.H. Zessin. 1992. Major demographic parameters for White Somali goat and Black-headed Somali sheep in the Somalia central rangeland. In: Rey B. et al. (eds). Small ruminant research and development in Africa. Proceedings of the first biennial Conference of the African Small Ruminant Research Network. ILRAD, Nairobi, Kenya, pp. 159-175.

Braden, A.W.H. 1971. Studies of flock mating in sheep - 3. Effect of undernutrition of ewes during joining. Aust. J. Exp. Agric. Anim. Husb. 11:375-378.

Branckaert, R. 1987. Le mouton Djallonké (The West African Dwarf Sheep). Possibilités d'amélioration et de sélection. ILCA, Addis Ababa, Ethiopia.

Boyd, H. 1965. Embryonic death in cattle, sheep and pigs. Vet. Bull. 35: 251-266. (A.B.A., 33, No. 3119).

Braden, A.W.H. and P.E. Mattner. 1970. The effects of scrotal heating in the ram on semen characteristics, fecundity and embryo mortality. Aust. J. Agric. Res. 21: 509-518.

Branckert, R., Habonimana G. and A. Nivyobizi. 1986. Contraintes essentielles et recherches prioritaires dans le développement de l'élevage des petits ruminants dans les zones densément peuplées de hautes terres africaines. Dans: (CTA compte rendu du séminaire sur la coordination de la recherche pour le développement des petits ruminants en Afrique, Montpellier, France).

Brien, F.D., Cumming, I.A., Clarke, I.J. and C.S. Cocks. 1981. Role of plasma progesterone concentration in early pregnancy of the ewe. Aust. J. Expr. agric. Anim. Husb. 21: 562-565.

Charray, J., Coulomb, J., Haumesser, J.B., Planchenault, D. and P.L. Pugliese. 1980. Les petits ruminants d'Afrique Centrale et d'Afrique de l'Ouest. Synthèse des connaissances actuelles. IEMVT. Maisons-Alfort, Cedex, France.

Coop, I.E. and V.R. Clark. 1969. The influence of nutritional level in early pregnancy of the ewe. Journal of Agricultural Science 73: 387-394.

Corner, G.W. 1923. The problem of embryonic pathology in mammals with observation upon uterine mortality in the pig. Am. J. Anat., 31:523-545.

Crew, F.A.E. 1925. Prenatal death in the pig and its effect upon the sex-ratio. Proc. R. Soc. Edinb., 46:9-14.

Cumming, I.A. 1972a. The effects of increasing and decreasing liveweight on ovulation and embryonic survival in the Border Leicester x Merino ewes. Proc. Soc. Anim. Prod. 9: 192-198.

Cumming, I.A. 1972b. The effect of nutritional restriction on embryonic survival during the first three weeks of pregnancy in the Perendale ewe. Proc. Aust. Soc. Anim. Prod., 9: 199-203.

Cumming, I.A., Blockey M.A. de B., Winfield, C.G., Pair, R.A. and A.H. Williams. 1975. A study of relationships of breed, time of mating, level of nutrition, liveweight, body condition and face cover to embryo survival in ewe. J. Agric. Sci. Camb. 74: 187-192.

Dennis, S.M. 1969. Laboratory diagnosis of infectious bovine abortion J.A.V.M.A. 155: 1913-1922.

Dettmers, A., Igoche, C.A. and K. Akinkuolie. 1976. The West African Dwarf Sheep. I. Reproductive Performance and Growth. Nigerian Journal of Animal Production 3(1): 139-147.

Devendra, C. and M. Burns. 1983. Goat Production in the tropics (2nd Edition) (Tech. Comm. No. 19. Commonwealth Bureau of Animal Breeding and Genetics). Commonwealth Agricultural Bureaux: Farnham Royal, U.K.

Dubois, J. and J. Hardouin. 1987. L'élevage des petits ruminants en milieu villageois au Cameroun. Premiere partie: les productivités. Tropicultura 5(3):103-106.

Dumas, R. 1980. Contribution à l'étude des petits ruminants du Tchad. Rev. Elev. Med. Vet. Pays Trop. 33(2): 215-233.

Dutt, R.H. 1963. Critical period for early embryo mortality in ewes exposed to high ambient temperatures. J. Anim. Sci. 22: 713-719.

Dutt, R.H. 1964. Detrimental effects of high ambient temperature on fertility and early embryo survival in sheep. Int. J. Biometeorol. 8:47-56.

Dutt, R.H., Ellington, E.F. and W.W. Carlton. 1956. Effect of shearing and exposure to elevated air temperature on fertility and early embryo survival in ewes. J. Anim. Sci. 15: 1287-1288 (abstr.).

Dutt, R.H., Ellington, E.F. and Carlton W.W. 1959. Fertilization rate and early embryo survival in sheared and unsheared ewes following exposure to elevated air temperature. J. Anim. Sci. 18: 1308-1318.

Edey T.N. 1967. Early embryonic death and subsequent cycle length in the ewe. J. Reprod. Fert. 13, 437.

Edey, T.N. 1969. Prenatal mortality in sheep. A review. Anim. Breed. Abst., 37, 173-190.

Edey T.N. 1970a. Nutritional stress and pre-implantation embryonic mortality in Merino sheep, 1965. J. Agric. Sci. Camb. 74:181-186.

Edey, T.N. 1970b. Nutritional stress and pre-implantation embryonic mortality in Merino sheep, 1966. J. Agric. Sci., Camb., 74: 187-192.

Edey, T.N. 1970c. Nutritional stress and pre-implantation embryonic mortality in Merino sheep, 1967. J. Agric. Sci., Camb., 74: 193-198.

Edey T.N. 1970d. Nutritional stress and pre-implantation mortality in Merino sheep, (1964-7). General discussion and conclusions. J. Agric. Sci., Camb., 74: 199-204.

Edey, T.N. 1976. Nutrition and embryo survival in the ewe. Proceedings of the New Zealand Society of Animal Production. 36-231-239.

Edgar, D.G. 1962. Studies on infertility in ewes. J. Rep. Fert. 3: 50-54.

Egan. A.R. 1974. The Diagnosis of trace element deficiencies in the grazing ruminant. In: Trace Elements in Soil-Plant-Animal Systems. D.J.D. Nicholas and A.R. Egan (eds.). Academic Press, New York.

El-Naim, Y.A. 1979. Some reproductive traits of Sudan Nubian goats.

Ferguson, W. 1959. Identification of Rift Valley fever in Nigeria. Bull epizoot. Dis. Afr. 7: 317-318.

Foote, W.C., Pope, A.L., Chapman A.B., and L.E. Casida. 1959. Reproduction in the yearling ewe as affected by breed and sequence of feeding levels. II. Effects on ovulation rate and embryo survival. J. Anim. Sci., 18: 453-462. (A.B.A., 27, No. 1894).

Gongnet, G.P. and K.P. Abassa. 1988. Loss of conceptuses due to the slaughtering of pregnant does and ewes in Tchad. Unpublished data. EISMV, Dakar, Senegal.

Green, W.W., and Winters L.M. 1945. Prenatal development of the sheep. Tech. Bull. Minn. Agric. Exp. Sta. No. 169: 36 pp. (A.B.A., 14:235).

Guerra, J.C., Thwaites, C.J. and T.N. Edey. 1972. The effects of components of body weight on reproductive efficiency in Merino ewes. J. Agric. Sci. Camb., 78: 245-249.

Gunn, R.G., Doney, J.M. and J.F. Russell 1972. Embryo mortality in Scottish Blackface ewes as influenced by body condition at mating and by post-mating nutrition. J. Agric. Sci. Camb. 79: 18-25.

Hammond, J. 1921. Further observations on the factors controlling fertility and foetal atrophy. J. Agric. Sci. Camb., 11: 337-366.

Hanley, S. 1961. Prenatal mortality in farm animals. J. Reprod. Fert., 2: 1982-194.

Hanrahan, J.P. 1983. The inter-ovarian distribution of twin ovulations and embryo survival in the bovine, Theriogenology. 20(1): 3-11.

Haresign, W. 1981. The influence of nutrition on reproduction in the ewe. I. Effects on ovulation rate, follicle development and LH release. Anim. Prod. 32: 197-202.

Hartley, W.J. 1963. Selenium and ewe infertility. Proc. N.Z. Soc. Anim. Prod. 23: 20-27.

Haumesser, J. B. 1975b. Quelques aspects de la reproduction chez la chèvre rousse de Maradi - Comparaison avec d'autres races tropicales ou subtropicales. Rev. Elev. Med. Vet. Pays Trop. 28(2): 225-234.

Haumesser, J.B. and B. Poutrel. 1973. Contribution à l'étude des rickettsioses au Niger. Enquête épidémiologique réalisée dans la région de Maradi. Rev. Elev. Med. Vet. Pays Trop. 26(3): 293-298.

Haumesser, J.B. and P. Gerbaldi. 1980. Observations sur la reproduction et l'élevage du mouton Oudah nigérien. Rev. Elev. Med. Vet. Pays Trop. 33(2): 205-213.

Hendy, C.R.C. 1980. A single visit survey of animal performance in goat flocks of Mtwara region. In: Proceedings of the 7th scientific conference of the Tanzania Society of Animal Production held at Moshi, Tanzania. Tanzania Society of Animal Production. 7:96-108.

ILCA. 1983. L'élevage des petits ruminants dans les régions tropicales humides. Etude de systèmes No. 3. Addis Ababa, Ethiopie.

Kamwanja, L.A., Ayoade J.A. and T.P.E. Makhambera. 1985. Characterization of small ruminants in the Mitundu area, Lilongwe, Malawi. In: Wilson, R.T. and Bourzat, D. (eds). Small Ruminants in African Agriculture. Proceedings of a conference held at ILCA, Addis Ababa, Ethiopia.

Karua, A.K. 1989. Some performance indicators of Malawi indigenous goats under village and ranch conditions. In: Wilson R.T. and Azeb M. (eds). African small ruminant research and development. Proceedings of a Conference held at Bamenda, Cameroon. pp. 23-28.

Kelly, R.W. 1984. Fertilization failure and embryonic wastage. In: Lindsay D.R. and D.T. Pearce (eds). Reproduction in sheep. Butterworth, London.

Kelly, R.W. 1986. Reproductive wastage in sheep. Journal of Agriculture 27(1): 22-26.

Killeen, I.D. 1967. The effects of body weight and level of nutrition before, during and after joining on ewe fertility. Australian Journal of Experimental Agriculture and Animal Husbandry. 7:126.

Kombate, L. and K.P. Abassa. 1987. Loss of conceptuses due to the slaughter of pregnant does and ewes in Togo. Unpublished data. EISMV, Dakar, Senegal.

Lagemann, J. 1977. Traditional African Farming System in Nigeria: An analysis of reaction to increasing population pressure. Afrikastudien No. 98. IFO-Institut. Munich, Weltforum Verlage, Munchen.

Lawson, R.A.S., Parr R.A. and L.P. Cahill. 1983. Evidence for maternal control of blastocyst growth after a synchronous transfer of embryos to the uterus of the ewe. J. Reprod. Fert. 67: 477-483.

Lefèvre, P.C., Baketana, K. and L. Bertaudière. 1979. Note sur un foyer de Chlamydiose abortive sur la chèvre au Tchad. Rev. Elev. Med. Vet. Pays Trop. 32(1): 33-35.

Lindsay, D.R. 1976. The usefulness to the animal producer of research findings in nutrition on reproduction. Proc. Aust. Soc. Anim. Prod. 11: 217-224.

Lindsay, D.R., Knight T.W., Smith J.F., and C.M. Oldham. 1975. Studies in ovine fertility in agricultural regions of western Australia: Ovulation rate, fertility and lambing performance. Aust. J. Agric. Res. 26, 189-198.

Macfarlane, W.V., Pennycuit, P.R., Yeates, N.T.M. and E. Trift. 1959. Reproduction in hot environments. In Lloyd C.W. (ed.) Recent Progress in the Endocrinology of Reproduction. New York: Academic Press, pp. 81-95.

Mack, S.D., Sumberg, J.E. and C. Okali. 1984. Small ruminant production under pressure: The example of goats in southeast Nigeria. In: Sumberg, J.E. and Cassaday, K. (eds). Sheep and goats in humid west Africa. Proceedings of the Workshop on small ruminants production systems in the humid zone of west Africa held in Nigeria.

Mattner, P.E., and A.W.H. Braden. 1967. Studies in flock mating of sheep., 2. Fertilization and prenatal mortality. Aust. J. Exp. Agric. Anim. Husb., 7: 110-116. Summ.: 99. (A.B.A., 35 No. 3725).

Mbwiria, S.K., Dickson, J.O. and J.F. Bell. 1984. Blood selenium concentrations of sheep and goats from selected areas of Kenya. Proceedings of the third small ruminant - CRSP Kenya Workshop, 5-6 March 1984, Nairobi, Kenya, SR-CRSP: Nairobi, pp. 147-151.

Meyer, H.H., Clarke, J.N., Harvey, T.G. and I.C. Malthus. 1983. Proceedings N.Z. Soc. Anim. Prod., 43: 201-204.

Moor, R.M., Rowson, L.E.A. and R.V. Short. 1960. Egg transfer in sheep factors affecting the survival and development of transferred eggs. J. Rep. Fert. 7: 145-152.

Moor, R.M. and L.E.A. Rowson. 1964. Influence of embryo and uterus on luteal function in the sheep. Nature Lond. 201, 522.

Mukasa-Mugerwa, E. and B. Tekelye. 1988. The reproductive performance of Ethiopian Highland sheep. Animal Reproduction Science, 17: 95-102.

Murayi, Th., Sayers, A.R. and R.T. Wilson. 1985. Production en station du mouton à queue grasse longue d'Afrique au Sud du Rwanda. In: Wilson, R.T. and D. Bourzat (eds). Les petits ruminants dans l'agriculture africaine, CIPEA. Addis Abeba, Ethiopie.

Murayi, Th., Sayers, A.R. and R.T. Wilson. 1987. La productivité des petits ruminants dans les stations de recherche de l'Institut des sciences agronomiques du Rwanda. CIPEA. Rapport de recherche No. 15. Addis Abeba, Ethiopie.

Nsekayarenze, J. 1988. Contribution à la détermination de l'âge du foetus de brebis Peul-Peul du Senegal (A propos de 138 foetus récoltes aux abattoirs de Dakar). These de doctoral en médecine vétérinaire No. 39. EISMV, Dakar, Senegal.

OIE. 1988. Compte rendu de la réunion sur la fièvre de la vallée du Rift en Afrique de l'Ouest tenue à Dakar, Paris, France.

Ojo, S.A. 1980. The merit of the indigenous goats as a competitive meat producer in meeting Nigeria's protein requirement. Paper presented at the 18th Annual Conference of the Nigerian Veterinary Medical Association, Ibadan, Nigeria.

Okoh, A.E.J. 1980. Abortion in sheep near Kano, Nigeria. Trop. Anim. Hlth. prod. 12: 11-14.

Okoh, A.E.J. 1986. Enzootic abortion of ewes in Nigeria: an investigation into the naturally occurring disease in a research animal facility. Rev. Elev. Med. Vet. Pays Trop. 39(2): 181-184.

Osuagwuh, A.I.A. 1984. Studies on the protein, energy and mineral utilization by the pregnant West African Dwarf goat in humid tropical zone of Ibadan. Ph. D dissertation. University of Ibadan, Nigeria.

Osuagwuh, A.I.A. 1985. Incidence and control of preweaning mortality and abortion in small ruminants. Proceedings of National Conference on Small Ruminant Production. The National Animal Production Research Institute, Shika-Zaria, Nigeria, 239-52.

Osuagwuh, A.I.A. and J.W. Akpokodje. 1984. The reproductive performance of the West African Dwarf (Fouta Djallon) goat. Trop. Anim. Prod. 9: 231-238.

Osuagwuh, A.I.A. and J.W. Akpokodje. 1985. An outbreak of abortion in West African Dwarf (Fouta Djallon) goat due to malnutrition. University of Ibadan, Nigeria.

Osuagwuh, A.I.A., Taiwo, B.B.A. and L.O. Ngere. 1980. Crossbreeding in tropical sheep: incidence of dystocia and parturition losses. Trop. Anim. Hlth. Prod. 12: 85-89.

Parr, R.A., Cumming I.A. and I.J. Clarke. 1982. Effect of maternal nutrition and plasma progesterone concentrations on survival and growth of the sheep embryo in early gestation. J. Agric. Sci. Camb., 98: 39-46.

Quinlivan, T.D., Martin C.A., Taylor W.B. and I.M. Cairney. 1966. Estimates of pre- and perinatal mortality in the New Zealand Romney Marsh ewe. I. Pre- and perinatal mortality in those ewes that conceived to one service. J. Reprod. Fert., 11: 379-390. (A.B.A., 35 No. 480).

Reynolds, L. 1979. Breeding performance and growth rate of the indigenous Malawi goat. Research Bulletin of Bunda College of Agriculture 10:90-100.

Robinson, T.J. 1951. The control of fertility in sheep. II. The augmentation of fertility by gonadotropin treatment of the ewe in the normal breeding season. J. agric. Sci. Camb. 41:6-63.

Robinson, T.J. 1957. Progesterone in the physiology of farm animals (ea. J. Hammond). Vol. III London: Butterworths.

Rombaut, D. and G. Van Vlaenderen. 1976. Le mouton Djallonké de Côte d'ivoire en milieu villageois. Comportement et alimentation. Rev. Elev. Md. Vet. pays Trop. 29(2): 157-172.

Rutagwenda, T., Schwartz, H.J., Carles, A.B. and A.N. Said. 1985. Effects of seasonal forage supply on some fertility parameters in the small East African goat in Northern Kenya. In: Wilson, R.T. and D. Bourzat (eds). Small Ruminants in African Agriculture. ILCA, Addis Ababa, Ethiopia. pp. 26-33.

Sarr, J., Diop, M. and Y. Dieme. 1988. La fièvre de la vallée du Rift chez les petits ruminants dans la vallée du fleuve Sénégal. ISRA. L.N.E.R.V. RF No. 003/VIRO. Dakar, Senegal.

Sayer, G.J. 1979. The influence of radiant heat load on reproduction in the Merino ewe. I. The effect of timing and duration of heating. Aust. J. Agric. Res. 30: 1133-1141.

Scalon, P.F. 1972. Frequency of transuterine migration of embryos in ewes and cows. J. Anim. Sci. 34(5): 791-794.

Scott, G. 1975. The sheepman's production handbook. Abegg printing: Denver, Colorado, U.S.A.

Shavulimo, R. Sidahmed, A.E. Gisemba, F. and O. Odero. 1984. Health problems in Western Kenya. Proceedings of the third small ruminant CRSP Kenya workshop. Kebete, Kenya.

Shelton, M. and J. Groft. 1974. Reproductive efficiency in Angora goats. Tex. Agric. Exp. Stn. Bull, 1136.

Singh, D.K.; Singh, L.B.; Singh, C.S.P. and H.R. Mishra. 1986. Factors affecting prenatal mortality in goats. Indian Journal of Animal Science 56 (7):785-788.

Smith, I.D. 1965. The influence of level of nutrition during winter and spring upon oestrous activity in the ewe. World Review of Animal Production 4: 95.

Smith, J.F. 1971. The effect of temperature on characteristics of ram semen. Aust. J. Agric. Res. 22, 481-490.

Smith, J.F., Jagusch, K.T. and P.A. Furquhar. 1983. The effect of duration and timing of flushing on the ovulation rate of ewes. Proc. No. Z. Soc. Anim. Prod., 43: 13-16.

Suleiman, A.H. 1976. Some production traits of Sudanese indigenous sheep under irrigated Gesire conditions. B.V.Sc. thesis. University of Khartoum, Sudan.

Thwaites, C.J. 1967a. Embryo mortality in heat stressed ewes. I. The influence of breed. J. Reprod. Fert. 14:5-14.

Thwaites, C.J. 1967b. Embryo mortality in heat stressed ewes. Ph.D. thesis. Univ. New England, Armidale, Aust.

Thwaites, C.J. 1967c. Embryo mortality in heat stressed ewes. The influence of breed. J. Rep. Fert. 14: 5-14.

Thwaites, C.J. 1971. Short-term heat stress and embryo morality in the ewe. Aust. J. Exp. Agric. Anim. Husb. 11: 265-267.

Van Niekerk, C.H., Belonje, P.C. and G.L. Hunter. 1968. Early embryonic mortality and resorption in Merino ewes due to malnutrition. Proceedings of the Sixth International Congress on Animal Reproduction and Artificial Insemination, Paris, 1: 455-458.

Van Rensburg, S.J. 1971. Malnutrition of the foetus as a cause of abortion. J.S. Afr. Vet. Med. Assoc.

Van Vlaenderen, G. 1985. Togo septentrional. L'élevage ovin. Revue Mondiale de Zootechnique No. 53, 19-26.

Von Kaufmann, R.R., Wilson R.T. and L. Reynolds. 1986. The economic importance of small ruminants in agricultural communities and land use systems in Africa. Dans: CTA compte rendu du séminaire sur la coordination de la recherche pour le développement des petits ruminants en Afrique.

Waites, G.M.H. and B.P. Setchell. 1969. Physiology of the testis, epididymis and scrotum. In: McLaren A. (ed). Advances in Reproductive Physiology, 4: 1-63. (Lagos Press: London).

Watson, W.A. 1952. Abortion and stillbirth in sheep. Vet. Bull 32(5): 259-264.

Wentzel, D., Morgenthal, C.J., Van Niekerk, C.H. and C.S. Roelofse. 1974. The habitually aborting Angora doe: II. The effect of energy deficiency on the incidence of abortion. Agroanimalia 6: 129-132.

White, D.H., Rizzoli, D.J. and I.A. Cumming. 1981. Embryo survival in relation to number and site of ovulations in the ewe. Aust. J. Exp. Agric. Anim. Husb. 21: 32-38.

Wilkins, J.F., Fowler D.G., Buidon B.M., Piper L.R., Hall D.G. and N.M. Fogarty. 1984. Proc. Aust. Soc. Anim. Prod., 15:768.

Willingham, T., Shelton, M. and P. Thompson. 1986. An Assessment of reproductive wastage in sheep. Theriogenology. 26(2): 179-188.

Wilmut, I. and D.I. Sales. 1981. Effect of an asynchronous environment on embryonic development in sheep. J. Reprod. Fert. 61(1): 179-184.

Wilmut, I., Sales D.I. and C.J. Ashworth. 1985. Physiological criteria for embryo mortality: Is a synchrony between embryo and ewe a significant factor? In: Land, R.B. and Robinson B.W. (eds.). Genetics of reproduction in sheep. Butterworths, London.

Wilson, R.J. and A. Traore. 1988. Livestock production in central Mali: Reproductive performance and reproductive wastage in ruminants in the agropastoral system. Theriogenology. 29(4): 931-944.

Wilson, R.T. 1976. Studies on the livestock of Southern Darfur, Sudan III. Production traits in sheep. Trop. Anim. Hlth. Prod. 8: 103-114.

Wilson, R.T. and K. Wagenaar. 1982. An introductory survey of livestock population demography and reproductive performance in the area of the Niger range and livestock project. ILCA, Addis Ababa, Ethiopia.

Winters, L.M.; Green W.W. and R.E. Comstock. 1942. Prenatal development of the bovine. Tech. Bull. Min. agric. Exp. Sta. No. 151.

Woolliams, C., Wiener, G. and N.S.H. McLeod. 1983. The effects of breed, breeding system and other factors on lamb mortality. 2. Factors influencing the incidence of delayed birth, dystokia, congenital defects and miscellaneous causes of early death. J. Agric. Sci. Camb. 100: 553-561.

Wosu, L.O. and B.M. Anene. 1990. Incidence and seasonality of reproductive disease conditions in small ruminants in Nsukka area, Nigeria. Beitr. Trop. Landwirtsch. Vet. Med. 28 H.2: 185-189.

Wosu, L.O. and E.C. Dibua. 1992. Lamb and kid wastage through slaughtering of pregnant ewes and goats at Enugu and Nsukka abattoirs in Anambra State, Nigeria. In: Rey, B., Lebbie, S.H.B. and L. Reynolds (eds). Small ruminant research and development in Africa. Proceedings of the first biennial conference of the African small ruminant research network. ILRAD, Nairobi, Kenya.

Yenikoye, A. 1984. Annual variations in oestrous behaviour, ovulation rate and the possibility to ovulate in Niger ewes of the Peulh breed. Reprod. Nutr. Develop. 24(1):1119.

Yenikoye, A., Pelletier J., Andre D., and J.C. Mariana. 1982. Anomalies in ovarian function of Peulh ewes. Theriogenology. 17(4):355-364.