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Trypanotolerance in small ruminants of sub-Saharan Africa
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Stanny Geerts1,2, Sabine Osaer3, Bart Goossens4, Déthié Faye5
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1. Institute of Tropical Medicine, Animal Health Department, Nationalestraat 155,
B-2000 Antwerp, Belgium
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2. International Trypanotolerance Centre, PMB 14, Banjul, The Gambia
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3. Boterbloemlaan 13, B-1933 Sterrebeek, Belgium
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4. UNOPS, Endemic Livestock Project, P.O.Box 4060, Bakau, The Gambia.
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5. BP 53, Butare, Rwanda
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Corresponding author: Geerts, S. (sgeerts@itg.be)
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Abstract
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Although a lot of information is currently available on trypanotolerance in cattle, until
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recently the trypanotolerant nature of small ruminants was not well known.
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Trypanotolerance in small ruminants is less pronounced than in cattle and should
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rather be considered as resilience than as resistance. West African Dwarf (WAD)
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goats appear to be less trypanotolerant than Djallonke sheep. However, recent studies
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have shown that there is an important introgression of genes of trypanosusceptible
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breeds into WAD goat populations, which possibly explains the loss of
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trypanotolerance in these animals. Measures need to be taken to safeguard and
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upgrade the genetic purity of trypanotolerant goat and sheep breeds in Africa.
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Trypanotolerant sheep and goat breeds
Small ruminants play an important role in the rural economies of Africa. They
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are kept mainly to generate income, as savings and for ceremonial purposes. In some
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countries such as The Gambia, the use of goat milk for home consumption is also
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important [1]. Sheep and goats are frequently managed by women and children.
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Agyemang [2] estimates that about 32% of the sheep and 47% of the goats in West
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and Central Africa are trypanotolerant. The breeds concerned are the Djallonke sheep
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(Figure 1a) and the West African dwarf (WAD) goats (Figure 1b) . Both are dwarf
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breeds with a height range of 30–50 cm for the goats, and 40–60 cm for the sheep. In
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East Africa the Small East African (SEA) goats and the Red Maasai sheep are
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considered as trypanotolerant [3;4]. They are slightly taller than the West African
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breeds, and are not considered as dwarf breeds [5].
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Trypanotolerance is the ability to survive, reproduce and remain productive
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under trypanosomiasis risk without the need for the use of chemicals to control the
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vector or drugs to control the parasite [6]. It offers farmers an important option for
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sustainable livestock production in areas at risk from trypanosomiasis. Contrary to the
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widespread belief that these trypanotolerant breeds are less productive than others due
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to their small size, it has been convincingly demonstrated that the productivity of
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trypanotolerant cattle and small ruminants is similar or even better than that of
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trypanosusceptible breeds when kept under similar conditions [7;8]. For example, the
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productivity of Djallonke sheep and WAD goats kept under tsetse fly challenge was,
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respectively, 42% and 68% higher than that of susceptible breeds, even when the
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susceptible breeds (e.g. Sahelian) were maintained in tsetse free conditions [7].
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Over the past decade the trypanotolerant nature of small ruminants has been
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studied in depth at the International Trypanotolerance Centre (ITC, Banjul, The
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Gambia) and elsewhere. This review summarizes and critically analyses the available
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information on trypanotolerant sheep and goats in sub-Saharan Africa.
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The trypanotolerant character in small ruminants
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Griffin and Allonby [3;4] were the first to show – both under experimental and
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field conditions in Kenya - the trypanotolerant character of some indigenous sheep
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and goat breeds. Comparison of indigenous SEA and Galla goat breeds with exotic
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Saanen and Saanen x Galla crossbreed showed that SEA were more tolerant to
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trypanosome infections than the Galla whereas the Saanen were highly susceptible
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and the crossbreeds showed a tolerance intermediate between Saanen and Galla.
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Similarly Red Maasai sheep exhibited a much higher tolerance to Trypanosoma
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congolense than Blackhead Persian or Merino sheep. Although Whitelaw et al. [9] in
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different breeds of goats in Kenya were not able to confirm the observations of Griffin
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& Allonby [3;4], other studies strongly indicate that SEA goats [10;11] and Red
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Maasai sheep [12;13] can be considered as trypanotolerant. Mutayoba et al.[14]
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compared SEA goats from different areas of East Africa and concluded that there
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might exist many varieties or types within the SEA goat population, some of them
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being more trypanotolerant than others.
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Several authors have shown that WAD goats and Djallonke sheep are more
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resistant to trypanosome infections than other breeds (such as Sahelian or Red Sokoto
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goats, Sahelian or Fulani sheep) or cross-breeds (F1 Sahelian-Djallonke) [15;16].
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Although, in some experiments, the resistance of trypanotolerant small ruminant
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breeds was significantly better than trypano-susceptible breeds only for T. vivax, and
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not for T. congolense [17]; in other experiments1, the opposite was true . These
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differences might be explained by the trypanosome strain which was used, as it is now
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well known that the pathogenicity of T. congolense varies widely from one subgroup
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(savannah, forest, kilifi) to the other [18], or even within the savannah subgroup [19].
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Surprisingly, Cameroonian dwarf goats experimentally infected with T. brucei all
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died, whereas no clinical signs developed after infection with T. congolense or T.
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vivax [20]. Very severe anaemia and weight loss with no tendency to recovery were
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also reported in Nigerian Djallonke ewes infected with T. brucei [21]. A similar
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susceptibility of WAD goats to T. brucei was not confirmed in other experimental
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infections [22] and was, to the best of our knowledge, never reported from the field
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[23].
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1
Touré,S.M., Seye,M., Mbengue,M. and Dieye,T. (1983) Trypanotolerance: studies
of comparartive pathology on dwarf Djallonke sheep and Sahelian Fulani sheep.
In Proceedings 17th ISCTRC Conference (OAU-IBAR, ed), pp. 326-336, OAU
4
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Genetic origin and mechanisms of trypanotolerance in small ruminants
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The genetic origin of the trypanotolerance trait in East African Galla goats
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was illustrated by the demonstration that Saanen x Galla crosses showed an
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intermediate tolerance between Saanen and Galla [3]. Similarly, by comparing pure
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bred with cross-bred animals, Kanyari et al. [10] and Goossens et al. [16] showed the
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genetic basis of trypanotolerance in SEA goats and Djallonke sheep, respectively. By
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contrast Faye et al. [24] were not able to show any difference in the degree of
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parasitaemia, anaemia and antibody response between WAD goats and their F1
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crosses (WAD x Sahelian). However, it is important to note that the WAD goats used
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in this study were selected on the basis of their phenotype. This experiment should be
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repeated using genetically characterised animals given the recent observations2 on an
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important degree of introgression of Sahelian genes into the WAD goats. The same
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remark can be made for most of the other studies since the animals were selected
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purely on phenotypic criteria.
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Contrary to cattle few research has been carried out to identify the
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mechanisms of trypanotolerance in small ruminants. Very elegant studies using
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haemopoietic chimaeras combining trypanotolerant (N’Dama) and susceptible
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(Boran) genotypes have shown that trypanotolerance in cattle is a trait that involves
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two at least partly independent mechanisms, i.e. the control of parasitaemia and the
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control of anaemia. The control of parasitaemia does not depend on the haemopoietic
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tissue and thus not on the immune system whereas the control of anaemia is
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dependent on the haemopoietic tissue genotype [25]. There are indications that similar
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Hoeven,E., Fidalis,M.N., Leak,S.G.A., Geerts,S., Hanotte,O. and Jianlin,H. (2007)
Introgression of the Sahelian breed into West African dwarf goats. In
Proceedings 28th ISCTRC Conference (Njogu,A.R., ed), pp. 622-626, AU
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discrete mechanisms controlling anaemia and parasitaemia might be present in
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Djallonke sheep [16], but this remains to be proven. Concerning the immune response
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in trypanotolerant animals most of the available data are derived from experiments in
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N’Dama cattle and show that there is no difference between trypanosusceptible and
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trypanotolerant cattle as far as antibody response to variable surface glycoproteins
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(VSGs) of trypanosomes is concerned [26]. However, significant differences do exist
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in antibody titres to non-surface exposed antigens (e.g. congopain) [26;27] which
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might be involved in the neutralisation of toxic or pathogenic molecules of parasite
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origin and thus contribute to trypanotolerance. To our knowledge similar experiments
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to examine the type of antibody response in trypanotolerant small ruminants have not
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yet been carried out, although significantly higher levels of anti-trypanosomal
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antibody titres were reported in Djallonke sheep as compared to Djallonke-Sahelian
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crossbreds [16].
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Trypanotolerance: resilience rather than resistance
By contrast to trypanotolerant N’Dama cattle, which are able to control
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parasitaemia quite well and which show a strong tendency to self-cure [12;28], the
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nature of trypanotolerance seems to be different in small ruminants. Several studies,
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both under experimental and field conditions, have shown that WAD goats and
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Djallonke sheep which were infected with T. congolense or T. vivax were able to gain
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weight, but showed a persistent parasitaemia [23;29;30]. In a long-term study using
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WAD goats and Djallonke sheep experimentally infected with a virulent T.
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congolense strain self-cure was only observed after 18 to 24 months [31]. This clearly
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suggests that ‘resilience’ is a more appropriate term to characterise trypanotolerance
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of sheep and goats than ‘resistance’. Resilience means that the animals are able to
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‘live with the trypanosome’ by limiting its pathological effects, the most prominent of
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which is anaemia. Concerning the control of anaemia, the results of experimental
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infections of small ruminants with T. congolense show that the hematocrit values in
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Djallonke sheep and WAD goats are significantly less affected than in non-
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trypanotolerant animals [15;17]. However, the erythropoietic response in Djallonke
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sheep and certainly in WAD goats seems to be less efficient than in N’Dama cattle
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[30].
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Concerning the genetic basis of resilience and the feasibility of breeding
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programmes for increased resilience there are only few data available for
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trypanotolerant small ruminants. Much research, however, has been done in the field
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of resilience to nematode infections in sheep [32-34]. According to Woolaston and
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Baker [32] breeding for resilience applies less selective pressure on the parasite than
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breeding for resistance because the emphasis is on co-existence of the host and the
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parasite . Nevertheless, Morris et al. [35;36] have shown that selection for resilience
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to nematode parasite challenge in Romney sheep flocks is possible although very
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time-consuming under commercial conditions. Compared with resistance, resilience
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to internal parasites appears to be somewhat less heritable but at least as variable
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[32;33]. In the field of trypanotolerance results are only available from the ITC’s
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breeding programme. This programme is carried out under village circumstances and
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aims to increase the efficiency of meat production and the resilience of WAD goats
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and Djallonke sheep [37]. The heritability estimates for body weight and growth rate
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traits for both species suggested that substantial improvement could be achieved by
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selection. Estimates of heritability for weight at birth, at weaning and at yearling age,
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pre-weaning and post-weaning growth rates were 0.5, 0.43, 0.30, 0.32 and 0.11 for
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WAD goats and 0.39, 0.54, 0.21, 0.54 and 0.23 for Djallonke sheep, respectively [37].
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Unfortunately hematocrit measurements were not included in the latter study. This
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would have allowed an even better estimate of the effectiveness of the breeding
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programme for improved resilience.
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Higher trypanotolerance in cattle than in small ruminants
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Although comparative studies of the degree of trypanotolerance between
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N’Dama and trypanotolerant small ruminants have not been carried out under
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experimental conditions, a large amount of data collected in various regions of The
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Gambia show that the prevalence of trypanosomiasis in N’Dama is quite similar to
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that found in Djallonke sheep and WAD goats when exposed to a similar
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trypanosomiasis risk [38]. However, it should be noted that small ruminants are less
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exposed to tsetse challenge than cattle because of their different grazing pattern
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(closer to the villages than cattle). This is supported by bloodmeal analysis of tsetse
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flies which shows that tsetse feed significantly less on small ruminants than on cattle
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[38]. Furthermore, Vale [39] showed that the feeding success of tsetse flies is also
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much higher on cattle (35%) as compared to sheep and goats (1%) due to the anti-
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feeding behaviour of the goats (including leg kicking and stamping, tail and ear flicks,
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skin rippling). Consequently, a similar prevalence of trypanosomiasis in
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trypanotolerant cattle and small ruminants living in the same environment strongly
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indicates that sheep and goat are indeed less trypanotolerant than cattle and points to a
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longer duration of the parasitaemia and a less efficient self-cure in the sheep and
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goats.
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WAD goats are less trypanotolerant than Djallonke sheep
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Several experiments carried out at the ITC in The Gambia have shown that
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WAD goats are less trypanotolerant than Djallonke sheep. After experimental
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infection with two T. congolense strains with different pathogenicity the anaemia was
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always more severe in WAD goats than in Djallonke sheep [29]. Furthermore,
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Goossens et al. [30] found a better haemopoietic response and a significantly higher
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antibody titre in Djallonke sheep than in WAD goats after experimental infection with
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a virulent West African strain of T. congolense. Follow-up for two years after an
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artificial infection with T. congolense showed that the productivity index of infected
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Djallonke sheep and WAD goats was significantly lower than that of control animals
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in the first year. However, infected Djallonke sheep became as productive as the non-
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infected control animals in the second year, whereas the productivity of infected
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WAD goats was only half of that of the control goats (Table 1), which again proves
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the superior trypanotolerance of Djallonke sheep as compared to the WAD goats [31].
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These observations were confirmed during a large-scale two-year field study in two
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areas, one with a high and the other one with a moderate tsetse challenge in The
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Gambia [23]. Although the prevalence of trypanosomiasis (predominantly T. vivax,
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followed by T. congolense and few T. brucei) was systematically higher in Djallonke
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sheep than in WAD goats, the mortality and the abortion rates were higher in goats
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than in sheep [23]. Both sheep and goats remained productive under moderate and
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high levels of trypanosome challenge, but the WAD goats were more affected
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(reduced haematocrit, weight loss) than the Djallonke sheep [23].
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The weak trypanotolerance of WAD goats from The Gambia was also
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confirmed by Faye et al. [24] and Dhollander et al. [40], who compared pure WAD
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goats with F1 crosses with Sahelian and Saanen goats, respectively. After
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experimental infection with T. congolense there was no significant difference in the
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levels of anaemia and parasitaemia between WAD and F1 crosses and the weight gain
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was equal or even higher in the crosses than in the apparently (based on phenotype)
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pure breeds.
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Introgression of non-trypanotolerant genes in WAD goats
All the previously mentioned studies were carried out with animals that were
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not genetically characterised. Therefore, they have to be interpreted very cautiously in
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the light of recent work on the genetic background of WAD goats . Hoeven et al. (see
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footnote 2), using 15 microsatellites, examined 615 individuals from 17 indigenous
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West-African goat populations from five West-African countries. Principal
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component and admixture analysis indicated that there is a gradient of introgression of
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Sahelian genes within the WAD goat populations consistent with the geographical
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location and tsetse distribution. A first gradient was observed from north to south
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(north to south Senegal and Guinea-Bissau), and a second gradient from east to west
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(from Mali to Guinea) (Figure 2). Apparently, although the goats phenotypically
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resembled dwarf goats, 31% to 53% of the genes of the four examined Gambian
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populations were of Sahelian origin, which might explain the loss of trypanotolerance
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in these WAD goats. Similar studies on the genetic background of other breeds of
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trypanotolerant small ruminants would be very useful.
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Trypanotolerance in small ruminants is a relative phenomenon
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There are several factors that might have a negative impact on the
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trypanotolerance trait of small ruminants, such as concurrent helminth infections,
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inadequate nutrition level and the severity of the trypanosome infection.
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In a controlled experiment, Djallonke sheep were able to withstand a single infection
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with T. congolense, but when exposed to an additional Haemonchus contortus
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infection, some animals lost their capacity to control the pathogenic effects of both
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parasitic infections, which led, in some cases, to mortality because of their additive
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effect [41]. The interaction between trypanosome and helminth infections was
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evidenced by a higher eggs per gram of faeces (EPG) in Djallonke sheep infected with
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both pathogens, confirming the immunodepressive effect of trypanosomiasis. This
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effect was also demonstrated in WAD goats by Faye et al. [24], who observed a
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significantly lower antibody response to H. contortus in T. congolense infected
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animals than in otherwise non-infected animals. Osaer et al. [23;42] confirmed these
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findings under natural field conditions with Djallonké sheep and WAD goats living
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under high trypanosomiasis risk.
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Dietary supplementation was acting independently but beneficially on packed
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cell volume (PCV) level and weight gain. Hence, it diminished the severity of
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anaemia, and reduced the weight loss caused by helminths and/or trypanosome
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infection [41]. This was also observed in an on-farm intervention trial under high
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trypanosomiasis risk [42]. Improved dietary levels in Djallonke ewes interacted
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positively with trypanosome infection on some haematological and productivity
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parameters, including reproductive performance [43]. Goossens et al. [30] further
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showed that trypanosome-infected Djallonke sheep, when adequately fed, mounted a
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better haematological response in the acute phase, as compared to infected WAD
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goats. This was confirmed by Katunguka et al. [44] who also described a better
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erythropoietic response in trypanosome-infected sheep fed with higher protein
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supplements. This proves the beneficial effects of nutrition in the control of anaemia,
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which is an important feature in trypanotolerance, as previously observed in N’Dama
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cattle [45]. On the other hand, some studies carried out in goats and sheep showed that
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trypanosome-infected animals under high protein level of diet had a higher
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parasitaemia score than those under low level [44;46]. This was explained by an
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enhancement of the growth and energy metabolism of trypanosomes due to the high
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concentration of serum cholesterol and non-esterified fatty acids generated from the
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diet [44].
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The severity of the trypanosome infection (virulent strain and/or natural high
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trypanosomiasis challenge) may also affect the level of trypanotolerance in small
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ruminants, as observed by Osaer et al. [29] and Goossens et al. [30]. Whitelaw et al.
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[9] and Faye et al. [24] were not able to show any difference in susceptibility between
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supposedly ‘susceptible’ and ‘resistant’ breeds of goats after infection with a highly
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virulent trypanosome strain as determined by decrease in PCV.
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The above studies indicate that all these factors (trypanosome infection,
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species and strain; inadequate nutrition; helminth infection) act independently but all
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contribute to the severity of the anaemia. Since the degree of trypanotolerance in
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small ruminants seems to be linked to the activity of the haematopoietic response
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[3;9;15;30;47] it is evident that all factors with a negative influence on the
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erythropoietic response, will also have a negative outcome on the degree of
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trypanotolerance.
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Resistance to ticks and helminths
Many studies have been carried out to examine the genetic resistance of sheep
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and goat breeds to gastro-intestinal (GI) nematodes. This review, however, focuses
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only on trypanotolerant breeds. Both under experimental and field conditions, it has
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been shown that there exists a marked individual variability in response to infections
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with H. contortus with a large percentage (about two thirds) of Nigerian WAD goats
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being resistant and a small proportion (less than 10%) being susceptible to infection
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[48-50]. Although a genetic basis for ‘haemonchotolerance’ has not yet been
4
established, the observations strongly point to a genetic resistance to H. contortus.
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Similarly in a multifactorial field trial Goossens et al. [16] showed significantly
6
higher nematode egg counts in Djallonke-Sahelian crossbreeds than in pure Djallonke
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sheep, which indicates an innate resistance and/or a more efficient immune response
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to nematodes.
9
Thirty years ago, in East Africa, Preston and Allonby [51;52] showed that Red
10
Maasai sheep are more resistant to H. contortus than other sheep breeds, which was
11
later confirmed and examined in more detail by Baker et al. [34;53]. Similarly, it was
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shown that SEA does and kids were more resistant to GI nematodes than were Galla
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does and kids [54;55] .
14
Although resistance to certain tick species (Amblyomma variegatum and
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Hyalomma spp., but not Boophilus spp.) has been clearly demonstrated in N’Dama
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cattle [56] almost no research has been carried out to study this aspect in
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trypanotolerant small ruminants. In a longitudinal study over a period of five years
18
Odo [57] was not able to find any significant differences in tick loads between WAD,
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Red Sokoto goats and their crossbreds. Unfortunately, Odo did not give any
20
information on the tick species involved.
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Genetic purity of trypanotolerant sheep and goats
Many countries have adopted livestock-improvement programmes based on
24
crossbreeding of endemic with exotic breeds. Furthermore, as mentioned above, there
25
is a tendency to increase the small size of the trypanotolerant small ruminant breeds
13
1
by crossbreeding with larger breeds resulting in an important introgression of genes
2
from trypano-susceptible breeds. Both approaches put the indigenous livestock breeds
3
at risk. Fortunately, in 1995, the ITC started a small ruminant breeding programme in
4
The Gambia, with the aim of improving the efficiency of meat production and the
5
level of trypanotolerance of WAD goats and Djallonke sheep. Analysis of the results
6
over a seven-year period (1995–2002) showed that the programme which was run
7
under low-input village conditions was very successful and resulted in clear genetic
8
improvement for body weight and growth rate [37].
9
In order to further promote the use of endemic livestock as a sustainable
10
approach for livestock breeding in rural areas in West Africa a new regional project
11
has recently started (see Box 1). In addition to conservation of the local breeds and to
12
increase their productivity, the project takes in equal measure account of conservation
13
of their environment. This long-term multi- donor project aims at conserving and
14
promoting N’Dama cattle, Djallonke sheep and WAD goats and their unique genetic
15
traits, as well as critical habitat for these breeds in their regions of origin in West
16
Africa. By ensuring sustainable populations of targeted endemic ruminant livestock
17
breeds in four West African countries it will support human food production and
18
improve rural economies. It will be implemented by establishing models for
19
community-based management of endemic ruminant livestock and their habitat at
20
pilot sites, and strengthen production, marketing, and policy environments in support
21
of these breeds. The project aims to integrate relations between animal genetic
22
resources, ecosystems, production systems and human welfare. Participation of
23
governments, NGOs and research institutes as well as co-funding by several donors
24
will be instrumental in assuring long-term sustainability of all the interventions at the
25
community level.
14
1
2
Acknowledgements
3
The authors want to thank the Belgian Directorate General for Development
4
Cooperation (Brussels) for its financial support of the research project on
5
trypanotolerant small ruminants at the International Trypanotolerance Centre, Banjul.
6
The authors are also grateful to Profs. P.H. Holmes and M. Murray for their critical
7
review of the manuscript.
8
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54 Baker, R.L. et al. (1998) Resistance of Galla and small East African goats in
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55 Baker, R.L. et al. (2001) Genetic resistance to gastro-intestinal nematode
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Glossary
Trypanotolerance is the ability to survive, reproduce and remain productive under
trypanosomiasis risk without the need for using chemicals to control the vector or
drugs to control the parasite [6]. As explained in the text trypanotolerance can either
be innate resistance or resilience to trypanosome infections.
Resistance is the ability of a host to initiate and maintain responses to suppress the
establishment of certain parasites, in casu trypanosomes and/or eliminate the parasite
load [32]. Since self-cure often occurs in bovines resistance is the appropriate term to
characterise trypanotolerance in N’dama cattle.
Resilience is the ability of the host to maintain a relatively undepressed production
level under parasite challenge [32]. Djallonke sheep are able to gain weight and to
reproduce even in the presence of a persistent parasitaemia. Therefore resilience is the
most appropriate term to describe the phenomenon of trypanotolerance in sheep.
Box 1. Project ‘Sustainable management of endemic livestock in West Africa’
20
 Project area: The Gambia, Mali, Senegal, Guinea
 Funding: African Development Bank, United Nations Development
Programme, Global Environment Facility, the Governments concerned,
FAO, CIRDES, ILRI
 Duration: 2008–2013
 Some of the expected outcomes
o Production and productivity of endemic ruminant livestock
sustainably improved
o Commercialisation and marketing systems of endemic ruminant
livestock and livestock products strengthened
o Natural resources in project pilot sites conserved, and sustainable
managed for the benefit of endemic ruminant livestock, ecosystem
services and human livelihoods
o Legal, policy and institutional frameworks established at the local,
national, and sub-regional level for in-situ conservation of endemic
ruminant livestock
o A sub-regional networking system established for cooperation,
information exchange and coordinated support for the conservation of
endemic livestock
 Some of expected realizations
o Rehabilitation and equipment of five zoo-technical research stations
with a view to re-launching genetic improvement programmes in the
participating countries
o Establishment of multiplication systems within 200 village herds in
order to ease access by mixed farmers to selected breeding stock
o Training of 15,000 livestock farmers including 8000 women in
different domains (animal feeding, breeding management and
20
improvement of the habitat of small ruminants
o Development and equipment of 17 slaughter areas, two sub-regional
livestock markets and 17 local livestock markets
o Construction and equipment of mini-dairies of a capacity of 200 to
600 l per day for women’s associations
More info: Dr. B. Goossens (BartG@unops.org)
1
2
21
1
2
Figure 1. Trypanotolerant small ruminants at the International
3
Trypanotolerance Centre in The Gambia. (a) A flock of Djallonke sheep (photo by
4
Andreas Schönefeld©).
5
6
(b) West African Dwarf (WAD) goats (photo by Abdou Fall©)
7
22
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
Figure 2. Population structures of indigenous goat populations in West Africa
(red= WAD, green = Sahelian) (source: Hoeven et al., 2007-see footnote 2; Hoeven,
E. 2004. Genetic characterisation of WAD goats, unpublished report, ITC, 17 pp.)
Legend: geographic location of sampled West-African goat populations; for Senegal (SE): SESL=StLouis, SEF=Fatick, SEC=Casamance (Kolda-Sédhiou); for The Gambia (GA): GABG=BrikamaGunjur, GAK=Keneba; GAN=Niamina, GAS=Sololo; for Guinea-Bissau: GB=Gabù-Bafata; for
Guinea (GU): sites A, B, C, D and E; for Mali (MA): MAM=Manankoro; MAS= Sagabory;
MAT=Tousséguéla
72%
Mauritania
31%
69%
SAH
SESL
Table
1. Productivity indexa of Djallonke sheep and West African Dwarf (WAD)
41%
59%
Senegal
goats under an experimental
infection with T. congolenseb
16
SEF
31%
31%
28%
53%
Year 1
47%
Control
GAN
Year 2
Mali
Infected
57%
43%
GAK
69%
GABG
69%
Control
Infected
15.5
16.5
15.6
7.5
GAS

Djallonke
27%
73% sheep

WADSECgoats
72%
28%
13.3
4.9
11.1
1.2
58%
MAS
42%
GB
Gambia
17
Productivity index : weight (kg) of 5 month old offspring produced per female
a
33%
18
maintained per year
19
b
20
Data from Ref. [31]
Guinea-Bissau
24%
67%
GUA
76%
GUB
81%
58%
42%
80%
Guinea
31%
20%
GUC
69%
MAM
GUE
57%
Sierra Leone
GUD
Liberia
23
43%
Ivory
Coast
MAT
19%
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