Full Article

Indigenous genetic resources: A sustainable and environmentally friendly option for livestock production in areas at risk from trypanosomes

Guy d'Ieteren (1) & Kamau Kimani (1)
(1) International Livestock Research Institute, P O Box 30709, Nairobi, Kenya.

Summary

KEYWORDS: Breeding - Cattle - Disease resistance - Genetics - Parasites - Production - Trypanosomiasis - Trypanotolerance - Tsetse.

Introduction

The African continent is faced with the challenge of satisfying a dramatic increase in demand for livestock products, in particular for milk and meat. Domesticated species play an important role in supporting human populations and in generating income and economic activity. The areas with the greatest potential for significant increases in livestock population and livestock productivity are the sub-humid and the non-forested parts of the humid zones. Large areas of natural grassland could be better used to support the increasing demand for livestock products if constraints on their increased contribution to market economies were understood and overcome, and existing opportunities identified and exploited. Animal diseases, especially those caused by parasites, are a major constraint on animal production in these areas. Trypanosomiasis is arguably the most important of these. Jahnke et al. (1988) considered that a total increase in cattle of 33 million heads might be possible and would lead to an additional production of 495,000 metric tonnes of meat per year (assuming productivity of 15kg/head/year) and an increase in milk production of 1.26 million metric tonnes per year (using estimates of 38.3kg/head/year) if eradication or sustainable control of trypanosomes were achieved over the entire tsetse fly-affected area in the sub-humid and humid zones (10 million km2). Thus, the potential benefits of sustainable of trypanosome control would be considerable for the 40 countries in Africa affected by this disease. 

In Africa, the major pathogenic trypanosome species in livestock are transmitted by the tsetse fly (genus Glossina) and include Trypanosoma congolense, T. vivax, T. brucei brucei and T. simiae. The subspecies of T. brucei, T. b. rhodesiense and T. b. gambiense cause sleeping sickness in man. No other continent appears to be dominated by one disease to the same extent that Africa is dominated by tsetse fly-transmitted trypanosomes. This disease not only results in severe losses in the productivity of domestic livestock due to poor growth, weight loss, low milk yield, reduced capacity for work, infertility and abortion, but also impairs the development of animal agriculture in zones which constitute 41% of the land but which carry only 26% of the ruminant population. The annual loss in meat production alone was estimated at US $5 billion in 1984 (Murray and Gray, 1984), but this figure excludes milk, hides and mixed agriculture. The number of cattle at risk of contracting Tsetse transmitted trypanosomes has been estimated at 46 million, in an area of about 8.7 million km2 (Reid et al., forthcoming). In Africa, 80% of traction power is non-mechanised. A six-fold increase in agricultural output as a result of the availability of a draught ox to a family unit has been calculated (McDowell, 1977). Furthermore, the manure provided by livestock is essential for the production of food and cash crops and is a potential source of energy in the form of biogas. Trypanosomes infect a wide range of hosts, including wild and domestic animals. The success of the trypanosome as a parasite is due largely to its ability to change a single glycoprotein called variant surface glycoprotein, VSG (Cross, 1975), thereby enabling evasion of host immune responses and the establishment of persistent infections.

This article examines the current state of trypanosome infection in African cattle, and the options available for its control. In particular, it looks at the potential of using indigenous trypanotolerant livestock as a sustainable method for controlling trypanosomes in cattle in Africa.

Options for trypanosomes control

Many factors contribute to the complexity of the problem of African trypanosomes. One major factor is the complexity of the disease itself - for example, the multiplicity of species of trypanosomes which cause the disease, either individually or jointly. These trypanosomes are transmitted cyclically by the tsetse fly, of which there are some 36 species and subspecies, each adapted to different climatic and ecological conditions (Ford, 1971). While the tsetse fly is not the only vector of African trypanosomes, cyclical transmission of infection represents the most important problem because a tsetse fly, once infected, remains infective for a long period, in contrast to the ephemeral nature of non-cyclical transmission by other biting flies. At the same time, trypanosomes infect a wide range of hosts, including wild and domestic animals, which represent reservoirs for the parasite. Apart from this, the enormous geographical area affected by trypanosomes, the variety of ecosystems, and the limitations of methods currently available for extensive control contribute to the difficulty of containing the disease. While eradication of trypanosomes remains an unrealistic goal for most of Africa, considerable effort has been invested in control of this disease by the use of trypanocidal drugs, management of the vector and exploitation of the genetic resistance exhibited by indigenous breeds such as N'Dama cattle and Djallonké sheep.

The use of trypanocidal drugs is well established and represents the most widely adopted approach to control trypanosomes. However, there is scope for increased use (Geerts & Holmes, 1998). Reports show increasing cases of trypanosome resistance to current drugs, both in individual cases and regionally, especially in East and West Africa (Clausen et al., 1992; d'Ieteren et al., 1997; Rowlands et al., 1993). There appears to be little hope for developing new trypanocidal drugs to benefit smallholder farmers in the short term. Given the actual or potential problem of drug resistance in many areas, drug usage clearly cannot be relied upon continuously as the sole method of trypanosome control.

The main method currently employed to control tsetse flies is the use of synthetic pyrethroid insecticides to impregnate traps and screens, sometimes additionally baited with odour attractants (Jordan 1986). More recently, live animals that have been impregnated through spraying, dipping or by pour-on treatments have been used as live targets (Bauer et al., 1992). The limitations of these techniques still need to be assessed before a wider adoption is promoted. One of the major drawbacks to the sustainability of these recently developed tsetse fly control methods is that they require the active participation of the majority of communities contributing to a relevant production system in a given environment or region, in order to be successful in the long term. Thus, they require major economic incentives to be accepted by farmers for collective action, as compared to methods of a more private nature, such as the use of curative or prophylactic drugs or disease tolerant livestock. 

A potential vaccine against trypanosomes is an attractive option. However, there is little hope that a conventional, anti-infection vaccine will be produced in the near future. 

Trypanotolerance: A major asset for sustainable livestock production under trypanosomes risk

Trypanotolerance, the ability of some livestock species and breeds to survive, reproduce and remain productive under trypanosome risk without the aid of trypanocidal drugs, was recognised and exploited by farmers long before research on trypanotolerance began. The exploitation of trypanotolerant breeds is practised as a major (if not the only) option for sustainable livestock production in 19 countries in the most humid parts of West and Central Africa. In 11 countries, trypanotolerant cattle (mainly N'Dama) were either moved into the highest risk areas or were imported from other countries. There are now N'Dama herds in nearly all West and Central African countries which are the source of genetic material for further dissemination (d'Ieteren et al., 1994). Trypanotolerance in cattle is well documented, particularly in N'Dama cattle, the most numerous trypanotolerant breed, and in the West African shorthorn. While significant differences in resistance to trypanosomes also occur among various zebu (Bos indicus) types (Ismael and Njogu, 1985; Njogu et al., 1985; Dolan et al., 1994; Mwangi et al., 1994), most Bos indicus cattle in tsetse fly-infested areas still require regular treatment or are found only on the fringes of fly belts. Exotic breeds cannot be maintained even in areas of low tsetse fly risk without intensive trypanocidal drug therapy and veterinary care.

There is a continued perception that because of their small size, trypanotolerant livestock are less productive than other breeds (Holmes, 1997). The International Livestock Research Institute (ILRI) demonstrated, however, that in areas where the tsetse fly risk was low or zero, the productivity of N'Dama and West African shorthorn cattle was equal to that of the physically larger trypanosusceptible zebu. As relevant long-term contemporary breed comparisons are not usually available, an approach developed by the International Livestock Centre for Africa (ILCA) was used in two in-depth productivity studies, carried out in separate production systems with similar beef oriented objectives Cattle production efficiency was expressed by relating total annual output back to the unit of cow metabolic weight, and herd productivity was expressed by the cow productivity index multiplied by cow viability. Using this approach, the cattle production efficiency of N'Dama cattle raised under very high trypanosome risk was equal to the cattle production efficiency of grade Boran cattle also maintained under high disease risk but with permanent chemoprophylaxis (Feron et al., 1988; Trail et al., 1985). N'Dama cattle produced 137.3 kg of 8-month weaner calf per 100 kg cow metabolic weight per year versus 137.5 kg for the Boran cow herds. Trypanotolerant N'Dama cattle thus compare very well with Boran cattle, which are regarded as one of the best beef cattle breeds in Africa, with the added advantage that N'Dama cattle are not dependent on trypanocidal drugs, whereas Boran cattle would not survive without the drugs. Similarly, Agyemang et al. (1994) demonstrated that when milk extracted from N'Dama cattle for human consumption was taken into consideration, their overall productivity was superior to that of zebu breeds maintained under similar traditional systems in the absence of tsetse fly challenge.

The evaluation of the interactions between the components of trypanosomosis risk and the different disease control methods deserves further attention in order to design sustainable strategies which are tailored more to the specific needs, constraints and opportunities of individual production systems. There is no single solution that will be valid for all production systems, ecological zones, and regional or national markets. The decreasing efficacy of the trypanocidal drugs available and the difficulties of sustaining tsetse fly control measures increase the imperative need for enhancing trypanotolerance through selective breeding, either within breed or through cross-breeding.

Thus, livestock production under trypanosome risk will have to focus increasingly on integrated control strategies which are more reliant on trypanotolerant livestock, on methods for increasing disease resistance and/or on improved vector control techniques, and possibly on less (or more careful) use of trypanocidal drugs. 

Understanding trypanotolerance 

Trypanotolerance has been defined as the relative capacity of an animal to control the development of the parasites and to limit their harmful effects, the most prominent of which is anaemia (Murray et al., 1982; Murray and Dexter, 1988). Results in recent years have shown that these two parameters are strongly correlated with animal performance, especially post-weaning growth, reproductive performance and overall cow productivity (d'Ieteren, 1984; Trail et al., 1992; 1993; 1994). Understanding these mechanisms has been a major research goal over the last twenty years, firstly with the aim to identify markers that could be used in selection for disease resistance, and secondly, in the hope to improve disease control. Conferring to susceptible cattle a similar capacity to that identified in resistant cattle, and optimising this capacity in trypanotolerant breeds, are indeed challenging options to complement conventional control methods. The mechanisms underlying bovine trypanotolerance remain mostly unravelled; however, immune response to trypanosomes greatly differ between susceptible and resistant cattle, a feature that might be exploited to improve trypanosomes control (Authié et al unpublished; Authié et al., 1993; Williams et al., 1996). The search for the genes controlling resistance is hampered by the difficulty of accurately identifying trypanotolerant individuals based on their physical characteristics, under experimental conditions. Recent research however, provides encouraging preliminary results on some genes associated with trypanotolerance (ILRI, 1998).

Exploitation of trypanotolerance traits

Further to understanding the mechanisms underlying trypanotolerance, the exploitation of resistance traits relies on the characterisation of these traits in the field and their practical measurement. The successful use of any criteria for identification of trypanotolerant breeds of cattle and/or superior animals within these breeds depends on the practicality of their measurement, on the strength of the link between the criteria and economically important production traits such as viability, reproductive performance and growth, and on the associated genetic parameters. 

Experiments to determine the heritability of trypanotolerance in N'Dama cattle indicates some possibility of selection based on the capacity to control anaemia, measured by percentage volume of red blood cells in blood (Packed Cell Volume). There is also a preliminary indication that the ability to control parasite growth may involve a degree of genetic control (Trail et al. 1992).

These initial results provide evidence that trypanotolerance is not only a breed characteristic but is also a heritable trait within the N'Dama population. The genetic variation identified within the N'Dama breed has opened new opportunities for improved productivity through selection for disease resistance.

With the selection criteria for trypanotolerance already available, or in the process of becoming so, the design of selection programmes is becoming possible. The next step will be to compute the most appropriate relative weightings between these criteria and all economically important traits in order to develop appropriate and relevant selection indices. Finally, identification and utilisation of superior animals in breeding programmes will depend on accurate measurement of these criteria in a field-based trial.

Multiple attributes of trypanotolerant livestock

In addition to their resistance to trypanosomes, trypanotolerant cattle, and the N'Dama breed in particular, are reported to be resistant to several other important infectious diseases (Murray et al., 1991), including a number of tick-borne infections such as dermatophilosis (Stewart, 1937), heartwater, anaplasmosis and babesiosis (Epstein, 1971), as well as lower prevalence of strongyle infections (Mattioli et al., 1992). 

Conclusion

There is increasing recognition that Africa possesses animal genetic resources probably unparalleled in any other continent. Evidence that these resources can provide sustainable and environmentally sound solutions for some of the vast disease problems currently confronting Africa is now being found. For example, although less attention has been focussed on the use of trypanotolerant livestock to cope with trypanosomes compared to other methods, farmers in 19 out of 40 countries in the most humid parts of West and Central African countries affected by the disease are using trypanotolerant livestock as a major, if not only option, to cope with the problem in an economically sustainable and environmentally friendly way. The fact that these breeds also possess considerable production potential and that their disease resistance traits could be exploited in crossbreeding offers an unparalleled opportunity for improving livestock production in the vast areas of Africa dominated by the tsetse fly, ticks and helminths, particularly as production systems evolve towards more market-oriented models.

Complementary reading

d'Ieteren, G.D.M. Authié, E., Wissocq, N. and Murray, M. (1998). Trypanotolerance, an option for sustainable livestock production in areas at risk from trypanosomes. Revue scientifique et techique. Office International des Epizooties, 17(1), 154-175.
d'Ieteren, G., Authié, E., Wissocq, N., and Murray, M. 1999. Exploitation of resistance to trypanosomes. In: R.F.E.Axford, S.C.Bishop, F.W.Nicholas, and J.B.Owen (editors) Breeding for Disease Resistance in Farm Animals, 2nd Edition. CABI Publishing, Wallingford, England. 195-216.
Murray, M., d'Ieteren G. and Teale A. Chapter: Trypanotolerance In: Trypanosomiasis, second edition, I.Maudlin, P.H. Holmes and M.A.Miles eds. CABI Publishing, Wallingford, England. (In preparation).

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