Sustainable tick and tickborne disease control in livestock improvement in developing countries

veterinary parauto~gy ELSEVIER

Veterinary Parasitology 71 (1997) 77-97

Sustainable tick and tickborne disease control in livestock improvement in developing countries Julio J. de Castro Animal Health Officer, Tick and Tickborne Diseases, Animal Health Service, Animal Production and Health Division, The Food and Agriculture Organization of the United Nations, Via delle Terme di Caracalla, 00100 Rome, Italy

Abstract Tick and tickborne disease (TTBD) control is a major component of animal health programmes protecting livestock, thereby enhancing global food security. The present methods for TTBD control are reviewed and an integrated use of the tools is recommended with a broader view of how to link TTBD control to the control of other parasitic diseases. The work of FAO in this field is presented and it is advocated that, although there are still areas that need further investigation, a stage has been reached where robust integrated TTBD control schemes, based on ecological and epidemiological knowledge of ticks and their associated diseases, can be promoted and implemented. Major challenges are the implementation of these policies in the field through the continuation of the present on-going programme in Africa and support to Latin America and Asia. The importance of involving all parties, governments, international and private organisations and the agrochemical industry in developing sustainable, cost-efficient control programmes is stressed and a global strategy is proposed. The main thrust should now be to convince policy makers on the adoption of the strategies and veterinarians and farmers on their implementation. © 1997 Elsevier Science B.V. Keywords: Ticks; Tickborne diseases; Integrated control; Developing countries; Economics; World; FAO

1. Introduction F o o d security, sustainable and environmentally acceptable agricultural production systems and trade are closely related. In the long term, global food security depends on maintaining and conserving the national resource base for food production of which livestock is an important component. There can be no sustainable disease control independent of livestock agriculture's sustainable development. The latter is defined by 0304-4017/97/$17.00 © 1997 Elsevier Science B.V. All rights reserved. PII S0304-401 7(97)0003 3-2

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FAO as 'The management and conservation of the natural resource base, and the orientation of technological and institutional change in such a manner as to ensure the attainment and continued satisfaction of human needs for present and future generations. Such sustainable development (in the agriculture, forestry and fisheries sectors) conserves land, water, plant and animal genetic resources, is environmentally non-degrading, technically appropriate, economically viable and socially acceptable.' The strategies for the sustainable development of animal agriculture have been addressed in an FAO Expert Consultation (Mack, 1990). It is estimated (FAO, 1996) that the world population will increase by 72% between 1995 and 2050 and then gradually stabilise. Nevertheless, food requirements of the developing countries will double and triple in inter-tropical Africa. With growing urbanization and increased income the demand for animal protein usually goes up. However, it is expected that the livestock sector will only grow moderately over the next 15 years and the consumption of livestock products in the developing nations will still be well below that of the developed world. Further, in areas of sub-Saharan Africa and South Asia, consumption will remain at very low levels, particularly through lack of milk (Alexandratos, 1995). Animal diseases in general and tick and tickbome diseases (TTBD) in particular are among the many factors which directly and indirectly hamper the growth of the livestock sector and of the whole agricultural sector due to the many roles of livestock as a source of food and income through generation of employment, delivery of energy (dung, biogas), fertiliser, weed control, use of marginal lands, investment and savings as well as transport (Sansoucy, 1995). TTBD control can only be seen as part of a larger animal health intervention in the context of livestock management and farming systems. The nature of the intervention needs to match the problem as well as being economically justified and socially acceptable catering for the wide variety of production systems and management types ranging from the most intensive, with high management and resource demands, to systems where very little or even nothing needs to be done except to maintain the existing endemic stability. As all combinations cannot be covered, this review will be limited to the impact of TTBD in the context of world food security, the control tools at our disposal, the concept of integrated TTBD control, the role of FAO in developing and promoting this as well as the possible way forward. Although it has been the intention to maintain a global view, the paper has a natural bias towards cattle in the African production systems, partly due to the author's experience with cattle, but also because of the greater impact of TTBD on cattle and the complexity of the problem in Africa. However, the effects of TTBD in other parts of the world may be equally important though perhaps less well understood or divulged. The need for assessing the impact of TTBD on other species of livestock has been recognised by FAO, and problems in sheep and goats are currently being assessed (FAO, 1994). It is hoped that by focusing on principles, the concepts expressed in the paper can be applied in a wider context in so far as geographical regions and different animal species are concerned.

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2. The impact of ticks and tickborne/associated diseases An important component of livestock improvement in the developing world, together with good nutrition, management and the availability of markets, is the control of animal diseases. The problem is particularly serious in Africa, Asia, the Caribbean, and Latin America. Losses caused by tick infestation are usually defined as tick worry, blood loss, damage to hides and skins of animals and introduction of toxins. Regarding the indirect effects of ticks, four major tick-disease complexes are recognised affecting cattle on a world-wide basis (McCosker, 1979): (i) Boophilus spp.--Babesia spp. (Babesiosis)--Anaplasma marginale (Anaplasmosis). This is probably the most important complex. It occurs in Latin America, Oceania and Asia, large areas of Africa and the Near East. The ticks cause damage per se as well as transmitting anaplasmosis and babesiosis which particularly affect imported and/or crossbred/high grade dairy and beef cattle; (ii) Hyalomma spp.--Theileria annulata (Tropical Theileriosis). These ticks and the disease are mainly distributed across northern Africa, southern Europe, the Near East and West Asia. In the latter, small holders, peri-urban dairies and imported cattle in general are the main production systems affected by this complex and it is likely to gain in importance in northern Asia as the dairy sector develops in that region; (iii) Amblyomma spp.--Cowdria ruminantium. This tick species, which transmits heartwater, occurs throughout sub-Saharan Africa. It is particularly important in sheep and goats. This complex is also present in the Caribbean. In addition to heartwater, Amblyomma ticks also facilitate the development of dermatophilosis which is important in West Africa and the Caribbean (Morrow and Koney, 1994). Amblyomma cajennense infestations are locally important in areas of Latin America such as Brazil, Cuba and Mexico. Amblyomma spp. also transmit Theileria mutans, a generally mild disease of cattle found throughout sub-Saharan Africa; (iv) Rhipicephalus spp.--Theileria parva [East Coast fever (ECF), Corridor Disease, January Disease]. It occurs in cattle throughout Eastern, Central and Southern Africa. Other complexes which affect small ruminants, mainly sheep--particularly improved breeds--are Rhipicephalus spp.--Hyalomma spp.--Babesia ovis in Europe, the Mediterranean Basin and West Asia where it has the greatest impact, and H. anatolicum anatolicum--Theileria lestoquardi ( = hirci) which is an important cause of disease and mortality in the Mediterranean Basin, West Asia, the Indian subcontinent and possibly parts of China. The Rhipicephalus spp.--Nairobi sheep disease/Ganjam virus complex can produce serious outbreaks of disease when endemic stability is disturbed. Other livestock species are affected by TTBD but less is known about these although they may be locally very relevant. In Africa, TTBD are particularly important and they are considered the greatest animal disease problem (Young et al., 1988). It is accepted that theileriosis, dermatophilosis and heartwater are the major tickborne or tick-associated diseases of grazing cattle. Babesiosis and anaplasmosis may be important in certain regions and may cause problems in zero-grazing situations. The complexity of determining the direct and indirect economic impact of TTBD and their control is reflected in the fact that only rough estimates are available for the cost of

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some of the components. If one considers these estimates to be reasonably accurate, however, the figures for national as well as global losses are staggering. In Zimbabwe, the cost of acaricides alone for intensive tick control on commercial farms is estimated at US$ 9.63 per animal per year (Pegram et al., 1996), while in Zambia the annual cost was US$12 per animal per year (de Castro et al., 1997). Meltzer et al. (1996) estimated the cost of heartwater in the commercial sector in Zimbabwe as Z$ 19.4 million per annum; this is US$ 10.1 per head, of which US$ 9 were spent on dipping costs only. The only world-wide account of the costs (control expenses + damage) of TTBD in cattle was given by McCosker (1979), who estimated these as ca. US$ 7 billion per year. This calculation was based on Australian figures of A$ 42 million in losses for 1973 in a cattle population of 8.5 million head (ca. A$ 5 per head), multiplied by the world cattle population at risk. An adjustment of these values to current levels using various indices results in a cost per head of cattle of US$ 13-18 at 1996 prices. This estimate was confirmed by using the estimates of McLeod (1995) to a cost per head in Australia of ca. US$ 14. Granted that 80% of the world's cattle population of 1288 million ( F A O / O I E / W H O , 1994) lives in areas of TTBD risk (Snelson, 1975), the global costs of TTBD would now be between US$ 13.9 and 18.7 billion. Although a fairly crude estimate, these values may help us to comprehend the importance of TTBD of cattle; the above figures do not include other livestock. As with other livestock pests and diseases, one important aspect of the impact of TTBD is the loss of potential increased production caused by the hindrance of introduction of livestock production schemes based on exotic, more productive but susceptible stock. Including these indirect losses would make the above estimate even larger.

3. Tick control methods

3,1. Acaricides Earlier acaricides such as arsenic and chlorinated hydrocarbons, known for their high toxicity levels, have been replaced by organophosphates, amidines, synthetic pyrethroids, avermectins, fluazuron--an acarine growth regulator (Junquera et al., 1995)--and, very recently, fipronil, the anti-flea compound developed as acaricide in Brazil. Despite their well-known disadvantages--resistance, environmental pollution, residues in meat, milk, hides and skins and natural toxicity--acaricides are still the backbone of tick control as they are effective both in the short-term by cleaning the animal of ticks and in the long-term in reducing tick burdens. The spread of resistance to synthetic pyrethroids in Boophilus microplus in many parts of the world (Fig. 1) has forced veterinary authorities and farmers to seek new alternatives, such as amitraz and others, increasing the risk of resistance developing to these compounds. This sent a strong signal of the possible limitations of future use of chemical tick control and it is therefore essential that acaricides are managed as a precious but finite natural resource.

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Reported cases of SP resistance

Fig. 1. Reported synthetic pyrethroid resistance in Boophilus microplus. (Source: FAO World Acaricide Resistance Reference Centre, Berlin, Germany).

This should also be seen in the light of the costs of developing a new drug, estimated at an average of US$ 230 million per compound (De Alva, 1995). As expenses are expected to increase even further, companies may not be willing to get involved in the future development of drugs such as acaricides which are mainly marketed in the developing world. Environmental concerns and the need to improve efficacy have led to a concerted effort in the development of new acaricide-delivery methods (pour-on, spot-on, injections, intra-ruminal boluses, etc) which give better control by either targeting particularly damaging tick species or utilising the slow-release technology in addition to a more simple application principle. Further, it should be kept in mind that a number of organophosphorous compounds abandoned after their replacement with the synthetic pyrethroids could still be useful in many parts of the world (D.H. Kemp, personal communication, 1994). Furthermore, amitraz remains a very effective compound throughout most of Australia and Latin America where the problem of acaricide resistance in B. microplus is at its worst. Alternating pesticides is believed to reduce the selection pressure from any one chemical under certain circumstances (Roush and Daly, 1990; Roush, 1993). The real benefits of this approach are being tested in a trial comparing the effect on B. microplus resistance of rotating between an organophosphorous and a synthetic pyrethroid compound (F. Thullner, personal communication, 1996).

3.2. lmmunisation against ticks The use of the host's ability to produce anti-tick antibodies protecting itself partially or totally against ticks was suggested by Galun (1975). Subsequent work (Willadsen et al., 1995) has culminated in the development of a vaccine against B. microplus, based on tick antigen Bm86, which is now commercially available in Australia (TickGARDT~). The vaccine has also been tested in Brazil (Hungerford et al., 1995). This is surely one of the most important developments in tick control in recent years. A similar vaccine, developed and produced in Cuba under the name GAVAC TM, has been tested in Argentina, Brazil, Colombia, Cuba and Mexico (de la Fuente, 1995). Unfortunately,

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efforts to develop a vaccine against 3-host ticks, particularly Rhipicephalus appendiculatus, have been unsuccessful. This continues to be an important area of research at the International Centre of Insect Physiology and Ecology. 3.3. Genetic resistance

Host genetic resistance is life-long and heritable, and the degree of expression depends on the stimulation of the immune response to tick feeding. It varies between individuals, however, and its expression can be affected by external factors such as stress and nutrition. While the within-breed variation in genetic resistance to ticks could potentially be used to breed for resistance, the between-breed differences are well known in cattle, where Bos indicus breeds, in general, show much higher resistance than Bos taurus animals (Utech et al., 1978; de Castro and Newson, 1993). Norval et al. (1997) confirmed differences between breeds in resistance to Amblyomma hebraeum and cautioned against the use of B. taurus in areas where this tick and heartwater occur. A number of other breeds have been investigated for resistance to ticks (Ali and de Castro, 1993; Moran et al., 1996), with similar conclusions. The simplest form of utilisation of host genetic resistance is cross-breeding with B. indicus or other resistant breeds. This option has been successfully applied in Australia and parts of Latin America where European breeds have been replaced by Zebu animals. In some areas farmers are very reluctant to such change, however. In areas of Latin America farmers holding Zebu animals are responding to prevailing market forces and changing to European breeds, with consequent intensification in tick control. In developing countries where 3-host ticks cause problems, the indigenous cattle are already resistant to ticks to a large degree and probably also to some of the tick-borne diseases (TBD). This is often disregarded as productivity is generally believed to be low. Studies in Africa have shown that when the cattle in a herd are ranked for tick resistance, there is a significant cross-immunity between species (Kaiser et al., 1982; de Castro et al., 1991), suggesting that if cattle are selected for resistance against the most important tick species, this will improve the control of other species as well. In addition to the possible use of the resistance of the N'Dama breed to both ticks and trypanosomosis (Mattioli and Cassama, 1995) other suitable breeds, particularly of the Zebu type and their crosses should be promoted in an attempt to increase livestock production in Africa (Alexander et al., 1984; Hayman, 1974; Madalena, 1989). Recently a line of Bos taurus (Hereford X Shorthorn = Adaptaur) with very high and absolute resistance to Boophilus microplus in the presence of environmental stress, was identified. The resistance observed is acquired in early life in the presence of ticks and is stable, lasting for the animal's lifetime under the tick-challenge conditions tested (Frisch, 1994). A major gene is responsible for this phenomenon (Frisch, 1994; Kerr et al., 1994). This obviously represents a major advance in tick control that may have wide applications. 3.4. Tick resistance and disease transmission

Acquired resistance to ticks could possibly interfere with the transmission of disease agents. This phenomenon has been reported for T. annulata in Hyalomma anatolicumresistant cattle (Rubaire Akiiki, 1990) and it is worth further investigation.

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3.5. Management Reduction of the vegetation cover through heavy grazing, burning, etc., will make environmental conditions less favourable, reducing the number of ticks. These techniques are often harmful, however, and are not widely recommended. Zero grazing and other agricultural practices which indirectly reduce tick challenge are widely and successfully used by small-scale dairy farmers to control theileriosis in the highlands of Kenya. The use of grasses Stylosanthes spp. has been suggested; apart from their tick-trapping properties, livestock nutrition would be improved. They are not widely used, however. To have a significant effect on the tick population, they would have to be the only species being cultivated. Pastures can be vacated for periods longer than the survival of the ticks present (2 years for adult Amblyomma and Rhipicephalus, 18 months for Boophilus) or they can be managed effectively through rotational grazing in certain circumstances. These approaches require good fencing and management skills and their application in developing countries is limited, except possibly through the migratory pattern of pastoral peoples. The use of livestock species which are not the natural host for a species, e.g. sheep with regard to Boophilus spp., can reduce tick populations by reducing their opportunities for feeding. In places where there is a need to reduce tick challenge to game animals, cattle herds are used as 'attractants' (' vacuum cleaners') as they can be easily be treated with acaricides.

3.6. Biological control Parasitoids, predators and pathogens exist that target different tick species (Kaaya, 1992). In general, however, these have not until now been successful when used in tick control. A recent report of the successful experimental use of the fungus Metarhizium anisopliae sprinkled on cattle to control B. microplus (Lezama-Gutierrez et al., 1995) requires further investigation. Amblyomma ticks respond to the application of natural or synthetic pheromones to cattle by attaching on those areas where the pheromone has been applied. This finding has enabled the development of the combined use of acaricides and pheromones that is believed to have a potential role in controlling these ticks in a more selective manner and using less acaricide (Norval et al., 1996).

4. Tickborne disease diagnostic and control methods Efficient sustainable TBD control can only be accomplished if the epidemiology is known and reliable diagnosis can be established.

4.1. Diagnostics A number of diagnostic tests for TBD, mostly based on the use of complement fixation, agglutination and fluorescent antibodies, have been available for some time for

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anaplasmosis and babesiosis (Btise et al., 1995; Wright, 1990), heartwater (Du Plessis and Malan, 1987) and theileriosis (Norval et al., 1992). These tests have enabled workers to pertbrm field studies in the epidemiology of these diseases (James et al., 1985; Latif et al., 1995). New tests based on enzyme-linked immunosorbent assay (ELISA) are in different stages of development for anaplasmosis (Duzgun et al., 1988), babesiosis (Jorgensen et al., 1994), heartwater (Martinez et al., 1993) and theileriosis (Musoke et al., 1993a) or validation (Tapang et al., 1990; Echaide et al., 1995). Improved diagnostics (ELISA) enabled Deem et al. (1996) to challenge accepted wisdom in beartwater epidemiology by postulating that vertical transmission from dam to offspring plays an important role in endemic stability. Reliable diagnostics are also an invaluable aid in the developing and monitoring of the effect of new control measures. 4.2. Drug control Effective anti-protozoan drugs are now at hand in case of tick-control failure (Peregrine, 1994) and as an essential aid to treat back-up during TBD immunisation. Resistance to these drugs has not been reported (Peregrine, 1994). 4.3. Immunisation Immunisation against both babesiosis and anaplasmosis is widely used throughout the world. A number of laboratories produce attenuated B. bouis and B. bigemina vaccines. In addition, Anaplasma centrale-based vaccines are successfully used to protect against A. marginale and combined B. bigemina, B. bot~is and A. marginale vaccines are available and used widely in Australia, South Africa, Argentina, Brazil and Uruguay. Although progress has been made on recombinant vaccines for anaplasmosis and babesiosis (Montenegro-James et al., 1992; Harper et al., 1994) no vaccine of this nature is yet available for field use. Difficulties still exist with regard to the development of an appropriate immunisation procedure against heartwater. The traditional Ball 3 strain is being used, particularly in sheep and goats, but its use in cattle is restricted and requires close monitoring. Recently, Mahan (1996) reported successfully immunising sheep with an inactivated vaccine. Tropical theileriosis is prevalent in Northern Africa, Southern Europe, the Near East and West Asia. A schizont-based Theileria annulata vaccine has been available for some time (Pipano, 1990; Grewal et al., 1994) and it is being widely used. Work is also being carried out towards a sporozoite-based vaccine (Dhar et al., 1990) and also sub-unit vaccines (Hall et al., 1990). The infection and treatment method (Radley, 1981) developed for the immunisation of cattle against ECF has successfully been used through the FAO-implemented 'Coordinated Multi-Donor Programme for Integrated Tick and Tick-borne Disease Control in Eastern, Central and Southern Africa' as well as by bilateral projects in Kenya and Zambia. A trivalent vaccine composed of three stocks (Kiambu 5, Muguga and Serengeti transformed) has been successfully used to immunise cattle in Malawi, Tanzania, Uganda and Zambia (Musisi et al., 1992). Local Theileria stocks have been

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equally successfully used in the Eastern province of Zambia, the coast and central highlands of Kenya, and Zimbabwe. The Zimbabwe stock known as 'Boleni' can be used without oxytetracycline treatment which greatly reduces the cost. A similar mild Kenyan stock, 'Lanet', is being tested for its potential application as an immunising agent (Mbogo et al., 1996). The advantages of using the mild stocks are obvious: no need for tetracycline treatment, negligible immunisation reactions. They could therefore prove to be the immunising agents of the future. It is urgent and important, therefore, to evaluate their protecting capability and their safety against other T. parva stocks from different parts of Africa. Regrettably, the positive impact of the infection and treatment method in the livestock sector has been partly jeopardised by the considerable controversy surrounding its use for ECF immunisation almost since the method was developed. The finding that infection with most strains of T. parva, either naturally or following immunisation, may create carrier animals (Young et al., 1981) has been one of the main problems. Imrnunised animals may inadvertently introduce a new strain into other regions through pastoral migration or trade in livestock. The risk that foreign strains could break through the immunity of local animals has been unacceptable for some workers (Brandt et al., 1991). However, no scientific evidence has up till now been presented that the trivalent vaccine has caused problems in any of the countries where it has been used although it is possible that the trivalent vaccine may not protect in all areas and it may need to be modified as its use spreads. The use of local strains has been proposed as an alternative. They may have the advantage of offering better protection to homologous disease challenge in the area. This may be useful in some instances, e.g. on relatively small and homogenous islands such as Zanzibar or Pemba. However, the serious weakness of such an approach is the determination of the boundaries of the area in which the local stock is to be used, i.e. how many immunising stocks for Tanzania, Zambia, etc? Further, it assumes that the field situation is static and fails to take into account increasing movement of cattle, many of which are natural or artificial carders, within and between countries. The finding that an obligatory sexual cycle takes place in T. parva with recombination of genetic material raises the possibility that different parasites may recombine with the possible emergence of several new genotypes Morzaria et al. (1992). Further work is needed to elucidate the relevance of this finding and it may help in the understanding of the epidemiology of T. parva. The disagreement between scientists regarding the use of one or more immunising stock over a wide geographical spectrum vs. the approach of using local stocks has jeopardised the delivery of ECF immunisation to progressive farmers, adding to the estimated US$ 168 million loss that the disease causes in Eastern, Central and Southern Africa (Mukhebi et al., 1992). As the introduction of a new recombinant ECF vaccine for field use is possibly 5 - l 0 years down the road, additional losses can be anticipated if scientists continue to argue and the move towards introducing improved cattle gathers momentum. This problem, therefore, will have to be solved fast by clarifying the protection and cross-protection capabilities of stocks, allowing us to proceed with the only method at our disposal--infection and treatment.

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A T. part,,a sporozoite-derived antigen of 67 kDA, common to different parasite stocks, has been chosen as the most promising antigen for the development of a recombinant vaccine against ECF. Initial trials have revealed that it is able to engender protection against different field stocks (Musoke et al., 1993b). An immunisation schedule has been shown to protect 60-70% of cattle against syringe challenge (Musoke et al., 1992) and two immunisations may improve the observed protection. This vaccine is to be tested in the field (S. Morzaria, personal communication, 1996). These results are very encouraging for the medium to long-term future in the control of ECF. 4,4. Genetic resistance to tickborne diseases

There is less available evidence of genetic resistance to TBD than there is on tick-resistant breeds. Bonsma (1981) reported resistance to A. hebraeum and heartwater in cattle. Preliminary evidence of varying resistance to tropical theileriosis in different cattle breeds has been reported (Preston et al., 1992). Further investigation is required as there would be enormous advantages if cattle breeds resistant to one or more TBD are found (Spooner and Brown, 1991). Furthermore, the reported resistance to TBD in N'Dama cattle (Mattioli and Dempfle, 1995) is promising and requires further investigation.

5. The integration of different control methods 5.1. Justification

Experience has shown that absolute reliance on any one method of controlling ticks often fails to provide efficient, sustainable and long-term control. A good example is heartwater control in Zimbabwe where current control policies based on the extensive use of acaricides at an estimated annual cost of US$ 6.5 million have failed to modify the extent of the heartwater-endemic area (Meltzer et al., 1996). Often no other feasible alternatives exist, and traditional control methods, with all the risks involved, must be accepted while new and more robust approaches making use of a combination of alternatives is found. The integrated approach to TFBD control started in Australia in the 1960s, relying on the use of host resistance to ticks and the development of TBD vaccines. The principles stem from the concept of integrated pest management (IPM) which has been defined as the systematic application of two or more technologies, in an environmentally-compatible and cost-effective manner, to control arthropod pest populations which adversely affect the host species, in our case livestock (Bram, 1994). Tatchell (1992) refers to integrated tick management based on knowledge of tick ecology, economic justification and endemic stability for TBD. The latter has been defined as 'a stable endemic situation with high prevalence of infection but no or little clinical disease in the target population caused by a high transmission rate of the parasites between vector tick and the vertebrate host'. This situation is obtained when: (i) no or minimal tick control is applied and (ii) the offspring is infested early in life. However, in cases where a highly susceptible cattle

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population is introduced a n d / o r highly pathogenic disease agents such as T. parva continue to interact, the situation may remain unstable (Anon, 1990). In Africa, scientists began to re-evaluate TTBD control practices in the 1980s, and a number of studies have demonstrated that often costs of control do not justify the improvement in production achieved (Pegram et al., 1991). A more recent study (de Castro et al., 1997) comparing three control methods--intensive, strategic and no control--has shown that, as expected, traditionally-managed Sanga cattle in Zambia produced better under intensive tick control. However, considering the cost of control, the strategic tick control policy produced the best economic result, followed by the intensive and then the no tick control policies (Table 1). Further, none of these control regimens (based on hand-spraying to control mainly A. variegatum) prevented the transmission of ECF when it was introduced into the area towards the end of the trial. After the introduction of ECF, the study was re-designed and ECF immunisation introduced. The results suggest that immunisation combined with strategic tick control was the most cost-effective way to control ECF in the traditional sector of Zambia (B. Minjauw, personal communication, 1996). Previously, the cost-efficiency of ECF immunisation had only been demonstrated in improved cattle (Mukhebi et al., 1995; Pegram et al., 1996). Further, it appeared that after the 3 years of the trial, animals originally not immunised against ECF withstood lethal challenge, suggesting that the immunisation of cattle in the field may favour the establishment of endemic stability to ECF, the ideal goal in TTBD control. Similar work of integrated TTBD control (Young et al., 1988) has been applied in several African countries, such as Burundi (Kaiser et al., 1988), Zambia (Pegram et al., 1991; de Castro et al., 1997) and Zimbabwe (Pegram et al., 1996). In Latin America, advances have recently been made in understanding the ecology of Boophilus microplus (Nari et al., 1979a), the epidemiology of babesiosis (Martins et al., 1994) the economic losses involved (Guglielmone et al., 1992). The existence of reliable vaccines against anaplasmosis and babesiosis (Nari et al., 1979b) has led to the formulation of integrated tick and TBD control programmes (Nail, 1990 and Nari, 1995; Brizuela et al., 1996). It is essential that these are implemented without delay as

Table 1 Annual production value and tick control costs (US$ per carrying capacity unit) Period Group Cullstock Milk Weanedmale Totalofftake Tickcontrol Net value calves costs of production 1985-1992 1988-1992

T U T U S

47.62 35.36 44.01 25.31 40.74

T: treated with acaricides. U: untreated. S: treated at strategic times. Source: de Castro et al. (1997).

14.25 11.74 14.29 11.11 12.68

29.46 26.48 30.20 26.58 29.41

91.36 73.58 88.50 63.00 82.82

12.15 0 11.91 0 4.10

79.18 73.58 76.59 63.00 78.72

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acaricide resistance in B. microplus is becoming increasingly difficult to manage (Nolan, 1987). 5,2. The choice o f strategy

Workers and scientists in the field generally accept that traditional, chemically-based TI'BD control methods will not work in the long term as they are expensive, environmentally damaging and ticks develop resistance to the chemicals being used. Governments of developing countries are becoming aware that intensive tick control is only justified for the most susceptible European-type cattle. The costs involved and the development of resistance in the tick population have forced most countries to abandon the tick eradication efforts which were still being pursued 10 years ago (FAO, 1987). Argentina, however, still remains committed to its eradication programme. The ideal policy would be to make maximum use of acquired resistance to both Ticks and TBD, modified to suit each individual country, region or ecological zone. This needs to be based on the carefully managed use of acaricides in a strategic or threshold manner, in areas where TBD exist, this should be coupled with the use of immunisation or treatment methods to arrive at endemic stability. Further, they need to be socially acceptable and in agreement with the prevalent management level. The policies should be regularly reviewed and adjusted for any changes (biological, economic, social, climatic, etc). The type of strategy to be implemented in the different regions of the world will depend on a number of important factors. A sound knowledge of vector ecology and disease epidemiology are of great importance but the nature of the fanning system, the general economic situation of the country and socio-economic considerations will also have an important influence in the success of the approach. Budgetary constraints in many countries, particularly in Africa, have caused the breakdown of subsidised tick control and have forced several countries to revise it. However, because of the high costs of tick control under these circumstances, many dairy farmers in Africa and elsewhere have realised that to immunise their dairy cattle, with markedly reduced tick control, is cheaper than paying for the previously subsidised intensive tick control provided by the government (Webb, 1996). 5.3. Models o f uectors and disease

The complexity of the TTBD situation on a global scale means that the use of predictive models to understand the vector-host-disease interactions under different agro-ecological zones is essential. A number of models can be used to predict geographical tick distribution (Sutherst and Maywald, 1985). These models, based on climatic data, have been used to estimate the abundance and distribution of disease vectors (Perry et al., 1991) or to predict the likelihood of vectors--and diseases--becoming established in areas previously free of particular ticks and TBD (Alderink and McCauley, 1988; Norval et al., 1991). The principles and prerequisites for modelling the different TBD have been discussed (Dallwitz et al., 1986) and models have been developed (Byrom and Gettinby, 1992; Haile et al., 1992) on the epidemiology of T. parva and

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Babesia respectively. It is important that the development of models is continued as they will facilitate the formulation of regional control policies reducing the need for field studies (Sutherst et al., 1987). 5.4. The role of FAO

Since its creation in 1945 FAO has led efforts to control animal diseases. The principal objectives of the strategy of the FAO's Animal Health Service (for international animal health) is to secure food supply for a growing human population, to safeguard human health by combating zoonoses and to facilitate domestic and international trade in animals and their products (Anon, 1995). The control of TTBD is contributing to achieving this objective. Moreover, as early as 1956 FAO, as part of its Regular Programme activities, together with OIE, organised the first Expert Consultation to discuss the 'considerable advance in knowledge of tickborne diseases of livestock' reacting to concerns on the increase in animal movement at the time and the potential spread of TI'BD. Since then, a number of meetings have been organised by FAO in order to review progress and seek advice in the field of TI'BD control to be passed on to its member nations. Their outcome has forged FAO's policies regarding TTBD control, resulting in the development of a control programme in East Africa (FAO, 1980). This was later extended to Central and Southern Africa. Likewise, it has helped to establish the on-going A. variegatum eradication programme in the Caribbean (Pegram et al., 1997) and the World Acaricide Resistance Reference Centre (WARRC), as well as a number of reference centres and collaborating institutions throughout the world ( F A O / O I E / W H O , 1994). The WARRC was created to monitor acaricide resistance throughout the world with the use of a standardized and accepted testing technique, the larval packet test (Stone and Haydock, 1962) as well as to disseminate results and assist co-operating countries with the management of acaricide resistance problems. A recent important achievement of the Centre was the development of a resistance test for amitraz (F. Thullner and D.H. Kemp, personal communication, 1996). The recommendations stemming from the most recent FAO Expert Consultation for the control of TTBD applicable to Africa have been reviewed elsewhere (de Castro, 1995); the world-wide control strategies recommended by FAO endorse the integration of current methods, with the goal of more cost-effective policies, based on endemic stability (Anon, 1990). A more recent meeting of experts (Anon, 1995) assessed the relative impact of TTBD by production system and geographic area (Table 2) and defined areas of possible FAO involvement. It concluded that TTBD are of particular importance in certain production systems, such as small-holder mixed farming systems and peri-urban systems, throughout the world. It was perceived that FAO should play a key role in alerting governments and in facilitating and actively assisting in executing impact assessments with a view to implementing appropriate management programmes. 5.5. The implementation of integrated control measures

Tatchell (1992) argued that it was the 'user mentality' that led people to prefer tick control through chemical methods, as they are obviously effective and easy to apply.

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Table 2 The relative importance of TTBD in different production systems by the different geographic regions of the world Production system Periurban--Small Periurban--Large Mixed-farming--Small Mixed-farming--Large Pastoral--Traditional Ranching--Commercial

Africa

WANA

Asia

East

West

C and S

NA

WA

North

SE

South

South

America Carib

H L tt ~ M * M M *

It * L H • L M * L

L M ~ H M ~ M H *

M " I. M : L M L

M * L L L H L

H * M tt * L L L

H * M H 1. L M ~

it * M * H * L L L

M k H ~ H * L It *

M * L L L L L

c and S: Central and Southern; North: China; H: High. NA: North Africa; SE: Pacific; M: Medium. WA: Western Asia; South: India; L: Low in socio-economic importance; Carib: Caribbean. Bold: TBD considered important. FAO to focus on these systems/regions which have medium to high socio-economic potential or contribution, and where TBD are of major importance. Source: Anon (1995).

H o w e v e r , a n u m b e r of limitations need to be reversed in order for IPM to b e c o m e established as an important c o m p o n e n t of livestock production systems. Brain (1994) listed the f o l l o w i n g as having a limiting effect: (i) insufficient funding and support for applied research, demonstration, fundamental infrastructure and implementation; (ii) c u m b e r s o m e , expensive, t i m e - c o n s u m i n g and unclear pesticide regulatory processes; (iii) d e v e l o p m e n t of agricultural policies without considering IPM; and (iv) lack of co-ordination b e t w e e n federal, state and private sectors in research, planning and implementation. Further, livestock owners often p e r c e i v e no e c o n o m i c benefits to c o m p e n s a t e for the increase in m a n a g e m e n t inputs d e m a n d e d by IPM. Difficulties increase w h e n we consider the i m p l e m e n t a t i o n of I P M policies in the d e v e l o p i n g world. As IPM proposals depend mainly on social and cultural factors, economics, eco-climate, livestock production systems and market demands, they are more c o m p l i c a t e d than the simple application of a chemical. It is therefore important that the procedures proposed are not only e c o n o m i c a l l y viable but also simple and robust. They should also be clearly presented to the policy makers and users. Further, the IPM approach in T T B D control should be included in the veterinary training institutions' curricula. The relative importance of other insect pests of livestock (buffalo, tsetse and horn flies, s c r e w - w o r m , etc.) vis-h-vis ticks needs to be taken into account w h e n designing control policies. The use o f synthetic pyrethroids on cattle in tsetse control in Africa and the serious e m e r g e n c e of horn flies throughout Latin A m e r i c a are j u s t two e x a m p l e s of the need to integrate control methods b e y o n d T T B D . The o b s e r v e d southerly m o v e m e n t of non tsetse-transmitted trypanosomosis in Brazil and the potential introduction of A. t,ariegatum into the A m e r i c a s threaten the livestock industry o f those continents. C o m p e t i t i o n b e t w e e n a g r o c h e m i c a l c o m p a n i e s for a share in the ectoparasiticide market currently estimated at about U S $ 500 million per a n n u m - - e x c l u d i n g endecto-

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cides (F. Thullner, personal communication, 1996)--is intense, particularly in developing countries. This often manifests itself in the application of pressure on farmers to use chemicals, often in greater amounts and frequency that would be needed. Although a number of companies are aware of the problem and are making efforts to improve the situation through the International Resistance Action Committee (IRAC) of the International Group of National Associations of Agrochemical Manufacturers (GIFAP), many are not. At government level, things are more complicated. Often the veterinary services support new approaches but are unable to implement them because of lack of resources, for political reasons, or both. Further, interventions by donors and financial institutions often lack co-ordination and do not always offer the right advice. Moreover, control policies are regularly designed without applying IPM principles and the legislation in the different countries is usually outdated considering available scientific advances. This gap interferes with the implementation of the new policies. In general, developing countries are faced with much more pressing problems, mainly of social and economic nature, and unfortunately revision of animal disease control policies is only undertaken when diseases become a major problem either by creating serious losses or by interfering with foreign currency earnings. 5.6. The need f o r a global network

Today we have at our disposal a number of efficient remedies for significantly reducing losses caused by TTBD, with the possible exception of heartwater and dermatophilosis. This ability could be enhanced with improvements in the availability of a heartwater vaccine, a recombinant Theileria vaccine and the utilization of genetic tick-resistance together with more reliable TBD and acaricide-resistance diagnostic methods and a better understanding of epidemiology. However, this is not sufficient unless it goes together with increased awareness of the problem and the appropriate solutions in the relevant sector of government. A number of universities, research institutions and national and international organisations are currently engaged in various aspects of TTBD work. Often research and the application of technological advances are driven by small research groups or private companies which prefer to impose their products/vaccines on the market. Further, they are frequently highly focused on one disease or even one specific aspect of a disease and may have a narrow view of the field problems. As TTBD control moves into the era of integration, there is a need for a responsible and co-ordinated global approach to the problem. Considering the complexity of IPM, dialogue between the different partners in the control of TTBD is needed. The agrochemical industry up till now has not been much involved in this. FAO has initiated contacts with the relevant members of industry through a meeting held in Rome in 1995. The meeting stimulated the organisation of an Ectoparasite Resistance Working Group among industry. It also recommended the creation of the framework for a Tick and Tick-borne Diseases Working Group which will operate under the FAO umbrella. The group will be composed of FAO, the International Resistance Action Committee of the International Group of National

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Associations of Agrochemical Manufacturers, ILRI and representatives of relevant universities, research institutes, national governments and other non-governmental organisations. Broadly, the group would be concerned with regulatory matters, education, research and delivery of technology to users. The future of TTBD control rests on reaching an equilibrium between the host, the parasite, the vector and the environment. The past situation where methods were applied that kept the host alive regardless of the other factors and the costs involved are coming to an end. The new approach of integrated TTBD control is the way to the future. It is a more complex strategy with multiple inter-related components that need to be applied in the right amounts at the right times. Unless a coordinated and responsible effort is made, the new technology will not reach the farmers. The challenge to scientists in this field is to work together to develop practical, imaginative and cost-effective packages of TTBD control and, perhaps equally importantly, to learn how to market them.

Acknowledgements C.G.D. Brown, J.E. George, A.D. Irvin. R.G. Pegram, B.D. Perry, R.J. Tatchell, F. Thullner, G. Uilenberg, J.E. Vercoe and P. Willadsen, greatly contributed to the ideas contained in the final part of the paper during the meeting of experts held in Rome in November 1995. The author is also grateful to J.W. Hansen for his criticism of the manuscript.

References Alderink, F.J. and McCauley, E.H., 1988. The probability of the spread of Amblyomma variegatum in the Caribbean. Prevent. Vet. Med, 6: 285-298. Alexandratos, N., 1995. World Agriculture: Towards 2010, An FAO Study. FAO, Rome. Wiley, Chichester. 488 pp. Alexander, G.I., Reason, G,K. and Clark, C.H., t984. The development of the Australian Friesian Sahiwal. A tick-resistant dairy breed. World Anita. Rev.. 51: 27-34. Ali, M. and de Castro, J.J., 1993. Host resistance to ticks (Acari: Ixodidae) in different breeds of cattle at Bako, Ethiopia. Trop. Anim. Hlth Prod., 25: 215-222. Anon, 1990. Report of the FAO Expert Consultation on Revision of Strategies for the Control of Ticks and Tick-borne Diseases. Rome, 25-29 September 1989. Parassitologia, 32: 3-12. Anon, 1995. FAO strategy for international animal health. World Anita. Rev,, 84/85: 25-31. Bonsma, J.C., 1981. Breeding tick-repellent cattle. In: G.B. Whitehead and J.D. Gibson (Editors). Tick Biology and Control: Proceedings of an International Conference in Grahamstown. 27-29 January, 1981. Tick Research Unit. Rhodes University, Grahamstown, pp. 67-77. B6se, R., Jorgensen W.K., Dalgliesh, R.J., Friedhoff. K,T. and de Vos, A.J., 1995. Current state and future trends in the diagnosis of babesiosis. Vet. Parasitol., 57: 61-74. Bram, R.A., 1994. Integrated control of ectoparasites. In: Ectoparasites of animals and control methods. Rev. Sci. Techn, Off. Int. Epiz., 13: 1357-1365. Brandt, J., Geysen, D. and Berkvens, D., 1991. (Untitled). Equator, 3: 7-8. Brizuela, C.M., Ortellado, C.A., Sanchez, T.I., Osorio, O. and Walker, A.R.. 1996. Formulation of integrated control of Boophilus microplus in Paraguay: analysis of natural infestations. Vet. Parasitol., 63: 95-108.

J.J. de Castro/Veterinary Parasitology 71 (1997) 77-97

93

Byrom, W. and Gettinby, G., 1992. Using the computer model ECFXPERT to study ticks and East Coast fever. Insect Sci. Applic., 13: 527-535. Dallwitz, M.J., Young, A.S., Maboney, D.F. and Sutherst, R.W., 1986. Comparative epidemiology of tick-borne disease with special emphasis on modelling. In: M.J. Howell (Editor). Parasitology Quo Vadit. Australian Academy of Science, Canberra, pp. 629-637. Echaide, S.T. Echaide, I.E., Gaido, A.B., Mangold, A.J., Lugaresi, C.I., Vanzini, V.R. and Guglielmone, A.A., 1995. Evaluation of an enzyme-linked immunosorbent assay kit to detect Babesia bouis antibodies in cattle. Prevent. Vet. Med., 24: 277-283. De Alva, R., 1995. Creating new products for animal health. In: S. Rodriguez Camarillo and H. Fragoso Sanchez, (Editors). Tercer Seminario Internacional de Parasitologia Animal. Acapulco, Mexico, 11-13 octubre de 1995, pp. 86-87. de Castro, J.J., 1995. Worldwide FAO activities in the field of tick and tick-borne disease control with a summary of recommendations from recent workshops. In: A.D. Irvin, C.G. Stewart and G. Uilenberg (Editors). Tick and Tick-borne Diseases of Africa, Report on a Workshop held at the Onderstepoort Veterinary Institute, South Africa, 4-7 September 1995, pp, 21-28. de Castro, J.J., Capstick, P.B., Nokoe, S., Kiara, H., Rinkanya, F., Slade, R., Okello, O. and Bennun, L., 1991. Towards the selection of cattle for tick resistance in Africa. Exp. Appl. Acarol., 12: 212-227. de Castro, J.J. and Newson, R.M., 1993. Host resistance in cattle tick control. Parasitol. Today, 9: 13-17. de Castro, J.J., James, A.D., Minjauw, B., Di Giulio, G.U., Pertain, A., Pegram., R.G., Chizyuka, H.G.B. and Sinyangwe, P., 1997. Long-term studies on the economic impact of ticks on cattle in Zambia. Exp. Appl. Acarol., 21: 3-19. Deem, S.L., Norval, R.A.I., Yonov, T., Peter, T.F., Mahan, S.M. and Burridge, M.J., 1996. The epidemiology of heartwater: establishment and maintenance of endemic stability. Parasitol. Today, 12: 402-405. de la Fuente, J., 1995. Recombinant vaccines for the control of cattle tick. Monograph, Elphos Scientia, La Habana, 241 pp. Dhar, S., Malhotra, D.V., Bhushan, C. and Gautam, O.P., 1990. A study on quantum of infection for immunization against bovine tropical theileriosis by infection and treatment method. Ind. J. Parasitol., 14: 237-238. Du Plessis, J.L. and Malan, L., 1987. The application of the indirect fluorescent antibody test in research on heartwater. Onderstepoort J. Vet. Res., 54: 319-325. Duzgun, A., Schunter, C.A., Wright, I.G., Leatch, G. and Waltisbuhl, D.J., 1988. A sensitive ELISA technique for the diagnosis of Anaplasma marginale infections. Vet. Parasitol., 29: i-7. FAO, 1980. East Coast fever and related tick-borne diseases. Selected reprint of papers. FAO Animal Production and Health Paper, 19, 982 pp. FAO, 1987. The Eradication of Ticks. Proceedings of the Expert Consultation on the eradication of ticks with special Reference to Latin America, 22-26 June 1987, Mexico City. FAO Animal Production and Health Paper, 75, 322 pp. FAO, 1994. Tick and Tickborne Diseases of Sheep and Goats. Report of the FAO First Expert Consultation. FAO, Rome, Italy, 29-30 September 1994, 14 pp. FAO, 1996. Food Requirements and Population Growth. WFS 96/TECH/10. Provisional Version of Technical Paper for the World Food Summit, 60 pp. FAO/OIE/WHO, 1994. Animal Health Yearbook, 250 pp. Frisch, J.E., 1994. Identification of a major gene for resistance to cattle ticks. Proc. of the 5th World Congress of Genetics and Applied Livestock Production, 20: 293-295. Galun, R., 1975. Research into alternative arthropod control measures against livestock pests (Part I). In: Proceedings of a Workshop on the Ecology and Control of Ectoparasites on Bovines in Latin America, CIAT, Colombia, 25-30 August 1975, pp. 155-162. Grewal, A.S., Avtar, S., Kondal, J.K., Jyotika, K. and Talwar, G.P., 1994. The development and trials of attenuated Theileria annulata parasitized bovine lymphoblasts. In: K.V.S. Rao and V.S. Chauhan (Editors). Recombinant and synthetic vaccines. Springer Verlag, Berlin, pp. 45-49. Guglielmone, A.A., Aguirre, D.H., Spath, E.J.A., Gaido, A.B., Mangold, A.J. and De Rios, L.G., 1992. Long-term study of incidence and financial loss due to cattle babesiosis in an Argentinian dairy farm. Prevent. Vet. Med., 12: 307-312. Haile, D.G., Mount, G.A. and Cooksey, L.M., 1992. Computer simulation of Babesia boris (Babes) and B.

J..I. de Castro/Veterinary Parasitology 71 (1997) 77-97

94

bigemina (Smith and Kilborne) transmission by Boophilus cattle ticks (Acari: Ixodidae). J. Med. Entomol., 29: 246-258. Hall, F.R., Williamson, S., Brown, C.G.D., Hussain, K., Tait, A. and Shiels, B.R., 1990. Genes and vaccines in Theileria annulata. In: Dolan, T.T. (Editor). Recent developments in the research and control of Theileria annulata. ILRAD, Nairobi, Kenya, pp. 89-93. Harper, G.S., Riddles, P.W., Waltisbuhl, D.J. and Wright, I.G., 1994. Applications of recombinant DNA technologies in the development of a vaccine: examples in the development of a vaccine against Babesia. In: P.R. Wood, P. Willadsen, J.E. Vercoe, R.M. Hoskinson and D. Demeyer (Editors). Vaccines in Agriculture: Immunological Applications to Animal Health and Production. CSIRO Information Services, East Melbourne, pp. 161-169. Hayman, R.H., 1974. The development of the Australian Milking Zebu. World Animal Rev., I 1: 31-35. Hungerford, J., Pulga, M., Zwtsch, E. and Cobon, G., 1995. Efficacy of TickGARD TM in Brazil. In: S. Rodriguez Camarillo and H. Fragoso Sanchez (Editors). Tercer Seminario Internacional de Parasitologia Animal. Acapulco, Mexico, 11-13 octubre de 1995, p. 139. James. A.M., Coronado, A., Lopez, W., Melendez, R. and Ristic, M., 1985. Seroepidemiology of bovine anaplasmosis and babesiosis in Venezuela. Trop. Animal Health Prod., 17: 9-18. Jorgensen W.K., Dalgliesh R.J. and de Vos, A.J., 1994. Methods for diagnosis of babesiosis in developing countries. Present and future trends. In: G. Uilenberg, A. Permin and J.W. Hansen (Editors). Use of Applicable Biotechnological Methods for Diagnosing Haemoparasites. Proc. Expert Consultation, Merida, Mexico, 4 - 6 October 1993. FAO, Rome, pp. 65-84. Junquera, P., Correa, 1., Schmid, H.R., Friedel, T.F. and Hausermann, E.A., 1995. Fluazuron, a new tick development inhibitor for the control of cattle ticks. In: S. Rodriguez Camarillo and H. Fragoso Sanchez (Editors). Tercer Seminario Internacional de Parasitologia Animal. Acapulco, Mexico, 11-13 octubre de 1995, p. 142. Kaaya, G.P., 1992, Non-chemical agents and factors capable of regulating tick populations in nature: a mini review. Insect Sci. Applic., 13: 587-594. Kaiser, M.N., Sutherst, R.W. and Bourne, A.S., 1982. Relationship between ticks and zebu cattle in southern Uganda. Trop. Anita. Hlth Prod., 14: 63-74. Kaiser, M.N., Sutherst, R.W., Bourne, A.S., Gorissen, L. and Floyd, R.B., 1988. Population dynamics of ticks on Ankole cattle in five ecological zones in Burundi and strategies for their control. Prevent. Vet. Med., 6: 199-222. Kerr, R.J., Frisch, J.E. and Kinghorn, B.P., 1994. Evidence lbr a major gene for tick resistance in cattle. Proc. 5th World Congress of Genetics and Applied Livestock Production, 20: 265-268. Latif, A.A., Rowlands, G.J., Punyua, D.K., Hassan, S.M. and Capstick, P.B., 1995. An epidemiological study of tickborne diseases and their effects on productivity of Zebu cattle under traditional management on Rusinga Island, Western Kenya. Prevent. Vet, Med., 22: 169-181. Lezama-Gutierrez, R., Galindo-Velazco, E. and Cruz-Cobian, F., 1995. Effectiveness of the entomopathogenic fungus Metarhizium anisopliae in the biological control of ticks in bovine livestock, in field conditions. In: S. Rodriguez Camarillo and H. Fragoso Sanchez (Editors). Tercer Seminario Internacional de Parasitologia Animal. Acapulco, Mexico, 11-13 octubre de 1995, p. 145. Mack, S., 1990. Strategies for sustainable animal agriculture in developing countries. Proceedings of the FAO Expert Consultation held in Rome, Italy 10-14 December 1990. FAO Animal Production and Health Paper, 107,271 pp. Madalena, F., 1989. Cattle breed resource utilization for dairy production in Brazil, Rev. Brasil. Genet., 12, 183-220. Mahan, S., 1996. Successful protection of sheep against heartwater in the field by an inactivated vaccine. The Tick-ler I: 1. Martinez, D., Coisne, S., Sheikboudon, C. and Jongejan, F., 1993. Detection of antibodies to Cowdria ruminantium in the serum of domestic ruminants by indirect ELISA. Rev. Elev. M6d. V~t. Pays. Trop., 46: 115-120.

Martins, J.R., Correa, B.L., Cereser, V.H., Arteche, C.C.P. and Guglielmone, A., 1994. Some aspects of the epidemiology of Babesia boris in Santana do Livramento, Southern Brazil. Rev. Brasil. Parasitol. Vet., 3: 75-78.

J.J. de Castro/Veterinary Parasitology 71 (1997) 77-97

95

Mattioli, R.C. and Dempfle, L., 1995. Recent acquisitions on tick and tick-borne disease resistance in N'Dama (Bos taurus) and Gobra zebu (Bos indicus) cattle. Parassitologia, 37: 63-67. Mattioli, R.C. and Cassama, M., 1995. Comparison of characteristics of life cycle in female ticks collected on N'Dama and Zebu cattle. Trop. Anim. Hlth Prod., 27: 150-154. Mbogo, S.K., Kariuki, D.P., Ngumi, P.N. and McHardy, N., 1996. A mild Theileria parva parasite with potential for immunisation against East Coast fever. Vet. Parasitol., 61: 41-47. McCosker, P.J., 1979. Global aspects of the management and control of ticks of veterinary importance. Recent Adv. Acarol., 11: 45-53. McLeod, R.S., 1995. Costs of major parasites to the Australian livestock industries. Int. J. Parasitol., 25: 1363-1367. Meltzer, M.I., Perry, B.D. and Donachie, P.L., 1996. Mortality percentages related to heartwater and the economic impact of heartwater disease on large-scale commercial farms in Zimbabwe. Prevent. Vet. Med., 26: 187-199. Montenegro-James, S., Toro, M., Leon, E., Guillen, A.T., Lopez, R. and Lopez, W., 1992. Immunization of cattle with an inactivated polyvalent vaccine against anaplasmosis and babesiosis. Ann. NY Acad. Sci., 653: 112-121. Moran, M.C., Nigarura, G. and Pegram, R.G., 1996. An assessment of host resistance to ticks on cross-bred cattle in Bumndi. Med. Vet. Entomol., 10: 12-18. Morrow, A.N. and Koney, E.B.M., 1994. Proceedings of a Workshop on the Control of Amblyomma variegatum and Associated Diseases held in Accra, Ghana on 4 November 1994. Edinburgh University Press, Edinburgh, 89 pp. Morzaria, S.P., Young, J.R., Spooner, P.R., Dolan, T.T., Young, A.S. and Bishop, R.P., 1992. Evidence of a sexual cycle in Theileria parva and characterisation of recombinants. In: Munderloh, U.G. and Kurtti, T.J. (Editors). First Int. Conf. Tick-borne Pathogens at the Host-Vector Interface--An Agenda for Research: Proceedings and Abstracts. University of Minnesota, College of Agriculture, St. Paul, MN, pp. 71-74. Mukhebi, A.W., Kariuki, D.P., Mussukuya, E., Mullins, G., Ngumi, P.N., Thorpe, W. and Perry, B.D., 1995. Assessing the economic impact of immunisation against East Coast fever: a case study in Coast Province, Kenya. Vet. Rec., 137: 17-22. Mukhebi, A.W., Perry, B.D. and Kruska, R., 1992. Estimated economics of theileriosis control in Africa. Prevent. Vet. Med., 12: 73-85. Musisi, F.L., Quiroga, J.C., Mutugi, J., Jacobsen, P., de Castro, J.J. and Di Giulo, G., 1992. Immunisation against ECF: Recent experiences with the trivalent vaccine in East and Central Africa. In: R.W. Paling (Editor). Programme and Abstracts of 3rd Symposium on Tropical Animal Health and Production: Bovine Theileriosis, Faculty of Veterinary Medicine, Utrecht University, The Netherlands, 9 October 1992, pp. 26-32. Musoke, A.J., Morzaria, S.P., Nkonge, C., Jones, E. and Nene, V., 1992. A recombinant sporozoite surface antigen of Theileria parva induces protection in cattle. Proc. Nat. Acad. Sci., USA, 89: 514-518. Musoke, A.J., Katende, J.M., Toye, P.G., Skilton, R.A., lams, K.P., Nene V. and Morzaria, S.P., 1993a. Progress towards development of an antibody detection ELISA for the diagnosis of Theileria parva. In: Expert Consultation on the Use of Applicable Biotechnological Methods for Diagnosing Haemoparasites in Merida, Mexico, October 1993, pp. 174-181. Musoke, A.J., Nene, V. and Morzaria, S.P., 1993b. A sporozoite-based vaccine for Theileria parva. Parasitol. Today, 9: 385-388. Nari, A., 1990. Methods currently used for the control of one-host ticks: their validity and proposals for future control strategies. Parassitologia, 32: 133-143. Nari, A., 1995. Strategies for the control of one-host ticks and relationship with tick-borne diseases in South America. Vet. Parasitol., 57: 153-165. Nari, A., Cardozo, H., Berdie, J. and Canabez, F., 1979a. Estudio preliminar sobre la ecologla del Boophilus microplus (Can) en Uruguay. Ciclo no parasitario en un ~ea considerada poco apta para su desarrollo. Vet. Uruguay, 15: 25-31. Nari, A., Solari, M.A. and Cardozo, H., 1979b. Hemovacuna para el control de Babesia spp. y Anaplasma marginale en el Uruguay. Vet. Uruguay, 15: 137-148. Nolan, J., 1987. Strategies to contain and eliminate outbreaks of acaricide resistance. In: The Eradication of

96

J.J. de Castro/Veterinary Parasitology 71 (1997) 77-97

Ticks. Proceedings of the Expert Consultation on the eradication of ticks with special Reference to Latin America, 22-26 June 1987, Mexico City. FAO Animal Production and Health Paper, 75: 186-195. Norval, R.A.I., Perry, B.D., Gebreab, F. and Lessard, P., 1991. East Coast fever: a problem of the future for the horn of Africa? Prevent. Vet. Med., 10: 163-172. Norval, R.A.I., Perry, B.D. and Young, A.S., 1992. The reporting, diagnosis and surveillance of theileriosis. In: The Epidemiology of Theileriosis in Africa. Academic Press, San Diego, CA, pp. 231-278. Norval, R.A.I., Sonenshine, D.E., Allan, S.A. and Burridge, M.J., 1996. Efficacy of pheromone-acaricide-impregnated tail-tag decoys for controlling the bont tick, Amblyomma hebraeum (Acari: Ixodidae) on cattle in Zimbabwe. Exp. Appl. Acarol., 20 31-46. Norval, R.A.I., Sutherst, R.W. and Kerr, J.D, 1997. Infestations of the bont tick Amblyomma hebraeum, (Acari: Ixodidae) on different breeds of cattle in Zimbabwe. Exp. Appl. Acarol. Pegram, R.G,, James, A.D., Bamhare, C., Dolan, T.T., Hove, T., Kanhai, G.K. and Latif, A.A., 1996. Effects of immunisation against Theileria part~a on beef cattle productivity and economics of control options. Trop. Anim. Hlth Prod., 28:99-111. Pegram, R.G., James, A.D., Oosterwijk, G.P.M., Killorn, K.J., Lemche, J., Ghirotti, M., Tekle, Z., Chizyuka, H.J.B., Mwase, E.T. and Chizyuka, F., 1991. Studies on the economics of ticks in Zambia. Exp. Appl. Acarol., 12: 9-26. Pegram, R.G., Rota, A., Onkelinx, R., Wilson, D.D., Bartlette, P., Nisbett, B.S., Swanston, G., Vanterpool, P. and de Castro, J.J., 1997. The eradication of the Tropical Bont Tick from the Caribbean. World Anim. Rev., 87: 56-65. Peregrine, A.S., 1994. Chemotherapy and delivery systems: haemoparasites. Vet. Parasitol., 54: 223-248. Perry, B.D., Kruska, R., Lessard, P., Norval, R.A.I., Kundert, K. and Hugh-Jones, M., 1991. Estimating the distribution and abundance of Rhipicephalus appendiculatus in Africa. Prevent. Vet. Med., 11: 261-268. Pipano, E., 1990. Vaccination of cattle against Theileria annulata using culture-derived schizonts. In: T.T. Dolan (Editor). Recent Developments in the Research and Control of Theileria annulata. ILRAD, Nairobi, pp. 47-58. Preston, P.M., Brown, C.G.D., Bell-Sakyi, L., Richardson, W. and Sanderson, A., 1992. Tropical theileriosis in Bos taurus and Bos taurus cross Bos indicus calves: response to infection with graded doses of sporozoites of Theileria annulata. Res. Vet. Sci., 53: 230-243. Radley, D.E, 1981. Infection and treatment immunization against theileriosis. In: A.D. lrvin, M.P. Cunningham and A.S. Young (Editors). Advances in the Control of Theileriosis: Proceedings of an International Conference Held at ILRAD, Nairobi, 9-13 February, 1981. Martinus Nijhoff Publishers, The Hague, pp. 227-236. Roush, R.T., 1993. Occurrence, genetics and management of insecticide resistance. Parasitol. Today, 9: 174-179. Roush, R.T. and Daly, J.C., 1990. The role of population genetics in resistance research and management. In: R.T. Roush and B.E. Tabashnik (Editors). Pesticide Resistance in Arthropods. Chapman Hall, London, pp. 97-152. Rubaire Akiiki, C.M., 1990. The effects of bovine tick resistance on the susceptibility of Hyalomma anatolicum anatolicum to infection with Theileria annulata (Ankara). Vet. Parasitol., 34: 273-288. Sansoucy, R., 1995. Livestock--a driving force for food security and sustainable development. World Anim. Rev., 84/85: 5-17. Snelson, J.T., 1975. Animal ectoparasites and disease vectors causing major reductions in world food supplies. FAO Plant Protect. Bull., 23: 103-117. Spooner, R.L. and Brown, D., 1991. Theileriosis and evidence for genetic resistance. In: J.B. Owen and R.F.E. Axford, (Editors). Breeding for Disease Resistance in Farm Animals. CAB International, Farnham Royal, pp. 235-243. Stone, B.F. and Haydock, K.P., 1962. A method for measuring the acaricide susceptibility of the cattle tick Boophilus microplus (Can.). Bull. Entomol. Res., 53: 563-578. Sutherst, R.W., Floyd, R.B., Maywald, G.F. and Dallwitz, M.J., 1987. Modelling tick populations. 1. Introduction. In: R.W. Sutherst (Editor). Ticks and Tick-borne Diseases: Proceedings of an International Workshop on the Ecology of Ticks and the Epidemiology of Tickborne Diseases held at Nyanga, Zimbabwe, 17-21 February 1986. AC1AR Proceedings No. 17, Canberra, pp. 36-38.

J.J. de Castro/Veterinary Parasitology 71 (1997) 77-97

97

Sutherst, R.W. and Maywald, G.F., 1985. A computerised system for matching climates in ecology. Agric. Ecosyst. Env., 13: 281-299. Tapang, P., Kakoma, I. and Brodie, B., 1990. Validation of the dot-enzyme lined immunosorbent for bovine anaplasmosis. Trop. Vet., 8: 65-72. Tatchell, R.J., 1992. Ecology in relation to integrated tick management. Insect Sci. Applic., 13: 551-561. Utech, K.B.W., Wharton, R.H. and Kerr, J.D., 1978. Resistance to Boophilus microplus (Canestfini) in different breeds of cattle. Austr. J. Agric. Res., 29: 885-895. Webb, J., 1996. Risky business. New Sci., 149: 32-35. Willadsen, P., Cobon, G., Hungerford, J. and Smith, D., 1995. The role of vaccination in current and future strategies for tick control. In: S. Rodriguez Camarillo and H. Fragoso Sanchez (Editors). Tercer Seminario Internacional de Parasitologia Animal. Acapulco, Mexico, 11-13 octubre de 1995, pp, 88-100. Wright, I.G., 1990. Immunodiagnosis of and immunoprophylaxis against the haemoparasites Babesia sp. and Anaplasma sp. in domestic animals. Rev. Sci. Techn. Off. Int. Epiz., 9: 345-356. Young, A.S., Groocock, C.M. and Kariuki, D.P., 1988. Integrated control of ticks and tickborne diseases of cattle in Africa. Parasitol., 96: 403-432. Young, A.S. Leitch, B.L. and Newson, R.M., 1981. The occurrence of Theileria parva carrier state in cattle from an East Coast fever endemic area of Kenya. In: A.D. Irvin, M.P. Cunningham and A.S. Young (Editors). Advances in the Control of Theileriosis. Martinus Nijhoff, The Hague, pp. 60-62.