Parasites, animal production and sustainable development

ELSEVIER Veterinary Parasitology 54 (1994) 27-47

veterinary parasitology

Parasites, animal production and sustainable development

A.D. D o n a l d

Institute of Animal Production and Processing, CSIRO, P.O. Box 93, North Ryde, N.S. W. 2113, Australia

Abstract

Ecologically sustainable development is aimed at reducing environmental degradation while enabling economic development with equity between the developed and developing worlds and between generations. Parasite control in livestock can both contribute to, and take advantage of, sustainable agriculture. This will tend towards less intensive, lower input, diversified crop and animal production with less risk of parasite-induced losses and greater opportunities for integrated control including the exploitation of grazing management. Chemotherapy will continue to play a part but the most serious problem is resistance in the target species. Except for a few isolated issues, currently used parasiticides are relatively minor contaminants of the food supply or the environment. Nevertheless, the compounds of the future will need to be narrow-spectrum, non-persistent and rapidly degraded, with convenience in the hands of the user reduced in importance. Environmentally friendly alternatives to chemotherapy, including genetic resistance of hosts, vaccines, and biological control, show considerable promise and must be pursued. Sustainable systems pose optimisation problems and more attention must be given to systems research, models and products to aid decisions. If governments are serious about sustainable development, greater support will be needed for longer-term patient, multi-disciplinary research.

Keywords: Sustainable development; Chemotherapy; Resistance

I. Introduction

Ecologically sustainable deve lopment has become a concept of major interna- t ional impor tance following the release in 1987 o f the Repor t o f the World Com- mission on Env i ronment and Deve lopment (WCED, 1987 ) t i t led 'Our C o m m o n Future ' . The so-called Brundt land Repor t def ined sustainable development as that which "meets the needs o f the present without comprising the ability of fu-

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ture generations to meet their own needs". It particularly emphasised the integra- tion of environmental and economic objectives to ensure sustainable development of economic and social systems, with a strong emphasis on equity between the developed and developing worlds and between generations. It advocated a new era of economic growth as essential to relieve poverty in the developing world, but one that is "less material- and energy-intensive" and "based on policies that sustain and expand the environmental resource base". Although infant mortality has fallen and human life expectancy has expanded while global food production has increased faster than population growth, there are increasing numbers of hun- gry people, a widening gap between rich and poor, and environmental failures such as land degradation, destruction of forests, acid rain, global warming, ozone depletion and chemical pollution.

The substance of the Report is concerned with directions for policy change across a wide range of issues and was the impetus behind the United Nations Conference on Environment and Development (UNCED) attended by world leaders in Rio de Janeiro in 1992. At UNCED, Climate Change and Biodiversity Conventions were signed by more than 150 countries and will come into force when ratified by 50 and 30 countries, respectively. The Conference also endorsed Agenda 21, a plan to deal with the most urgent problems of environmental degradation and human development into the next century. It includes actions to foster integrated pest and disease management and to promote applications of biotechnology to develop resistance to diseases and pests, improve diagnostic techniques and vaccines for the control of animal diseases, and minimise the re- quirement for "unsustainable synthetic chemical input".

Global sustainable development encompasses lofty ideals which will be difficult to attain. However, their most important effect is to alert us to the urgency and magnitude of the world's problem, and to the realisation that some of the concerns of the environmental and consumer movements in the developed world---even though they have the political and market power to have them attended to--seem trivial by comparison with those confronting many developing countries. Parasite control in livestock is not a first-order problem in sustainable development but it is a component of most sustainable animal production systems. As a World Association it is worthwhile for us to better define our potential contribution within a broad understanding of the global problem.

2. Agriculture, food security and animal production

The world currently produces more food per head of population than ever be- fore and at a global rate of increase that is still greater than the rate of population increase. This is due to phenomenal increases in productivity, due mainly in turn to large increases in inputs, but there are large differences in food production sufficiency between regions and countries. There is also widespread land degradation resulting from increased land clearance, cropping and grazing in marginal lands, insufficient fertiliser use or lack of appropriate livestock and crop manage-

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ment. In input-intensive systems, agricultural chemicals have played a large part in production increases since 1945, but this has resulted in contamination of soil and water by fertilisers and pesticides, and of plant and animal products by residues. Overuse of pesticides threatens the health of humans and other species and has increased pesticide resistance. Nevertheless, except for resistance to internal and external parasiticides, the adverse consequences of excessive chemical inputs is of much less importance in animal compared with crop production.

The demand for meat and milk has been growing as incomes rise and a great deal of agricultural development in industrialised nations is devoted to meeting these needs. The rising demand for livestock feedgrains accounted for two-thirds of the increase in grain production in North America and Europe from 1950 to 1985, and the total biomass of domestic livestock on the planet is greater than that of people! To meet the food needs of an ultimate world population of about 12.5 billion there will need to be considerable improvements in traditional agriculture and some changes in food habits. This is likely to mean reduced consumption of animal products, particularly those from production systems which con- vert plant products of relatively high nutritive value suitable for direct human consumption. However, ruminants play a crucial part in the conversion to high quality human food of low quality plant material in the world's extensive grass- lands. Farm animals in general also make the same conversion of by-products and wastes as well as returning valuable plant nutrients to the soil in the more intensive mixed crop-livestock systems, which have many inherently sustainable properties. It is easy to overlook the huge importance of draught animal power in food production in the developing world. Moreover, the need is not only to feed more people but also to attack under-nourishment. In the developing world the immediate focus is necessarily on staple foods such as foodgrains and starchy roots as sources of calories, but a high rate of growth of protein availability is also needed from animal products such as milk, meat and fish as well as from pulses and oilseeds.

There are also non-food products from the land such as timber and pulp from forests, and textile fibres such as cotton, linen, jute, and from animals, wool, cash- mere and mohair. These are affected by the same agricultural sustainability issues as food production but, in addition, the textile fibres are competing with synthetic fibres on sustainability and environmental as well as economic grounds. Synthetic fibres are produced from non-renewable fossil fuels by large scale chemical synthesis which emits compounds such as nitrous oxide or carbon di- sulphide as potential atmospheric pollutants. Superficially, they would seem to be less environmentally friendly than the production of 'natural' fibres such as cotton and wool. However, cotton production has been associated with intensive application of insecticides, herbicides, fertilisers and irrigation with the risk of pollution of irrigation 'tail water' and ground water. Similarly, the application of insecticides to sheep for the control of ectoparasites has the potential to leave significant residues in shorn greasy wool if applied too close to shearing.

Sustainable development is a difficult compromise between reducing environmental degradation while enabling economic growth. This compromise, particu-

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larly in the developing world, is needed not only to improve the lives of those living there, but also to help people and governments to reduce current consumption while investing in environmental remediation and protection for the benefit of future generations. We are used to arguments in the developed world aimed at avoiding the use of chemical agents in parasite control, but the Brundtland Re- port argues for sensible compromise:

"Many countries can and should increase yields by greater use of chemical fertilisers and pesticides, particularly in the developing world. But countries can also improve yields by helping farmers to use organic nutrients more efficiently. Hence governments must encourage the use of more organic plant nutrients to complement chemicals. Pest control must also be based increasingly on the use of natural methods." (WCED, 1987, p. 135).

3. Organic farming

In some contrast to the global compromise, this is a movement predominantly in the developed world, based on the complete avoidance of synthetic inputs to agriculture. It is supported by a small but growing consumer demand prepared to pay a premium for certified organically produced products. The principles of organic agriculture include working with natural systems, enhancing biological cycles, maintaining soil fertility with the minimum of non-renewable resources, protecting the environment and attending to animal welfare. There are voluntary associations in many countries fostering organic agriculture and an International Federation of Organic Agriculture Movements (IFOAM), founded in 1972, with its headquarters in Germany and member organisations in nearly 70 countries. It has published Basic Standards of Organic Agriculture (IFOAM, 1989 ). Other non-government organisations as well as governments in a number of countries have established standards and certification schemes which have a good deal in common (New Zealand Biological Products Council (NZBPC), 1988; Austra- lian Quarantine Inspection Service (AQIS), 1992; UKROFS, 1992 ).

The UKROFS Standards for Organic Food Production (UKROFS, 1992), which are typical, define organic production systems as "designed to produce optimum quantities of food of high nutritional quality by using management practices which aim to avoid the use of agrochemical inputs and which minimise damage to the environment and wildlife". They include "grazing systems that are an integral part of the crop rotation and which seek to eliminate animal parasites". Systems of livestock management which involve routine use of prophylac- tic drugs (including parasiticides and vaccines) are not permitted. The livestock plan must provide sufficient land "to prevent the build-up of parasites". How- ever, any necessary veterinary treatment must not be withheld, and conventional veterinary treatments may be used where it is necessary to save the life of the animal, to prevent suffering or where no alternative treatment or prevention is available. Animals so treated are subject to two (UKROFS, 1992 ) or three (AQIS, 1992) times the withholding period specified for the particular treatment, and

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must be identified and quarantined from other stock, with the quarantine area of the farm not to be used for organic production for at least 12 months (AQIS, 1992). The Australian Standard (AQIS, 1992) includes a list of Approved Ma- terials for Animal Pest and Disease Control that consists essentially of natural products, simple and traditional inorganic and organic compounds and homoeo- pathic preparations, but no modern specifically active compounds. This Stan- dard is remarkable for the sweeping statement: "Products derived from recombinant-DNA technology are not compatible with the principles of organic agriculture and therefore are not permitted under this Standard"!

Experiences with organic meat production in Britain have shown that systems for beef or sheep which do not use anthelmintics can be successful and profitable if they are highly diversified, operate at low stocking rates, and premium prices are received for the meat to compensate for lower gross margins compared with higher input systems (Newton, 1989; Young, 1989; Younie, 1989 ). In Australian studies, price premiums for organic produce may be necessary to compensate for lower returns in the first few years of transition from conventional to organic agriculture. With lower farm operating costs for organic farming, enterprise gross margins may not differ greatly (Wynen, 1990, 1992 ).

Organic farming, as distinct from sustainable agriculture, and the demand for strictly organic products are minority activities, and on a global scale are likely to remain that way. In Europe, less than 1% of farmers and less than 0.5% of farm- land is under organic production. In the USA less than 0.5% of farmers are 'organic'. Demand for organic fresh fruit and vegetables and grains could reach 5% of the total UK market, but the market for organic meat is likely to be limited because most 'organic' consumers are vegetarians (Rural Industries Research and Development Corporation (RIRDC), 1990).

4. Implications of sustainable development for parasites and their control in animal production

4.1. Production systems

Organic farming with its prohibition against synthetic inputs is no solution to global food security with a world population expected to reach about 12.5 billion in the 22nd century. However, its other principles are highly relevant to sustainable and efficient agriculture. The development of appropriate practical systems could learn much from successful organic farmets.

Single-enterprise farming with high levels of inputs is least sustainable in the long run. Intensive, single-species grazing systems have the potential to degrade land and water. They also tend to increase the risk of parasitic disease and reduce the options for management-based control, leading to excessive dependence on chemotherapy. In the 1960s and 1970s, multiple dosing with anthelmintics in pure sheep enterprises on permanent pastures in Australia and New Zealand was shown to be highly profitable and was fairly widely adopted (reviewed by Morley

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and Donald, 1980), but the penalty--anthelmintic resistance--was ultimately paid (Waller, 1986).

Zero-grazing systems, e.g. feedlots or housing for ruminants, penned or caged pigs or poultry, may carry low risks of parasitic disease requiring no control measures, and are efficient in energy conversion and use of land. They are threatened most by problems of effluent disposal and by animal welfare concerns. Moves against intensive poultry production, particularly caged layers, and an increase in free-range egg production will increase the importance of some parasites, e.g. as- caridoid nematodes and cestodes, which it has been possible to ignore in intensive systems. This may raise the need for new parasite control agents and integrated control systems, with the possibility of spin-off benefits for small-holder poultry production in developing countries.

Ideal sustainable farming systems on arable land are less-intensive diversified ones, which include crop and animal production in appropriate rotations, to op- timise nutrients and biological activity in the soil, and ground cover and weed control. In areas where land and climate are poorly suited to cropping, ruminant animal production is appropriate in extensive grazing systems at low stocking rates. In these cases there should be greater opportunities for integrated parasite control and less risk of parasite-induced losses, but realisation of the ideal will depend ultimately on the economics of alternative products and production systems. The ordinary operations of the market are unlikely to generate rapid moves to ideal sustainable systems, particularly as they result in lowered farm productivity in the short run. However, this can be influenced by government policies and it is notable that a number of EC countries, in response to severe environmental damage from intensive agriculture, have introduced regulations on the use of pesticides and chemical fertilisers, reductions in stocking rates and the location of intensive livestock industries (Hester et al., 1993 ).

Much research has already been done, particularly in Britain, Australia and New Zealand, on integrated gastrointestinal nematode control systems for cattle and sheep which incorporate grazing management with limited chemotherapy (reviewed by Michel, 1969, 1976; Brunsdon and Adam, 1975; Anderson et al., 1978; Brunsdon, 1980; Morley and Donald, 1980; Thomas, 1982). The British work made particular use of conservation aftermaths or new leys and led to quite detailed grazing plans (Rutter, 1975; Ministry of Agriculture, Fisheries and Food (MAFF), 1980, 1981 ). In contrast, the Australian and New Zealand studies con- centrated on alternate grazing by sheep and cattle or by different age classes of these species on permanently grazed pastures. It is difficult to judge the extent of adoption of integrated control in any of these countries, but the anecdotal evidence suggests, not much (Waller, 1993 ). As has often been pointed out, this is readily explained by the cheapness and flexibility of control based on anthelmintics alone. This is likely to continue so long as effective anthelmintics are available and there are no environmental prohibitions on their regular use. Neither of these conditions can now be assumed and, with growing interest in sustainable systems, the time is ripe to re-examine integrated parasite control in farming systems, including measures other than grazing management. Morley and Donald


(1980) discussed issues surrounding the use of fodder crops, new sowings and aftermath for the production of safe grazing in practical farming conditions. De- spite the fact that 60% of Australia's sheep population is run on mixed livestock- cereal grain farms, almost no attention has been given to integrated parasite control in crop-livestock production systems in Australia. However, the need now is not so much for more research on the principles, but on the further development of commercial production systems which incorporate sustainable parasite control in close consultation with farmers and farm advisers, and aided by simulation models.

4.2. Chemotherapy

Chemotherapy will continue to be an important part of efficient systems well into the future, but there are several issues surrounding its place in sustainable animal production.

Resistance in the target species This is the most important sustainability problem in parasite control. Parasite

resistance increases costs, reduces the efficiency of production, depletes the stock of effective control tools, and increases the risk of environmental contamination as frequency of use and dose or application rates increase with declining effectiveness.

Among the gastrointestinal nematodes of ruminants there is some degree of resistance to all classes of available broad-spectrum anthelmintics, and some narrow-spectrum ones, in nematodes of sheep and goats in many countries. There is a serious lack of anthelmintic effectiveness in some countries, including those with substantial sheep industries such as Australia, New Zealand and South Af- rica (Waller, 1986, 1987; Martin, 1987; Borgsteede, 1990; Rolfe, 1990; Taylor, 1990; Van Wyk, 1990; Scott et al., 1990 ). Resistance appears not to be a significant field problem in the nematodes of cattle and possible reasons for this have been the subject of speculation (Coles, 1988 ). Resistance to levamisole (Lyons et al., 1981 ) and fenbendazole (Geerts and Van Olme, 1989 ) in Ostertagia ostertagi has been suspected but not substantiated after further work (Lyons et al., 1983; Borgsteede et al., 1992).

Among ectoparasites, resistance is most important in the one-host cattle tick, Boophilus microplus, in Australia, South Africa and South America (Wharton and Norris, 1980; Solomon, 1983; Nolan and Schnitzerling, 1986; Nolan et al., 1989). In Australia, resistance has progressed through each successively introduced acaricide group amounting to 22 different compounds, such that there is now resistance to all registered acaricides except ivermectin. Fortunately, except in one case, local populations vary in their complement of resistance mechanisms so that chemical control has not yet completely failed. However, the outlook is not good for existing compounds or for the development of new ones. The sheep blowfly, Lucilia cuprina, in Australia and South Africa comes next with resistance developing to the organochlorines (now banned) and to the organophos- phates, although these, particularly diazinon, continue to be used despite the


shorter period of protection against strike that they now afford. Resistance to the synthetic pyrethroids has occurred in the horn fly, Haematobia irritans, in the USA associated with the use of impregnated ear tags (Sparks et al., 1985 ), and in the sheep body louse, Damalinia (Bovicola) ovis, associated with pour-on application (Johnson et al., 1990 ). Both methods of delivery are operationally con- venient but likely to favour resistance by prolonged exposure of the parasite to sub-lethal concentrations.

In the most serious cases resistance seems clearly to be associated with heavy reliance on chemical control, applied frequently and sometimes haphazardly in timing and intensity or, if less frequently, in control schemes in which it has decisive effects on parasite population size while leaving some survivors. Advocat- ing integrated control in which chemotherapy plays a much less dominant part has had little effect because there has continued to be little incentive to move from the simple to the complex, and because there has been little effort to translate complex principles into practice.

Residues in foods Chemical residues in foods have become a major community concern and a

strong driving force behind reduced chemical inputs in agriculture. These concerns tend to extend uncritically to all drugs or pesticides applied to animals or plants as well as to accidental contaminants. In a United States consumer survey in 1988, residues in meat were seen as more threatening than cholesterol or sat- urated fat (Sundlof, 1989 ). Consumers increasingly demand that the food supply should be free of contaminants of all kinds, whether or not they are known to be harmful. As a result, governments set conservative maximum residue limits (MRLs) which are often unrelated to true hazard, or even to recommendations of the Codex Alimentarius Commission, and there are strong market pressures on farmers to conform.

In the case of anthelmintics, residues are not a major problem. Their mammal- ian toxicity is low and treatment close to slaughter is unlikely. Their half-lives vary and have been taken into account in setting MRLs but violations will occur if withholding periods and recommended dose rates are not adhered to. Particu- lar restrictions apply to the treatment of lactating animals where anthelmintics or their metabolites are likely to be secreted in milk for human consumption. The benzimidazoles and their prodrugs were subjected to close scrutiny because some are known teratogens at doses which are not maternotoxic (Delatour and Parish, 1986 ). Sundlof ( 1989 ) reported no violative residues of the benzimidazole anthelmintics in recent years in the USDA Food Safety and Inspection Service monitoring programme.

There is slightly more of a problem with external parasiticides, but even here the prevalence of residues in foods of animal origin is very low. Organophos- phates are rapidly degraded by mammals and again no residues were detected in liver samples analysed in the USDA FSIS monitoring programme in 1985 and 1986 (Sundlof, 1989). The organochlorines are very persistent and are among the most important contaminants affecting the food supply, but their manufac-


ture and sale is now very restricted and their use on livestock completely banned in industrialised countries. Nevertheless, there continue to be violations from accidental contamination of animal feed supplies when the compounds are used for other purposes and typical incidents are described by Sundlof (1989). As a result of these and unspecified consumer fears, further restrictions and down- wards revisions of MRLs for parasiticides cannot be ruled out. This will place further pressure on chemotherapy for parasite control.

Environmental contamination By comparison with crop protection chemicals, the environmental impact of

anthelmintics has been generally regarded as unimportant. This is because they and their metabolites are confined to the excreta of treated animals and are in a relatively small proportion of the total excreta produced by whole farm animal populations in a region. Such evidence as is available suggests that levamisole and the benzimidazoles pose little cause for concern (reviewed by Waller, 1993 ), but there is more worry about the avermectins. There is evidence for adverse effects on a variety of dung-colonising insects in dung from cattle treated with ivermectin by injection or sustained release bolus (Roncalli, 1989; Wall, 1992; Strong, 1993 ). The effect appears to be much more transient in sheep because the water- based oral formulation used results in rapid absorption and elimination. In contrast, the injectable formulation for cattle is deliberately designed to promote slow absorption and prolonged blood levels of the drug in order to provide more persistent protection against ectoparasites (Wardhaugh et al., 1993 ). Adverse effects on a wide range of non-target species is a consequence of the very wide spectrum of activity of the avermectins, exacerbated by a desire to market a product such as the injectable formulation for cattle as an almost universal parasiticide. The true extent of the problem arising from typical parasite control programs needs further research. This should particularly take into account the effects of the tem- poral and spatial distribution of dung deposits containing avermectin residues at toxic concentrations on populations of dung-colonising fauna. However, if we are able to move to ideal systems of parasite control, i.e. occasional chemotherapy combined with other measures, the problem should not be important.

Ectoparasiticides pose greater hazards of toxicity to non-target species because most tend to be broadly active insecticides. However, they are less hazardous used on animals than when used for crop protection, because their application to animals is much more localised. Nevertheless, there are some areas of particular concern. First, when applied to sheep for the control of ectoparasites, the compounds may be present in the fleece at shearing, particularly if they have been applied not long beforehand. They will be removed almost entirely from the wool at scouring but will be present in one or more fractions of the scour effluent. Lipophilic compounds will be found in the grease and may persist through the lanolin refining process. Strict standards are being introduced for residues in lanolin used in cosmetics. Lipid soluble compounds in residual wool grease and po- lar compounds adsorbed to particulate matter may occur in the dirt fraction be- yond the levels acceptable for land fill disposal, so requiring expensive toxic waste


disposal. Finally, for the aqueous phase, a number of countries are introducing very stringent limits for pesticide levels in aqueous discharges. These are based on ensuring whole of life survival of the most susceptible species in the receiving water ecosystem (Russell, 1993 ). In Australia, the problem is worse than it should be. In 1988, 180 million lousicide treatments were sold for a total sheep population of 160 million whereas only 20-30% of flocks are infested. Most wool grow- ers treat for lice as a form of prevention because they cannot be sure their flocks are free from lice. There is an urgent need for a very sensitive and reliable detec- tion method for lice so as to reserve treatment for infested sheep. Other measures are needed to ensure that insecticides are not present in significant amounts in the fleece at shearing.

A second important problem is contamination of the soil at dip sites and yards with high concentrations of persistent insecticides and acaricides, including those no longer used on sheep and cattle. These can be a source of transferred contamination to wool and meat, and a direct human health hazard if such sites are later used by people for other purposes. In northern N.S.W. more than 1600 cattle tick dips have been built as part of the operations of the Tick Quarantine Area. Ar- senic was used until 1955 and DDT until only 1962, but residues of both are present at high levels at most sites today. There are houses and other recreation and community facilities built on or next to former dip sites and sampling has revealed high residue levels at these sites (DIPMAC, 1992). The resolution of this problem is taxing the N.S.W. Government and is a powerful example of the hazards of persistent chemicals.

Sustainable chemotherapy There is no reason to oppose the use of synthetic chemicals in principle, but

they must be part of integrated control systems which minimise the development of resistance. Their use must not be a threat to biodiversity by significantly affecting the survival of populations of non-target species. Sustainable chemicals of the future must have a narrower, more specific spectrum of activity, be non-persistent and rapidly degraded to harmless metabolites. Convenience in the hands of the user must be reduced in importance.

The disincentives for the pharmaceutical industry to develop new compounds of this kind, and the commercial incentives to promote and use chemotherapy alone, are matters of serious public policy which governments must consider. Also, there is a responsibility on veterinary parasitologists and licensing authorities to shift the emphasis in evaluating chemicals. Chemicals must be evaluated for their effects on animal performance and economic gains within sustainable production systems that incorporate integrated control, and less emphasis must be given to numbers of parasites killed by a single application (Donald, 1985 ).

4.3. Alternatives to chemotherapy

The need to reduce dependence on chemotherapy is now urgent but most ap- proaches still require sustained research effort.


Genetic resistance of hosts Genetic resistance is the ultimate in sustainable parasite control, particularly

for resource-poor farmers. The introduction of known resistant genotypes is the fastest route to success

and is exemplified by the infusion of Bos indicus cattle into the beef industry of northern Australia over the last 50 years. The industry was founded on British breeds of Bos taurus but these suffered severely from the effects of the cattle tick and babesiosis introduced accidentally in 1872. Brahman cattle, which have substantial resistance to the cattle tick and superior heat tolerance, were first introduced for cross-breeding in the 1930s. Now about 30% of cattle in Queensland are high-grade Brahman and most of the remainder have 25-75% Brahman con- tent. This has been by far the most important solution to the cattle tick problem in northern Australia. Ironically, however, there are now pressures within the industry to increase the proportion of Bos taurus blood as the industry attempts to satisfy higher value, more discriminating beef markets. Brahman cattle tend to have lower growth rates under the good nutritional conditions that exist in feedlots (Frisch, 1987), and there are perceptions that their meat is tougher. Simi- larly, in Africa most of the indigenous cattle are of Bos indicus stock with high resistance to ticks, but the pressure of population growth and the need for rapid livestock improvement has led African governments to introduce crossing with European breeds. This has increased production but lowered resistance to ticks and tick-borne diseases and created a total dependency on acaricides (de Castro, 1991).

Another case is that of trypanotolerance in N'Dama and West African Shor- thorn cattle in West and Central Africa. These breeds have a remarkable ability to control trypanosome parasitaemia and resist the development of anaemia. This resistance is highly heritable and genetically correlated with production. Because of their small size they were thought to be unproductive and have not been ex- ploited, but recent work has contradicted this view. In addition to their produc- tive potential and obvious adaptation to tsetse-infested areas, these breeds show resistance to other diseases and environmental constraints, and have considerable potential as dual purpose animals in the tropics (Murray et al., 1991 ).

These instances show that adaptation to harsh environments, including resistance to parasitic disease, in locally evolved livestock breeds is likely to come at the expense of production traits. In other words, the adaptation is at the expense of the high rates of growth, reproduction and milk production, which have come to be expected in more benign environments. Moreover the ability of these local breeds to respond to improvements in one or more of the factors to which they are adapted, e.g. poor nutrition or parasite exposure, is often less than that of breeds which have developed under more favourable conditions. Animal breed- ers have been attempting to find the ideal compromise, with a good deal of success in the Australian tropical beef industry. It is now more important to find this compromise while preserving, as far as possible, the benefits of resistance to parasitic disease so as to reduce the need for other means of control.

In sheep, there is substantial evidence for variation between breeds in resis-

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tance to nematode infections (Barger, 1989 ), but cross-breeding is not a practical objective in fine wool production. However, the magnitude of between-sire differences within breeds is of a similar order (Gray et al., 1987 ), and selection for resistance to gastrointestinal nematodes within breeds is an increasingly active area of research in both sheep and cattle (reviewed by Kloosterman et al., 1992). In Australia and New Zealand, there are six experimental sheep flocks selecting for resistance to trichostrongyles and at least three are producing highly resistant lambs. Widespread adoption of parasite resistance as a breeding objective in the sheep and wool industry depends on further research to provide confirmation that there are no negative correlations between this trait and resistance to other diseases or production traits. Also required are more accurate estimates of genetic correlations with production traits and the development of predictive markers rather than faecal egg counts as the selection tool.

In cattle in northern Australia, a Hereford/Shorthorn line has been selected for the past 30 years for high weight gains in the presence of natural exposure to cattle ticks and other environmental stresses. In this line, now called the 'Belmont Adaptaur', there recently has been a remarkable increase in resistance to cattle ticks with evidence that it is controlled by a dominant major gene or a closely linked group of genes. Preliminary results indicate that the resistance, at levels comparable to that of Brahmans, is fully expressed in crosses, thereby offering an opportunity to gain the benefits of cross-breeding without loss of either desirable Bos taurus characteristics or tick resistance (J.E. Frisch and C.J. O'Neill, unpublished data, 1993).

Advances in molecular genetics now offer opportunities to identify genetic markers for parasite resistance to hasten progress in selection for resistance. Somewhat further off, they will also enable identification of genes with large effects and selective transfer, by transgenesis, to other populations of different genetic background.

Vaccines Conceptually, vaccines meet the requirements for sustainable control because

they will be specific against their target parasites with effects limited to the individual vaccinated host animal. There should also be no food residue problems, although adjuvants will need to be acceptable for use in food animals. Ideally, they will need to be applied only infrequently because their effects are expected to be prolonged. The one exception to environmental innocuity could be the use of live genetically modified viral or bacterial vectors for vaccine delivery. These might have to overcome formidable regulatory barriers to their general release.

Vaccines against parasites have had very limited commercial success so far. Attenuated parasites have yielded some technically, if not always commercially, successful vaccines, e.g. Dictyocaulus viviparus in cattle, Dictyocaulus filaria in sheep, Ancylostoma caninum in dogs, Babesia boris in cattle and Eimeria spp. in chickens (Smith, 1992 ). The major barriers to success have been the difficulty of producing attenuated parasites or antigenic fractions of parasite material in commercial quantities, and the complexity of the immune response to parasites. The

A.D. Donald/Veterinary Parasitology 54 (1994) 27-47 39

first of these barriers has been overcome conceptually by the development of recombinant DNA methods and by peptide synthesis, although effective production does remain technically complex (Emery and Wagland, 1991 ).

The complexity of the immune response continues to delay the development of subunit vaccines through difficulties in the identification of truly protective antigens, a less than complete understanding of the nature of protective responses in each major host-parasite system and insufficient knowledge on the optimum means for antigen presentation and immunopotentiation. Thus, although a number of projects have been in progress for up to 10 years, the launch of a commercial subunit vaccine is still awaited. The most successful and advanced, directed against the cystic stage of Taenia ovis in sheep (Johnson et al., 1989), is in the late stages of commercial development (Smith, 1992).

In the search for subunit vaccines, the covert antigen approach is based on vaccination with parasite antigens that are not normally presented to the host, but whose integrity is important to the life of the parasite. Such antigens are likely to be conserved and show little variation and there would be no natural reinforce- ment of immunity. Considerable success in this approach has been achieved against Boophilus microplus (Willadsen and Kemp, 1988 ) and Haemonchus contortus (Munn et al., 1993 ). In the conventional antigen approach, the antigens identified are recognised by the host during normal infection so that the immunity produced by vaccination will reinforce, and be reinforced by, natural infection (Emery and Wagland, 1991 ). However, conventional antigen vaccination is subject to all the well-known limitations of the evolved host-parasite relationship in which immunity is both slow to develop and labile, with substantial heteroge- neity in responsiveness between individuals.

In humans, and probably also in companion animals, Behnke et al. (1992) argue that acceptable anti-nematode vaccines will need to induce sterilising immunity so that the efficacy of treatment will not be misinterpreted by patients or health care personnel. They cite the commercial failure of the canine hookworm vaccine as a case in point (Miller, 1978 ). It will be no easy task to achieve sterilising immunity and, even though it may be important for the companion animal market, it need not be the objective in farm animal production. As for chemotherapy, vaccine efficacy should be judged on its economic benefits in animal production systems combined with other measures, and not simply by the level of protection generated in experimental vaccination and challenge studies. A vaccine of moderate efficacy, when measured in experimental terms, may be effective in the field by priming the host to progressively develop immune regulation of parasites so reducing the rate of parasite population increase.

As well as technical problems there are also commercial uncertainties and Wil- liams ( 1987 ) expressed considerable pessimism about the prospects for vaccines, especially in the developing world. Given the large research and development costs incurred already, it is difficult to see these vaccines being within the reach of most farmers in developing countries, but their need to use them as a substitute for failed chemotherapy is probably less than that confronting farmers in the developed world, for whom sustained research continues to be well justified.


Biological control Using the term to mean exploiting the properties of one living species to con-

trol populations of another species, biological control is also a highly sustainable approach to parasite control, provided that the control agent is specific and not a threat to non-target species. There have been some notable successes in the biological control of weeds and insect pests of crops. Often the pest species is an accidental or deliberate introduction from another region of the globe and control has been achieved by finding and introducing a natural enemy from the same region. There are no documented cases of this kind in the control of livestock parasites but there has been research on the biological control of the free-living stages of nematode parasites.

The effects of locally present or introduced species of dung beetles on the development and availability of infective larvae of cattle or horse parasites on pastures has been studied in South Africa (Reinecke, 1960 ), the USA (Fincher, 1973, 1975 ), and Australia (Bryan, 1973, 1976; English, 1979; Bryan and Kerr, 1989). Although there are species of beetles native to Australia, other, more efficient, dung-dispersing species from Africa, notably Onthophagus gazella, were introduced. Expected benefits included the reduction of populations of some dipteran flies and parasitic nematodes of livestock. Studies showed that dung beetle activity, sufficient to produce intense beetle damage and complete destruction of faecal deposits, can reduce peaks of infective larval availability on pasture by up to 94%. However, beetle populations are themselves subject to seasonal influences so that these effects have been highly seasonal. There have been no well controlled experiments on the effects of dung beetles either on the seasonal pattern and intensity of nematode infections or on animal production. The direct effects of dung beetles on nematode larval availability over the year, even those of the highly active, introduced species in Australia, do not seem sufficiently decisive to justify such studies.

Nematophagous fungi occur naturally in the faeces of sheep and cattle, but there is potential to exploit them as agents to substantially reduce the translation of nematode eggs to infective larvae on pasture. Detailed systematic studies with cattle were initiated in the 1980s by Gronvold and colleagues in Denmark, and pursued by others including comprehensive work in progress with sheep by Waller and colleagues in Australia (reviewed by Gronvold, 1989; Hashmi and Connan, 1989; Waller and Larsen, 1993 ). There are species of fungi which, when incor- porated into faeces in sufficient quantity, are capable of substantially reducing infective larval availability on pasture, reducing levels of infection in grazing calves or lambs, and increasing liveweights (Hashmi and Connan, 1989; Gronvold et al., 1989). Current work is directed towards a number of areas. One is a search for superior, locally adapted species and strains of fungi capable of withstanding gut passage. Genetic manipulation could make further improvements or produce synthetic 'species'. Methods for delivery, preferably as feed supplements or by intra-ruminal sustained release, and optimum use in parasite control programs need evaluation as do the environmental implications of these agents (Waller and Larsen, 1993).

A.D. DonaM / Veterinary Parasitology 54 (1994) 27-47 41

Biological control is usually for public benefit and typically it has been re- searched, developed and applied by public agencies, although sometimes supported by levies on the industries most likely to benefit from the control. Nema- tophagous fungi for parasitic nematode control are somewhat different as they are unlikely to achieve sufficiently high concentrations in faeces by natural spread, they will be most efficient when administered to animals. Therefore, there could well be commercial interest in their development because their benefits can be captured by the individual farmer. Further research is needed to confirm the promise of nematophagous fungi, but their adoption will also require the development, by farmers, of a truly preventative attitude to parasite control. However, this is a necessary attitudinal change for sustainable production systems in general.

4.4. Systems research

Sustainable animal production systems are more likely than not to be complex ones in which a wide variety of factors need to be optimised. If we are serious about their development, then systems research must receive more attention. An important component in the development of integrated parasite control, and its practical application on farms, is research in the quantitative biology of host- parasite systems and the production of mathematical models and decision-support software (DSS). These are needed to help farmers and their advisers optim- ise control measures for the particular enterprise and the environmental and market conditions currently affecting it.

There has been much excellent work done on the quantitative biology of host- parasite relationships for a number of important internal and external parasites of livestock, including the development of models which have advanced our understanding of the epidemiology of parasitic infections and have enabled simu- lated control options to be explored. For example, in the field of gastrointestinal nematodes of cattle and sheep there have been comprehensive studies of Oster- tagia ostertagi in cattle ( Smith an d Grenfell, 1985; Gren fell et al., 1987 a,b; Smith et al., 1987a,b), Haemonchus contortus (Smith, 1988, 1990) and Trichostrongy- lus colubriformis (Barnes and Dobson, 1990) in sheep, and mixed nematode infections in sheep (Callinan et al., 1982; Paton and Gettinby, 1985; Thomas et al., 1986; Leathwick et al., 1992 ). These models have usually contained a good deal of parasitological detail and their objective functions have mostly been expressed in terms of parasite population size. Some have included simple routines to simulate host mortality (Barnes and Dobson, 1990) or loss of liveweight due to parasitism (Leathwick et al., 1992 ). That of Callinan et al. ( 1982 ) included effects on sheep production through equations relating nematode infection rate to food intake and utilisation of metabolisable energy for growth, linked to subroutines for liveweight change and wool production. However, except for Meek and Mor- ris ( 1981 ) there has been little incorporation of economic measures, or exploration of parasite control options and their costs and benefits in production systems or whole-farm models. At the same time, there has been extensive development,

42 A.D. Donald / Veterinary Parasitology 54 (1994) 27-4 7

for example for the sheep industry, of models and DSS packages such as FLOCK- PLAN in Britain, STOCKPOL in New Zealand, and SHEEPO and MIDAS in Australia (summarised in White, 1992 ), but in general without attention to parasites or their control.

These two strands need to be brought together more effectively, so that the effects of parasites and their control can be assessed economically in models whose objective functions include the volume and value of animal products. In these parasite control could be optimised within bio-economic models of whole farms and their management. This would aid an objective appraisal of the importance of parasites in animal production and would considerably enhance the value of parasite models as research tools as well as decision-support tools for farm advisers and farmers. Above all, this would stimulate a joint exploration by parasitologists, animal production scientists, farm advisers and farmers, of realistic options for change towards sustainable parasite control.

5. Conclusions

Sustainable development in general, and including sustainable control of parasites, involves a degree of altruism which will be hard to achieve. It calls for sacrifices by those of us on the earth now and especially by those who are better off, in favour of the long-term survival of the planet and its physical and biological systems, and an equitable distribution of its resources among future generations of humans. Governments have not so far shown much will to tackle the issues urgently at the international level.

At the domestic level also, governments in many industrialised countries have adopted economic policies in the last 20 years which are based on a declining role for government, tax reductions and the pre-eminence of the market. Govern- ments certainly intervene in those markets, but in ways which are still short term in outlook in response to immediate political pressures, and which reflect modes of economic thinking which are frankly opposed to sustainable development. Current economic systems do not have built-in methods for incorporating concern for sustainability or for valuing ecological systems that contribute to our well-being. Methods of calculating GNP contain no measures of resource depletion or degradation and no account is taken of the services performed by natural ecosystems. Fortunately, things are beginning to change and there is now an In- ternational Society for Ecological Economics concerned about such matters. It is to be hoped that governments and their advisers will begin to adopt such thinking and, in particular, will model and value ecological goods and services and then devise policies to translate those values into appropriate incentives. This will still require taking a much longer view than is typical of elected governments!

Coming down to our immediate concerns, the traditional market place for both farmers and those who supply their inputs has favoured the frequent and widespread use of chemical methods of parasite control. These are clearly becoming unsustainable. Fortunately, both farmers and their suppliers have begun to recog-


nise this and to respond. However, most of the new knowledge required to bring about ecologically sustainable development, including the development of sustainable parasite control, is of a public good character and needs to be fostered and financially supported by governments. In my country, research funding continues to be pushed towards private sources replacing public funds, and not sur- prisingly towards processes and products with identifiable commercial value in the short term. Longer-term research and patient, multi-disciplinary and systems research which are mainly to yield knowledge on how to manage systems sustain- ably and which cannot attract commercial investors, continue to be under-re- sourced. Governments must acknowledge the crucial role of public research and development and the need for widespread dissemination of its results in the quest for sustainable development.

There is a further and related issue at the level of research policy and management. Again in our field, it is notable how much larger is the level of effort in the basic biological sciences and their application to the development of processes and products such as drugs and vaccines, compared with theoretical and applied research in the quantitative biology of host parasite systems and the development of control systems. The problem is not helped by declining public funds for research generally, but we cannot provide sustainable parasite control without a better balance between these two ends of the spectrum.

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Parasites, animal production and sustainable development