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R.D. Hodges and A.M. Scofield
Department of Biochemistry, Physiology & Soil Science, Wye College {University of London), Ashford, Kent, TN255AH, England
The term 'iatrogenic disease' has been used recently to refer to those defects or diseases occurring in plants or animals which can be directly ascribed to aspects of the husbandry system producing the plants, etc. They are the undesirable side effects of production systems. However, this term is misleading and should probably not be used in an agricultural context. If such terms are necessary, we prefer the more classically correct term of 'agricologenic', or farmer-induced disease.
This review takes the widest view of the ways in which husbandry systems can detrimentally affect the organisms produced. For example, disease may be induced by the effects of applied agrochemicals on the host plant or on the ecosystem in which host and pathogen co-exist, or may arise from impoverishment of the soil microflora caused by reduction of soil organic matter.
The general theme of the review is that the greater the interference with the agricultural ecosystem by increasing inputs of foreign materials and intensive husbandry methods, the greater the tendency to generate agricologenic disease.
All systems of agriculture are highly artificial, simplified ecosystems when compared with the natural ecosystems in which crop plants and animals originally evolved. Although many varieties of crops and animals have been bred to respond efficiently to agricultural conditions, nevertheless, there are many ways in which plants and animals can be influenced by stress or imbalance induced by aspects of the system, such that they develop diseases or become more susceptible to pests. In human medicine the principle has long been recognized that doctors may unintentionally induce disease by their treatments, and this process has been called 'iatrogenic disease'. Recently, the term iatrogenic has been used to refer to disease arising in plants as a result of certain crop production practices (Horsfall, 1 972 ; Griffiths & Berrie 1 978, Griffiths, 1 981). These authors used the term in a comparatively narrow, chemically oriented sense, just as the modern medical interpretation of iatrogenic disease usually applies to those problems arising as side effects of pharmacological agents, they have restricted the use of the term to diseases of plants induced or exacerbated by the use of agrochemicals (Griffiths, 1981).
Because of its medical origin and the restricted way in which it has been used in crop production, it is considered that the term iatrogenic disease is misleading and should not be used in an agricultural context. In a recent paper, Hodges & Scofield (1983) suggested the term 'agricologenic' as a suitable term to describe farmer-induced diseases.1 This term is intended to have the widest possible interpretation in that it will be used to cover any deleterious effects of the husbandry system which directly or indirectly give rise to imbalances, defects, diseases or susceptibility to pests in the organisms produced. Agricologenic disease was therefore defined as: 'Any disease or pest infestation which results directly from aspects of the husbandry system used to produce the affected organisms, together with any underlying defect, imbalance or susceptibility which may not be immediately manifested but which is also a direct effect of the production system' (Hodges & Scofield, 1982).2
This review will take the widest view of the ways in which husbandry systems can detrimentally affect the plants or animals produced, in that it will consider not only the processes by which specific diseases may be induced in individual organisms but also the ways in which modifications of the ecosystem may increase the probability of more generalized disease as well as inducing a state of 'dis-ease' or imbalance in parts of the agricultural system. The general theme of the review will be the tendency for modern, intensive agriculture, largely because of its involvement with agrochemicals, to generate agricologenic disease, and the likelihood that a more biological approach to husbandry systems will reduce the incidence of such problems. It is not the aim of the review to make a critical assessment of the relevant work but rather, by selecting from a substantial literature, to provide a descriptive account of the range of problems that have been encountered in practice.
The evolution of our present system of agriculture has taken place over a period of several millennia. During this time wild species have been domesticated and adapted to human needs and cultivated plants and domesticated animals have undergone a process of rapid evolution, such that even a flew centuries ago they were very different from their wild progenitors. More recently, this process has been speeded up through intensive plant and animal breeding to make them even more productive and adapted--and consequently even more removed from their ancestral origins. This process of genetic change has been a major factor in the development of our present highly-productive system of agriculture, but it has also resulted in species which can only survive within a protected agricultural environment. Thus as wild species have been brought into cultivation or domestication so, for a variety of reasons, the pressures of pests and diseases have tended to Increase and, in the case of plants, a new problem, that of weeds, has been added.
Throughout the greater part of agricultural history food production relied upon biological processes for pest and disease control and biological and geochemical processes (e.g. fallowing) for the renewal of soil fertility. Because there was no scientific basis to agriculture at this time, these processes were poorly understood, and consequently the history of mankind records many instances of crop failure and subsequent famine. Primitive agriculturalists had plenty of problems. Nevertheless, there are a number of recorded instances of 'primitive' agricultural systems based entirely upon biological processes which were apparently very productive, efficient and sustainable (for example: China-- King, 1926; Africa--Clayton, 1964 and Gleave & White, 1967; South America -- Hyams, 1952). Until about 130 years ago there was no alternative to the 'biological approach' in the development and improvement of agriculture but about the middle of the last century, the work of Boussingault in France, Liebig in Germany and Lawes and Gilbert in England initiated the development of what we now call agricultural science. Because chemistry was the most advanced of the sciences at that time, and because chemical investigations provided a relatively straightforward model to explain the basis of plant nutrition, the development of agricultural science tended to become overshadowed by the 'chemical approach', resulting in the growth of the modern fertilizer industry and, more recently, the pesticide industry. Thus modern forms of crop production, crop protection and veterinary medicine have involved an increasing use of chemical inputs--insecticides, herbicides, fungicides, fertilizers, drugs; and at the same me much higher nutritional planes have been introduced for both plants and animals. More recently still, the intensive application of economic theory to agriculture has resulted in what has been termed 'agribusiness', the development of production systems organised more on an industrial than on a husbandry basis.
Although all these factors combined have resulted in a greatly increased production, the effect of the application of these new technologies over a comparatively short time span has been to put pressures on the plants and animals involved, often resulting in deleterious consequences which are the unexpected and unwanted side-effects of the technologies. Such deleterious side-effects are what are called here agricologenic disease. It is only in recent decades that increasing knowledge of biological science and of how its principles should be applied to the very complex situation that is usually found in a soil/crop ecosystem have made us aware that a straightforward chemical approach does not take note of the intricacies of what is a complex biological system. Thus, although our crops and farm animals are superficially greatly different from their wild ancestors, their fundamental biochemical and physiological mechanisms and their interrelationships with other organisms (such as the soil bacteria) are probably basically little changed from those of their ancestors. It is possible that a return to a more biological approach to food production with a greater awareness of the complex organisms we are concerned with may result in a more balanced and sustainable system in which there is less stress and thus less potential for agricologenic disease. Historically speaking, the modern intensive system of food production is only a very recent phenomenon in the overall development of agriculture, is unlikely to be sustainable in the long-run, and thus may turn out to be only a temporary phenomenon on the timescale of the history of mankind (Lovett, 1980; Ulbricht, 1981).
The effect of cultivation and tillage practices upon the development and incidence of disease in crops is very variable making it difficult to draw any generalized conclusions (Shipton, 1977; Sumner et al., 1981). One of the main reasons for using crop rotations as opposed to monoculture is to prevent the build-up of plant pathogens which would otherwise significantly reduce production. However, experience has shown that although a monoculture of crops may or may not be as productive as when they are included in a rotation, the occurrence and development of diseases under monoculture is very variable and depends very much on the individual crop and soil (Shipton, 1977). For example, there may be a maximum development of the disease producing a severe impact on the crop over the period of a few years (brown root rot of tomatoes Pyrenochaeta Iycopersici; club root of brassicas, Plasmodiophora brassicae. Alternatively, there may be only a limited development of disease (Fusarium oxysporum in potatoes), an almost total lack of disease, or a decline in disease after an initial high level (Gaeumannomyces graminis in wheat). Many of these responses, such as the decline in an initial infection and the almost total suppression of disease (soil suppressiveness) are almost certainly due to poorly understood microbiological mechanisms (Papavizas & Lumsden, 1980).
Shipton (1979) describes a number of examples of crops where monoculture has resulted in considerable increase in disease incidence. For example, he mentions the increase in intensification of soybean culture in the U.S. Mid-West which has been followed by an increase in brown stem rot caused by Cephalosporium gregatum and Phytophthora sp.; and also the papaya decline in Hawaii, a replant problem caused by Pythium aphanidermatum and Phytophthora parasitica.
Lewis (1980) considers that monoculture allied to unwise use of insecticides has created many pest problems, and as an example he quoted the sequence of pest problems arising from the intensive culture of cocoa in Sabah, Malaysia in the 1950's and 1960's when the use of insecticides as the sole means of pest control resulted in the development of a sequence of pests, each of which was more difficult to control. Eventually the situation was stabilized by a system of integrated control. A more widespread example of this interaction between monoculture and pesticides is quoted by Lovett (1982) from Holm et al. (1977). The use of hormone-type weedkillers to control populations of broad-leaved weeds, often of secondary importance, has led to the replacement of these weeds by different populations, frequently of narrow-leaved perennial plants which are much more difficult to manage.
The subject of crop rotations and plant productivity has been reviewed in detail by Sumner (1982) and, in particular, he considers the impact of rotations on plant pests and diseases. Sumner quotes a very extensive range of examples from the literature which suggest that:
1. In general, rotations can control many soil-borne pathogens, although this does not usually apply to those pathogens which can survive saprophytically in the soil.
2. Foliage pathogens are frequently spread by air-borne spores and are thus not primarily controlled by the cropping sequence. However, the initial primary inoculum in crop residues or in the soil may greatly influence the progress of a disease. On the other hand monocropping has led to an increased severity of foliage diseases in many parts of the world.
3. In the case of bacterial plant pathogens, primary infections normally come from sources other than the soil, and thus with certain exceptions crop rotations have only a limited control over many plant bacterial diseases.
4. Crop rotations are effective in controlling many insect pests, particularly those that are restricted feeders. However, because insects are mobile, rotations will not necessarily manage all insect pests in field crops.
In the case of soil-borne pathogens, Sumner (1982) states that: 'Crop rotation is known to produce a soil mycoflora richer and more variable than monoculture, and that may be beneficial in inducing biological control of certain pathogens, either by reducing the population (inoculum density) of the pathogens, or by reducing the capability of the pathogens to cause disease (inoculum potential)'.
The impact of minimum tillage/zero tillage/conservation tillage systems on plant disease appears to be highly variable, depending on the crop and the pathogen (Sumner et al., 1981). Unger & McCalla (1980) consider that many insect problems are not affected by the tillage system but others may be increased in zero tillage as compared with conventional tillage. A similar situation occurs with plant diseases, with some exceptions being increased with zero-tillage. The effects of direct drilling techniques on the disease patterns in cereals have been reviewed by Shipton (1979) and Yarham (1979). Overall these techniques have been found to have relatively little impact, either positive or negative, on the incidence of disease. However, recent experience in Britain has shown that regular use of direct drilling techniques frequently results in serious problems with weeds such as sterile brome grass (Bromus sterilis) and blackgrass (Alopcurus myosuroides).
Disease may increase in double-cropping when compared to monocropping. Thus vegetable damage increased and yields were reduced when two crops per year were compared with one crop of vegetables alternating with a green manure crop (Janes et al., 1955). Intercropping of two or more crops in the same area frequently reduces the development and spread of some plant pathogens, but this effect does not occur in all cases (Summer et al., 1981).
Many plant breeding programmes are primarily intended to enhance productivity, but the genetic uniformity plus the widespread development of monoculture that often follow the production of successful crop varieties may result in a greatly increased likelihood of disease. A number of important instances where such situations resulted in severe problems have been summarised by Council on Environmental Quality (1980). For example, the severe corn blight epidemic in the U.S.A. in 1970 resulted from the widespread use of hybrid corn varieties carrying a cytoplasmic factor for male sterility. This factor conferred the advantage of ease of production of hybrid varieties and, by 1970, most inbred; U.S. corn varieties contained the factor. However, it also transferred an extreme susceptibility to Helminthosporium maydis the pathogen causing southern corn leaf blight, and this resulted in the 1970 disease epidemic (Ullstrup, 1979 ;Cowling, 1978; Shipton, 1979). This problem is potentially very widespread because, as the U.S. National Academy of Sciences has stated: 'Most major crops are impressively (genetically) uniform and impressively vulnerable' (N.A.S.,1979).
Other examples of new crop varieties that have proved susceptible to attack by existing insects or pathogens which had previously not been important can be found in the high-yielding varieties of 'Green Revolution' wheat and rice. The earlier varieties, in particular, possessed relatively simple genetic structures which made them susceptible to attack, and their genetic uniformity together with their introduction over wide areas resulted in severe pest and disease problems, making it necessary to replace them quickly with more resistant varieties (Day,
1977). Examples of this problem relating to high-yielding varieties of a number of crops in India are described by Safeeulla (1977). Chang (1979) states that: 'Concerted efforts are needed to deal with the rising incidence of diseases and pests in predominantly high-yielding areas, especially the rice bowls of Asia' Chang also states that the lush growth made by these new varieties when fertilised and irrigated, the increased genetic uniformity, the intensified continuous planting of the same crop in an area, and continuous staggered plantings throughout the year, have resulted in devasting epidemics of diseases, insect pests' or both'. Marshes (1977) has detailed the hazards of genetic homogeneity of major crops as follows :
1. The widespread use of one or a few similar genetically homogeneous cultivars provide ideal conditions for the spread of newly introduced exotic parasites, or virulent strains of existing parasites, to which the crop is susceptible.
2. As monotypic monocultures are particularly prone to disease and pest epidemics, their culture often requires the consistent and heavy use of fungicides and pesticides, which carries with it the dangers of environmental pollution and the development of resistant strains of fungi and insects.
3. In general, plant breeders use the best currently available varieties extensively as parents in their improvement programmer. If the best varieties represent a narrow genetic base .... then the capacity for future gains by plant breeding is severely reduced.
4 The replacement of the ancient land races of modern varieties has led, and continues to lead, to the loss of much of the immense wealth of variation contained within and between these 'genetic treasuries'.
A very recent example of the hazards of genetic homogeneity in crops is that of oil seed rape production in Britain (D.R. Scarisbrick 1983 -- personal communication). Oil seed rape (Brassica napus) production has risen from about 10,000 hectares in 1970 to about 220,000 hectares in 1983, thus becoming the third largest arable crop in Britain. However, this increase was largely based upon the use of two highly-productive cultivars which are susceptible to several diseases. Whereas the cultivation of this crop was originally relatively free of disease problems, oil seed rape is now becoming significantly affected by the spread of light leaf spot (Pyrenopeziza brassicae), Alternaria (Alternaria brassicae) and Sclerotinia sclerotiorum.
Another practice in the propagation and development of new varieties which predisposes to disease is the use of size controlling rootstocks in apple orchards Cowling. 1978). The propagation of apple varieties on these special rootstocks offers many advantages in the management of orchards. However, many of the most widely used size-controlling rootstocks are highly susceptible to collar rot caused by Phytophthora cactorum and their use, in combination with other horticultural practices, has led to epidemics of collar rot in apple trees.
Plants require the presence of at least thirteen nutrient elements for normal balanced growth and optimal productivity, and these are usually divided into the major, minor and trace elements depending upon the amounts of each required by a crop. Significant deficiencies of any of these nutrients may cause reduced productivity and/or increased susceptibility to pests and diseases, and Schutte (1964) gives many examples of the effects of trace element deficiencies in soils. However, the results of such deficiencies should not be considered as agricologenic disease since no farmer willingly accepts the presence of an inherent soil deficiency if he has the means to correct it.
On the other hand, there are various ways in which unsuitable fertilizer practice can give rise to agricologenic disease. Two of the most important are, firstly, interactions between elements in the soil, at the soil-root interface or within the plant itself, may give rise to nutrient imbalances by modifying the availability or utilisation of essential elements; secondly, the presence of high levels of fertilizer ions in the soil may result in damage to plants, particularly to the roots.
a ) Nutrient imbalances
The interactions between nutrient elements in the soil are very complex and a significant increase in any one frequently alters the availability of others, either positively or negatively (Murder, 1953; Nielsen& Cunningham, 1962 ;Schutte, 1964; Voisin, 1965 ;McSheehy, 1971; Davidescu, 1974 :Bussler, 1974 ;Hodges, 1981). Thus the application of one or more of the major nutrients (nitrogen, phosphorus and potash) in quantities large enough to obtain maximum growth and productivity can result either in nutrient imbalances in the crop, or in excessive uptake of the major nutrients. Either of these situations may make the crop more susceptible to pests or diseases.
Kemp (1971) has demonstrated that application of nitrogen and potash to pasture to obtain maximum yield, results in an excess of potash and deficiencies of sodium, calcium and magnesium in the grass. Takahashi et al. (1977) have shown how, in Japan, the intensive use of fertilizers to increase grass production has resulted in widespread mineral deficiencies in the pastures. These imbalances may then be reflected in diseases in the plants or in stock feeding on the plants. Thus Davidescu (1974) states that excess nitrate fertilizer may result in an accumulation of nitrate ions in the plant. In non-optimal climatic conditions, this accumulation may be enhanced leading to direct toxic effects on animals feeding on the plants, or to an imbalance of other minerals which likewise affects the animals. Similarly, intensive application of potash fertilizer to grass may result in excess uptake of potassium and an increase in sterility and grass tetany in the stock (Davidescu, 1974).
Application of nitrogen fertilizer may increase or decrease the susceptibility of crops to disease, often depending upon the form of the fertilizer given (Huber & Watson, 1974; Henis, 1976; Kiraly, 1976; Shipton, 1979). Huber & Watson (1974) have described twenty root or cortical rots, six vascular diseases, seven foliar diseases, three nematode, gall or other diseases and three virus diseases in which applications of ammonia or nitrate nitrogen increased disease susceptibility.
Modified susceptibility to pests and diseases in plants as a result of fertilizer applications is widely reported in the literature, thus:
The susceptibility of cereals to leaf pathogens is usually increased by nitrogen fertilizer (Davidescu, 1974; Jenkyn, 1976).
Whitney (1976) states that nitrogenous fertilizers increase susceptibility to such diseases as rusts, powdery mildews and blasts but have little effect on madly other diseases. Potash and phosphate tend to Increase crop resistance to infection but there are exceptions to this particularly with virus infections.
Heavy application of fertilizer, especially nitrogen, may greatly increase the number and variety of` pests attacking cotton and rice crops (Brader, 1976). These crops are normally subjected to intense fertilization in order to obtain maximum productivity.3
Jones (1976) concludes that in most pest-crop situations nitrogen fertilizers Increase the number of pests.
The influence of fertilizers Oil the susceptibility of plants to pests and diseases has been recently reviewed by Coleman & Ridgway (1983)
The detrimental effects of high levels of soluble nutrient ions can also result from large applications of` fresh manures or slurries to talc land (Mashers et al..
b) Fertilizer damage
Addition of fertilizers to soils increases the concentration of salts in the soil water. Above certain levels of concentration many ions such as nitrate, chloride and ammonium, can have injurious effects on plants, particularly seedlings. Such effects may be reductions in germination of seeds and emergence of seedlings scorching and retardation of growth in young plants, and damage to roots at any stage of development (Phillips, 1972; Imai, 1977; Cleaver, 1 979).
Increasing fertilizer application may increase the susceptibility of a crop to mechanical damage. Thus with potatoes Paterson & Gray (1972) showed that the levels of injury to tubers during harvesting and grading rose with increase in the rate of fertilizer applied, particularly with the nitrogen component.
Organic matter is an essential component of soils because its presence. at least in natural, uncultivated soils, is largely responsible for their fertility. The presence in a soil of the right amount and type of organic matter gives rise to a wide spectrum of physical. chemical and biological properties which results in a well structured, fertile soil (Kononova, 1975; Koepf et a/., 1976; Hodges, 1977). In conventional agriculture, soil fertility is largely provided by means of applied mineral fertilizers and the return of organic matter is a secondary concern, if at all. Because of this, there is a tendency for the reduction of soil organic matter levels under conventional systems. particularly intensive systems (Cooke, 1974). and this may result in loss of soil structure, water-holding capacity, etc. (Agricultural Advisory Council' 1970; Boels et. al.. 1982) which may be followed by a reduction in productivity. On the other hand. the system of biological (organic) agriculture relies very largely on the return of manures and other organic residues to the soil to produce necessary nutrients for the crops, but this process also maintains other properties, such as structure, aeration and moisture-holding capacity, which together with balanced nutrient levels go towards the production of a truly fertile soil.
The recent development of minimum-tillage and no-tillage cropping systems can be an improvement to conventional tillage techniques in terms of the retention of soil organic matter, the reduction of soil erosion, etc. In many cases sod erosion on susceptible soils may be virtually eliminated with no-tillage techniques and at the same time, organic matter breakdown rates may be reduced due to minimal disturbance of the soil (Phillips et al., 1980).
Apart from this general point concerning the relationships between organic matter and what may be termed the 'hearth' of the soil, there is specific evidence which demonstrates that organic soil amendments can help to control soil-borne diseases (Patrick & Goussoun, 1965; Baker & Cook, 1974; Cook, 1977 and 1981). Cook (1977) states that: 'Few soil-borne diseases cannot be controlled by organic amendments of one kind or another' and describes the example of Avocado orchards in Australia. Orchards maintained with high levels of organic matter in the sol. show no signs of root rot due to Phytophthora cinnamon), whilst orchards with low levels of organic matter show severe root rot. Baker and Cook (1974) state: '.... manures stimulate high populations of soil microorganisms' and in doing so limit the germination of pathogenic spores or the growth of hyphae, or hasten the microbial digestion of propagules and pathogen infested remains. The digestion of sclerotic Phymatotrichum omnivorum by soil organisms after treatment of the soil with chicken and barnyard manures illustrates this'. Examples froth the early literature of disease control by organic amendments are: Sanford (1926) and Millard & Taylor (1927) with Actinomyces scabies; King en al. (1931) with cotton root fungus' and Fellows & Ficke (1934) with take-all of wheat.
Thus it can be considered that systems of agriculture which do not give priority to the maintenance of soil organic matter levels may predispose crops to a higher incidence of soil-borne diseases whilst systems which seek to maintain or enhance soil organic matter levels may help develop circumstances in which there is a naturally high level of biological control of these diseases. This may be one factor which would help to explain the claims frequently made by biological farmers that their crops tend to suffer less from pests and diseases than do those produced by conventional farmers (Howard, 1940; Balfour' 1975; Friend, 1983).
Plants subjected to water stress are likely to be more susceptible to disease, but with crops which rely on natural rainfall for their water requirements the availability of water is outside the control of the grower. However, with irrigated crops water availability is controlled and careless irrigation practices can give rise to conditions highly favourable for disease (Cowling, 1978). Cook & Papendick 1972) list eleven diseases which are particularly favoured by dry soils and eight diseases which are favoured by wet soils.
Excessive irrigation can provide long periods of time during which the humidity in the soil and around the plant is high, producing optimum conditions for the germination and spread of many fungus diseases. Thus well-irrigated tomato plants showed an increased incidence of anthracnose and Rhizoctonia fruit rots but less blossom-end rot (Crossan & Lloyd, 1956). Furrow or flood -irrigation may create conditions that favour the growth of pathogens needing high soil moisture' for example Pythium, and overhead, sprinkling irrigation can increase the hazard of splash dispersal of pathogens (e.g. bacterial blight and anthracnose of bean).
For many years, steadily increasing mechanization has been a regular feature of ,agricultural practice, and mechanization may give rise to increases in disease which are directly attributable to the changing practice. Cowling (1978) has described examples of this effect using the specific case of mechanical harvesting. Mechanical harvesting devices tend to wound plant tissue and this may cause problems with perennial fruit trees and bushes. Barnes (1964) mentions several instances of fruit tree diseases which have been enhanced by using mechanical shakers to harvest the fruit, and Cowling (1978) quotes how Monilia fructicola fruit rot in cherries developed to epidemic proportions as a result of the introduction of mechanical harvesting aids.
Malcolmson & (gray (1968) have related how the incidence of potato tuber rot, caused by potato gangrene (Phoma exigua) was increased by the more severe damage inflicted on some tubers by the introduction of elevator digger harvesters.
The application of pesticides to crops to protect them from pests, diseases and weed competition may result in deleterious secondary effects which were unexpected and unintended. Such effects are often an increased susceptibility to other pests and diseases. Herbicides and growth regulators, in particular, appear to be associated with this phenomenon.
This subject has been reviewed by N.A.S. (1968), Altman & Campbell (1977), Cowling (1978), Griifiths & Berrie (1978), Horsfall (1979) and Griffiths (1981). Altman & Campbell (1977) described more than 20 herbicides known to increase disease caused by six soil-borne pathogens, and at least 30 with the opposite effect on some ten pathogens. Horsfall (1979) listed 45 chemically induced iatrogenic diseases, 32 being caused by herbicides and growth substances, 11 by fungicides, 2 by nematicides and 1 by an insecticide.
Papavizas & Lewis (1979) have reviewed the secondary effects of a wide range of pesticides on soil-borne plant pathogens, giving numerous examples of both positive (disease-reducing) and negative (disease-enhancing) side-effects of these chemicals. Griffiths (1981) has classified the mechanisms associated with iatrogenic disease resulting from crop protection chemicals into three categories. These are:
(a)Effects on the host plant. This can be further subdivided into:
(i) Changes in host composition and structure. Thus 2, 4-D and maleic hydrazide alter the sugar content of host tissues and induce changes in disease proneness. Simazine increases the nitrogen content of plants and this may result in increased severity of certain diseases of several crops. Chlormequat chloride, a dwarfing agent used mainly on wheat, reduces eyespot disease due to its dwarfing effects but increases other diseases at the same time.
(ii) Leakage of metabolites from the plant surface. Residues of herbicides in the soil may affect crop plants, particularly young plants, resulting in increased leakage of metabolites to the plant surface. The metabolites increase the growth of pathogens around the plants and thus exacerbate plant disease.
(iii) Changes in defense mechanisms. There is some evidence that plant growth regulators and herbicides may modify natural defense mechanisms and thus increase disease attacks.
(b) Effects on pathogens. An increase in disease resulting from the direct action of chemicals enhancing growth or reproduction of pathogens is not a common phenomenon but there are well-attested cases.
(c) Effects on the ecosystem. Selective inhibition by agrochemicals of competitive or antagonistic organisms in the general crop ecosystem may allow an increase In the abundance of pathogens and thus an increase in the incidence of disease. This effect occurs particularly with soil-borne pathogens and there are many examples of soil treatments intended to control root diseases which have produced the opposite effect. This type of agricologenic effect is usually very complex, it is difficult to unravel and may remain unrecognised for long periods.
Specific examples from the literature of plant protection chemicals causing agricologenic diseases are:
(i) 2,4-D. The herbicide 2,4-D when applied to soil immediately prior to planting wheat, increased the damage caused by wireworms to the wheat (Fox, 1948). When used on corn (Zea mays), 2,4-D has been shown to increase the susceptibility of the crop to the European corn borer (Ostrinia nubilalis), the corn leaf aphid and the southern corn leaf blight (Helminthosporium maidis) (Oka & Pimentel, 1976).
(ii) Simazine. Attacks of the American Gooseberry mildew (Sphaerotheca mors-uvae) on blackcurrant bushes increased in incidence and severity with increasing rate of application of the herbicide Simazine (Upstone & Davies, 1967).
(iii) Romig & Sasser (1972) concluded that the herbicides trifluralin and dinoseb reduced the structural and biochemical defences of snapbeans, resulting in an increased severity of attack by Rhizoctonia solani. Levels of phytoalexin and phaseollin in the plants were reduced in direct relationship to the herbicide concentrations applied.
(iv) Similarly, trifluralin greatly increased disease in cotton in Israel caused by Rhizoctonia solani by increasing both the susceptibility of the host plants and the activity of the fungus in the soil (Neubauer&Avizohar-Hershenson, 1973).
(v) Recent experience (Watson, 1981) has shown that certain hormone herbicides used to kill broad-leaved weeds (e.g. mecoprop) are highly volatile compounds and that the vapours retain a high herbicidal potency. In suitable meteorological conditions herbicide vapours can arise from sprayed crops and, sometimes many hours after the original application, can damage nearby susceptible (broad-leaved) crops as well as wild plants in the local environment.
(vi) The regular use of herbicides to control weeds in cotton fields in Georgia, U.S.A. has resulted in a change in the weed flora, the original primary weeds giving way largely to species of nut sedges (Cyperus). Since nut sedges are good hosts of a nematode pest of cotton, Meloidogyne incognita, an increase in root-knot disease ensued (Bird & Hogger, 1973). Similar regular use of herbicides to control weeds in British apple orchards has resulted in the emergence of Phytophthora syringae as a major cause of storage rot (Harris, 1981). This organism, virtually unknown as a storage pathogen since the late 1930's re-appeared in 1973 as a result of changing management practices in the 1960's and is now considered one of the most important pathological hazards to top fruit storage.
Bollen (1979) has reviewed two types of interactions between fungicides and soil-borne pathogenic fungi which can be considered as resulting in agricologenic disease. Firstly, there is 'dominance change of pathogens' in which control of a fungicide-sensitive pathogen is followed by the increase of a fungicide-tolerant pathogen that was initially of only minor importance, and he gives a number of examples of this effect. Secondly, there is the 'boomerang effect' in which the disappearance of a pathogen after fungicidal treatment is followed by its reappearance in even greater quantities.
The intensification of crop production by conventional agriculture has been accompanied by a considerable increase in the use of pesticides and this has given rise to effects which can be included under the heading of agricologenic disease. The broad-spectrum effects of most pesticides can have a far-reaching ecological impact. particularly when they are used in large amounts, and this is best exemplified by the case of insecticides. The various problems arising from the intensive use of insecticides have been discussed in Onerous publications, including van den Bosch (1971, 1972, 1980); Conway (1973, 1982); Smith & Reynolds (1973); Gillham (1973); Barducci (1973); Newsom (1973);Watson & Brown (1977); Sawicki (1979) and Bull (1982). The more important problems are:
a. The development of resistance. Severe selection pressure on populations of insect pests caused by intensive pesticide use frequently results in the development of strains resistant to the chemicals used. Bull (1982) and Patton et al. (1982) have illustrated the increase in pesticide-resistant arthropods over the past 45 years: in the 1930 s there were about 7 resistant species, and by 1954 this number had increased to 25. Thereafter, with increasing insecticide use, the numbers increased rapidly. reaching 224 in 1967 and 432 resistant species in 1980. As resistance develops to a number of insecticides, so important crop pests become more difficult to control. For example, Lovett (1982) notes that species of Heliothis, major pests of several crops in many parts of the world which in Australia have developed resistance to a range of pesticides, are now reported to be becoming resistant to the synthetic pyrethroids, comparatively new pest control agents.
b .Resurgence of pests. Regular application of large amounts of insecticides to control insect pests has resulted in many cases of resurgence of these pests to high levels, following initially successful control. This may be due partly to development of resistance in the pests, but is frequently also caused by the ecological Imbalance resulting from the destruction of the pests' natural predators and parasites thus releasing them from any natural biological control
c. Development of secondary pests. Because of the ecological imbalance which may arise from excessive pesticide usage, insects which previously had little or no impact on a crop can develop into secondary pests, some of which eventually become major pests in their own right. Ku et al. (1980) have described the situation that has arisen in the rice crop in Taiwan:
'.... some species which were of minor importance in the past have become dominant pests in paddy fields in recent years. This situated on is believed to have resulted from the considerable changes which occurred in farming patterns and techniques and from the extensive use of synthetic pesticides, the latter being one of the main factors influencing outbreaks of many crop insects and mites. For instance the green rice leafhopper and the brown planthopper have increased following the widespread application of synthetic insecticides for the control of rice stem borers. This may be attributed to the fact that synthetic insecticides, though very effective against rice stem borers may adversely affect natural enemies, particularly spiders, which prey upon the ricehoppers, and that these same insecticides show relatively little effectiveness against the ricehoppers themselves. Some synthetic insecticides may have encouraged the development of minor pests to a position of agricultural Importance following prolonged and frequent usage'.
Examples of cases where one or more of these problems have had a serious impact on important crops have been described by Barducci (1973)--cotton in Peru; Conway (1973)--cocoa and oil palm in Malaysia; Lewis (1980)--cocoa in Malaysia; and Bull (1982)--cotton in Central America and Africa, and rice in Asia. Thurston & Glass (1979), when considering the production of cotton in rice Africa and America with the intensive use of insecticides, describe how in some instances, pest problems became so bad that 'yields diminished and in some areas production had to be abandoned'. Such a situation, where cotton production is no longer possible as a direct result of the previous production practices, and taking the disease analogy to its limit, could be termed 'a fatal case' of agricologenic disease.
Although resistance to insecticides has produced the most obvious problems, the development of resistance to other plant protection chemicals is beginning to be a cause for concern. Conventional fungicides have not given rise to many problems of resistance (Dekker, 1977), but the more recent development of systemic fungicides has resulted in the rapid appearance and increase of resistance in many pathogens (Wellman, 1977; Wade, 1982). Sbragia (1975) has commented: 'Since the introduction of the systemics, resistant strains of fungi have begun to develop at an alarming rate'. Patton & Conway (1982) have noted that between 1974 and 1978 the number of fungal and bacterial pathogens resistant to one or more chemicals doubled, rising from 35 to 70. An example of this phenomenon is given by Georgopoulos & Dooms (1973). They described how benomyl had been used in northern Greece for several seasons to protect sugar beet against leaf spot disease caused by Cercospora beticola. However, a very rapid development of resistance by the pathogen resulted in serious outbreaks of the disease in 1972.
Resistance of weed species to herbicides is also beginning to become a problem although, so far, resistant weed species are considerably fewer than resistant arthropod species. FAO (1977) reported that by 1976 resistance had developed in 19 weed species to a total of 7 compounds out of an overall total of more than 200 in use. In 1981, All & Souza Machado reported that 13 weed species were showing resistance to triazine herbicides in more than 25 locations in North America. Thus, although this problem is relatively restricted in scope, it is increasing and Craig (1982) believes that such figures may represent a considerable underestimate of the actual occurrence of resistance to herbicides.
A further problem that can arise from the use of plant protection chemicals is the possible interaction between a crop and two or more applied chemicals, resulting in unintentional damage to the plants. An example of this is given by Matsunaka (1983). The herbicide propanil can be used to control weeds in rice crops because the presence of the enzyme aryl acylamidase I in rice allows the plants to degrade the herbicide before it damages them. However, if insecticides of the organophosphate, carbaryl or carbamate types are used on the crop simultaneously with or very close to the application of propanil, leaf injury will occur. This effect results from the fact that these insecticides strongly inhibit acetylcholinesterase in insects and related enzymes in other organisms. Aryl acylamidase I closely resembles acetylcholinesterase in structure and thus is also inhibited. Without the enzyme to detoxify propanil, rice plants succumb to its herbicidal properties. Matsunaka (1983) considers this to be a 'severe problem' in the practical use of propanil on rice.
The manipulation of the environment by the farmer has widespread effects on all classes of animal life. The effects of agricultural practices, particularly the use of pesticides, on the natural fauna has been the subject of many reviews (e.g. Rudd, 1965; Thompson & Edwards, 1974; Matsumura, 1975, Edwards & Stafford, 1979; Clarke et al., 1981 ;Madge, 1981; Bunyan&Stanley, 1983) This review will concentrate on diseases of man and those animals, especially mammals, which the farmer has introduced into his modified ecosystem.
The more that toxic man-made compounds are introduced into the agricultural system the greater are the chances of accidental poisoning. The field of veterinary toxicology is well covered by Clarke et al. (1981). They divide man made hazards into industrial contamination, domestic materials, drugs, pesticides and food and water.
a ) Industrial contamination
Contamination of farmland occurs, for example, with fluorine, copper, cadmium and molybdenum. Itai-ltai disease of humans in Japan resulted from consumption of rice or drinking water contaminated with cadmium originating in the effluents of a mine (Lauwerys, 1979). Heavy metal contamination of farmland by the overzealous use of sewage sludges may be a potential source of problems (e.g. see Peterson & Alloway, 1979 for cadmium). Copper contamination as a result of using pig slurry is dealt with later. For further examples of illness in this category see Clarke et al. (1981).
b ) Domestic materials
Lead, largely from lead paint, is the most common single cause of poisoning in animals, particularly cattle and dogs (Clarke et al., 1981). Other hazardous materials include disinfectants, oil and antifreeze.
c) Drugs
With intensification greater reliance is placed on the use of drugs to control disease, and they are often used prophylactically with the consequent problem of resistance developing to some classes of drugs such as antibiotics and antiparasitics. The use of drugs is fraught with potential dangers for most are selective poisons and, if given at too high a dosage, too rapidly or too frequently, they may give rise to toxic effects. Clarke et al. (1981) give numerous examples of the side effects of many drugs used in agriculture.
It is interesting that although drugs have often controlled specific diseases, which could be a problem under intensive production conditions, they have sometimes resulted in the increased incidence of other diseases. For example, the increase in haemorrhagic disease in poultry may have been due to the increased use of coccidiostats containing sulphaquinoxaline (Gibson, 1966) which, given at too high a level, leads to sulpha poisoning (see Clarke et al., 1981).
Antibiotics. The increase in antibiotic usage is inversely related to the decrease in the number of livestock owners and proportional to the increase in size of individual animal populations (Walton, 1981). Animals fed antibiotics have an increased growth rate and consume more food and, incidentally, reduced incidences of diarrhoea have been reported in young calves and pigs and liver abcesses in beef cattle fed high grain rations when antibiotics were included in the diet (Maynard et al., 1979). There is general agreement that including antibiotics at a low level as a routine feed component does result in selection for resistance with a resulting increase in the percentage of resistant organisms recovered from the animals. However, there appears to be no solid evidence that this increase in resistant organisms has caused disease problems in man that were not present prior to the development of resistance (Goldberg, 1975). The development of drug resistance appears to occur mainly as a result of the use of antibiotics in therapy rather than from inclusion of drugs in the feed.
The problem of antibiotic residues in food has mainly been with milk where the main risk of milk contamination is due to intramammary introduction of therapeutic agents (e.g. penicillin) for the control of bovine mastitis (Walton, 1981). A small percentage of the human population suffer allergic reactions to some antibiotics, e.g. tetracycline and penicillin. The primary sensitization almost certainly results from parenteral, not oral, therapy (Wishart, 1983). There are apparently, no authenticated cases of allergy induction following consumption of antibiotics in milk (Wishart, 1983) but there are some reports of hypersensitivity following milk consumption (Siegel, 1959; Wicher, 1969).
It is believed that the residues in meat are generally so minute compared with the therapeutic dose, and these are usually reduced further by food preparation, that they are of little significance (Walton, 1981). In fact Lindemayr et al., (1981) found that when a group of eight people specially selected for their sensitivity to penicillin were fed deliberately contaminated meat they developed no clinical signs of allergy nor did their blood IgE antibody levels rise. However, anaphylaxis has been reported after eating penicillin-contaminated meat (Tscheuner, 1972) and it should be borne in mind that allergic reactions in sensitive people can be stimulated by very small doses of the allergen, so the problem cannot be dismissed out of hand.
Recently, certain ecological consequences of the use of Monensin as a growth promoter has come to light (Strauch, 1982, 1983). Monensin contamination of liquid slurry reduces gas production during fermentation ( Hilpert et al, 1983) Boehnke (1983, personal communication) considers this inhibitory activity to be more important than any possible problems to the consumer of growth promoter residues.
Hormonal growth promoters. Intensive animal production has made extensive use of synthetic and purified oestrogens, androgens, progestagens, growth hormones and antibiotics to stimulate growth and fattening of meat-producing animals. However, direct and indirect side effects of these practices are well recognised (e.g. Clarke et al., 1981; Boehncke, ] 983). For example, as a result of including oestrogens in the feed, or as implants, tile incidence of bulling in steers increased and led to an increase in illness or death as a result of this activity (Pierson et al., 1976). Urolithiasis in cattle and sheep reared in feedlots has been associated with the use of oestrogen implants (Wilson, 1966). Although anabolic agents that are potent androgens can lead to an increased growth rate in calves they may delay the onset of puberty and cause dystocia, poor milk production and virilization of the genitalia (Heitzmar., 1980). They can also interfere with reproduction.
There is also concern about the possible harmful effects on the consumer of the residues of these hormonal growth promoters in the meat and this has led to their stricter control. For example, it was found that traces of oestrogenic activity remained in the meat of cockerels implanted with diethylstilboestrol (DES), a practice that had been used for a number of years to chemically caponize the birds and so improve carcass finish and quality (Clarke et al 1981), and this led to discontinuation of such implants. In general, however there is no agreement amongst scientists that the amounts of oestrogens found in meat after DES implants might be harmful. Many natural foods, including soya beans, contain higher oestrogenic activity than that found in animal tissues.
d) Pesticides
Poisoning and disease caused by pesticides are amongst the most emotive cases of agricologenic disease. This may be due partly to the fact that the effects of pesticides on lower vertebrates and invertebrates are weld known and have been cause for concern for a long time (McEwen & Stephenson, 1979; Matsumura,
Direct poisoning of domestic animals. Although, as Clarke et al. (1981) point out, pesticides have been responsible for a large proportion of accidental poisonings amongst domestic animals, the number is gradually decreasing, largely due to the replacement of deadly rodenticides such as yellow phosphorus and zinc phosphide with safer compounds such as warfarin and alphachloralose, and of insecticides such as parathion and TEPP with less toxic substances such as malathion and dimethoate. The early, highly toxic, weedkillers such as DNC and DNPP have also been largely replaced by the less toxic hormone herbicides (Harden & Paver, 1961). Nevertheless, toxic compounds are still used and cause death and illness (see Rathus, 1973 and Matsumura, 1975 for many examples). In a recent survey by the Centra] Veterinary Laboratory at Weybridge it was found that one in 25 of all fate] poisonings of livestock was caused by pesticides, the commonest causes being from organophosphorus pesticides and rodenticides (Quick, 1982).
Direct poisoning of humans. Careless application of a number of pesticides and herbicides has been the cause of disease in a number of cases in man (Matsumura, 1975; Wren et a/., 1981). Corbett (1978) considers that most occupational deaths or illnesses caused by pesticides are due to careless application of high toxicity insecticides in under-developed countries. Organophosphorus insecticides, in particular, have an extremely high mammalian toxicity and poisoning amongst sprayers occurs with some frequency (McEwen, 1977). Kiss & Fazekas (1982), amongst others, have reported frequent cases of poisoning due to exposure to cholinesterase inhibitors. Certain individuals are sensitive to some pesticides and exposure to them can be a hazard to health (Israeli & Linde, 1970).
Numbers of cases of poisoning of agricultural workers due to direct contact with pesticides are difficult to estimate. A World Health Organisation committee estimated in 1972 that there were about 500,000 cases of accidental pesticide poisoning annually (WHO, 1973) and that about 57 of these were fatal. Although the cases of poisoning were divided approximately equally between the developed and the developing countries, only about 1% of the total were fatal in the former countries and the remainder, the greater proportion, of the fatalities occurred in the latter countries. The Council on Environmental Quality (1982) quotes the figure of 19,300 medically certified pesticide poisonings in Central America between 1971 and 1976. ICAITI (1977) estimates that more than 14,000 cases of poisoning and 40 deaths from pesticides occurred in the cotton growing areas of Central America between 1972 and 1975. In 1975 in California more than 1300 persons were sufficiently poisoned by pesticides to require medical attention (van den Bosch, 1980), and it has been estimated that this figure may be only about 1% of the actual affected cases (Kahn, 1976). No accurate recent figures appear to be available for pesticide poisonings but Bull (1982) calculates that, with real growth in the world pesticide market being about 5% per annum during the 1970's, on the basis of the WHO's 1972 figures and assuming similar rates of poisoning, in 1981 there may have been approximately 750,000 cases with 13,800 deaths worldwide.
Poisoning by pesticide residues. Although many cases of direct poisoning of humans and domestic animals by pesticides have been reported, it is more difficult to show that normal consumption of pesticide residues in food affects the health of the consumer (FAO/UNO, 1972 in Corbett, 1978; Matsumura, 1975), although cases of poisoning of animals fed plants heavily contaminated with the early highly toxic pesticides, such as arsenicals, have been reported. Curley et al. (1971) reported a case of human mercury poisoning following consumption of pigs fed grain treated with organomercurial fungicide.
Side effects of 'alternative' pest control methods. Because of their concern about the side effects of using synthetic pesticides. organic farmers and horticulturalists have tended to find more 'natural' alternatives for pest control in the belief that they are less ecologically damaging. They are, however, not necessarily safer to use, viz. nicotine and Diatomaceous earth (Abrams, 1954; Ross, 1981), and the fact that they can be labelled 'natural' should not be used as an excuse for failing to determine their safety, efficiency or impact on the environment as critically as synthetic compounds.
Biological control methods are becoming increasingly popular and are without doubt considerably safer than chemical pesticides (Burges, 1981) buts as Corbett (1978) has pointed out, the successful introduction of biological control agents, however natural they may seem, does create an essentially irreversible change in the environment which may lead to unforeseen problems. Moreover .they can cause, or could be potential causes, of disease to man and his livestock although such problems would appear to be minimal (Burges, 1981). For example, some fungal control agents, such as Beauveria bassiana used for insect control, can cause allergies in man (Roberts & Yendol, 1971) and Entomophthora coronata, also used in insect control, causes mycoses in man and horses (Ignoffo, 1973). Although there is as yet no evidence of such danger from viruses or bacteria used as control agents, because of their ability to mutate the theoretical hazards are awesome and their use must be carefully monitored. A review of the safety testing procedures and potential ecological and health hazards of microbial insecticides is given by Burges (1981) and Harrap (1982).
e) Food and water
Problems in grazing animals. Although the introduction of elements 'foreign' to the agricultural system presents the main potential for poisoning the organisms within it, poisoning does occur in animals under 'extensive' systems of management in which external inputs are minimal. Thus, animals may become ill if grazed on mineral-deficient soils (Underwood, 1981). On the other hand some minerals which are present in the soil but unavailable may be concentrated by me plants and cause illness upon ingestion. Examples include chronic copper poisoning or 'toxaemic jaundice' in sheep in Australia grazing non-gramineous plants that have accumulated copper; molybdenosis in cattle grazing soils high in molybdenum and selenium poisoning in animals grazing 'indicator plants' which have accumulated the mineral (Clarke et al., 1981).
Various weeds have naturally high, often toxic, levels of nitrate (Case, 1957 Clarke et al., 1981), but the nitrate content of forage plants such as oats sorghum and corn, can rise during adverse growing conditions such as drought, and cause losses in animals feeding on them (Case, 1957). This situation is most likely to occur after heavy fertilization.
Poisoning by the non-mineral constituents of plants is, like the mineral examples, essentially a local problem and occurs in localities such as Australia and the western U.S.A. where poisonous plants may form a large proportion of the herbage available to grazing animals (Clarke et al., 1981). The symptoms of poisoning can take many different forms. In Australia, impairment of reproductive performance occurs in stock grazing on normal healthy red clover or subterranean clover both of which contain oestrogenically active substances (Bennetts et al., 1946; Braden & McDonald, 1970; Adams et al., 1981). Plant species of the families Cruciferae, Compositae and Umbelliferae contain goitrogenic substances and goitre can occur in animals feeding on pastures containing these plants, or in animals fed extensively on kale. The goitrogenic factors can also be transmitted to the milk of cows when it can cause goitre in humans drinking it (Clements, 1960; Peltola, 1961).
Although the effects of nutrient imbalance are perhaps more dramatically demonstrable in animals fed artificial diets they can occur in those fed naturally on apparently good soils. The Ca/P ratio is important for adequate nutrition and early studies suggested that the ideal ratio lay between 2 and 1. This is more applicable to non-ruminants than ruminants which are more tolerant to extreme dietary Ca/P ratios. However, where legumes make an appreciable contribution to the sward a significant number of pasture samples will be found with dietary Ca/P of 3-4 which may be imbalanced for the aged dairy cow susceptible to milk fever (Suttle, 1968).
Problems in animals fed artificial diets. The grazing animal has, to some extent, the ability to select its own dietary constituents to provide a balanced diet especially when the pasture contains a mixture of herb and weed species, which generally have a high concentration of minerals (Thomas & Trinder, 1947; Thomas & Thompson, 1948). However, animals fed artificial diets are solely dependent on what the farmer gives them and there are numerous reports of disease resulting from the inclusion of toxic substances in the diet or of inclusion of substances which, although not themselves toxic, can affect the availability of other substances, so leading to disease. Artificially dried grass and silage may be dangerous if poisonous plants are present in the crop at harvesting, for many plants retain their toxicity after drying and processing (Clarke et al., 1981). Inclusion of diseased plants can also be dangerous e.g. fungal mycotoxins produced by Claviceps spp. infecting the seed heads of cereals can lead to ergotism.
As novel sources of nutrients are introduced into artificial diets for economic reasons so the potential for side-effects increases; e.g. the inclusion of rapeseed in chick diets can result in deaths due to liver lesions(Payne, 1977 Ibrahim et al., 1980). In the past cottonseed cake and meal contained up to 1% of the complex polyphenolic compound 'gossypol' which is toxic for pigs and other species (e.g. Aherne & Kennedy , 1983 ) Heat treatment in the commercial production; of cottonseed meal decreases the proportion of free gossypol but the availability of Iysine is reduced as a result of the complexing of the gossypol with proteins. The problems with cottonseed, rapeseed and other food plants which contain antinutritive factors (e.g. saponin in alfalfa meal) are tending to be overcome by breeding varieties with low levels of the toxic compounds. Moreover, the :technology for removing or inactivating the toxic compounds during the production of foodstuffs has much improved during the past decade (Chubb, 1983). Numerous examples of toxic dietary constituents are given in Clarke et al (1981) and Liener (1980) and the problems, once recognized, can usually be quickly overcome. Chubb (1983) also discusses anti-nutritive factors in animal feedstuffs and points out that although the initial response to ingestion is a reduced growth rate and poor feed conversion efficiency, increasing levels of ingestion can produce significant pathological changes and often death.
Examples of disease induced by the inclusion of apparently innocuous substances in the diet which are involved in complex interactions with other substances, include the induction or exacerbation of a zinc deficiency syndrome in pigs (parakeratosis) and poultry (e.g. perosis) when calcium is added to the diet. Calcium interference with zinc utilization is only produced when the diet contains appreciable quantities of phytin as is the case when protein sources such as soya bean or sesame meal, or large quantities of cereals other than maize are included (Suttle, 1968). Secondary iron deficiency can occur in pigs when very high dietary levels of copper are added to the diet as a growth stimulator despite the fact that the plants used to make the feed are rarely deficient in iron. The copper reduces iron absorption by the gut (Gipp et al., 1974). The condition is usually alleviated by the addition of zinc and iron (Suttle, 1968). Copper poisoning can also occur in pen or dry-lot animals, particularly sheep, fed copper-containing mineral mixtures without compensatory amounts of molybdenum (Underwood, 1981). Sheep are extremely intolerant to cooper excess and cases of poisoning have occurred when sheep have been fed rations which have been stored or processed in contact with copper salts used in pig rations (Buck, 1970).
The dietary requirements of vitamins, minerals, trace-elements etc. of farm animals have been calculated and provided the feed compounder and farmer is aware of these, and of the content of the feed, deficiencies in the diet should be avoidable. However, as this specialized knowledge is far from universal. imbalances can still occur and can lead to disease. For example, calcium deficiency can occur in many species of domestic livestock fed cereal grain-based rations which are not supplemented by calcium. Severe stunting of growth, gross dental abnormalities and some deaths occurred in lambs and young weaned sheep fed on such an unsupplemented diet (Franklin et al., 1948).
A, problem with balancing rations is that the requirements were calculated some time ago and, with recent intensification and selective breeding the food conversion ratio and growth rate of many livestock has changed (Payne, 1977).
For those vitamins whose requirements are provided in part by intestinal synthesis, the overall lifetime synthesis of a broiler chicken is likely to be markedly reduced by both shorter growing time and the inhibitory effect on intestinal synthesis of drugs, and even to the increased dietary levels of trace minerals. Vitamin responsive reproductive disorders have most commonly occurred when the breeder diets have contained abnormally high levels of trace minerals (especially as sulphates) and these problems have been exacerbated by hard water with sulphates greater than 50 ppm (Payne, 1977). Putnam (1973) considered that there was evidence that productive livestock kept under intensive systems have only marginal supplies of many of the vitamins and discusses a number of vitamin responsive conditions.
With artificial diets it is not only the nutrient composition that is important in ensuring the health of the animal but also the way in which the food is physically presented. For example, too fine grinding of food has led to mandibular disease and curled tongue in turkey poults (Gibson, 1966). Fine grinding of low roughage diets may lead to a dramatic fall in milk fat output of lactating cows (the low milk fat syndrome). This is due to an increased rumen propionate production which leads to a reduced mobilization of free fatty acids from adipose tissue which limits the synthesis of plasma triglycerides, a major precursor of milk fat (Annison, 1973).
The nutrients supplied in the common NPK type fertilizers are obviously required for the optimum growth of plants. However, when supplied in excess they can lead to problems for the consumers of the plants, because of alterations in the plant's chemical content, or for consumers of water that has been polluted by run-off or leaching of the fertilizer (Schuphan, 1974).
a ) Nitrogen fertilizers
Of chemicals used in synthetic fertilizers, N appears to cause the most dramatic problems. Several studies have shown a correlation between exposure to N fertilizers and human cancer (Armijo & Coulson, 1975; Anon., 1977). Cases have also been reported of human infants poisoned by drinking water containing excessive concentrations of NO3- (Steyn, 1977). The main source of NO3 pollution in water supplied in agricultural areas is percolation through the soil profile. This is far less where the ground is kept covered and organic sources of N are applied, than when inorganic N is applied and when monocultural systems are used (Koepf, 1974 ;Newman, 1981: Ott et al., 1983).
Accumulation of NO3- also occurs in food plants after application of high levels of N. This accumulation is far greater when N is supplied in an inorganic form than when supplied from compost or other organic manures (Vogtmann 1979; Eggert, 1983). NO3- accumulation has led to problems with consumers, including methaemoglobinemia in babies consuming spinach, which is used extensively in baby food (Schuphan & Harnisch, 1965; Becker, 1967; Schuphan, 1970, 1974). In these cases nitrite was the toxic principle, formed from nitrate during storage or transport before canning, or by bacteria in the babies' intestines. Schuphan & Harnisch (1965) were able to induce methaemoglobinemia in rats fed spinach from plots treated with high levels of nitrogen and which had been stored prior to feeding, but methaemoglobinemia did not develop if the spinach was fed fresh. Acute poisoning can occur after consumption of nitrate by ruminants when it is partly reduced to nitrite and ammonia by rumen micro-organisms. With a high nitrate intake nitrite accumulates in the amen fluid from where it is rapidly absorbed into the blood and converts oxyhaemoglobin to methaemoglobin which leads to low blood pressure (Geurnik et al., 1979). Nitrate poisoning occurs occasionally when cattle are fed on preserved grass such as hay or prewilted silage and also when fed indoors on fresh grass, and sometimes after consuming Cruciferae such as turnips (Guernik et al., 1982). No distinct evidence of similar poisoning of grazing cattle in the Netherlands was reported by Guernik et al. (1979). Disturbances similar to laminitis have also been seen in cattle and sheep fed on rations with a high NO3_ content and irregularities of reproduction and lowered milk yield have also been reported (Case, 1957). The NO3- levels in plants, particularly from heavily fertilized pastures, can rise dramatically under adverse growing conditions and Case (1957) reports cattle being poisoned after grazing drought stricker cornfields. Lotthammer et al. (1982) reported a significant increase in milk fever in cows maintained on pastures high in NO3-(>l% DM) compared to pastures low in NO3 - (<0.30% DM). Consumption of young spring grass rich in crude protein may give rise to an energy deficit because of the imbalance between the protein and the readily available carbohydrates which can lead to ammonia intoxication and a reduction in food intake (Martens & Rayssiguier, 1980). Also, among other effects (O'Hare & Fraser, 1975) high levels of rumen ammonia are believed by some workers to reduce the availability of magnesium Kelly, 1979; Martens & Rayssiguier, 1980; Underwood, 1981). In his review Becker (1967) claims other effects of feeding fodder with even relatively low nitrate/nitrite content have been found in animal trials and these include changes in thyroid metabolism, fermentation and the status of carotene and vitamin A and E.
Numerous studies have demonstrated a positive relationship between the incidence of tetany and fertilizer treatment of the pastures with nitrogen and potash. t'Hart & Kemp (1956) in a study of 3942 cows on Dutch farms found the incidence of grass tetany to be 4.3% on pastures treated with more than 50 kg N/ha, 6.5% on pastures with excess K and N but only 0.9%O on pastures with sufficient K. The magnesium levels in the plant also appear to be affected by the way in which the nitrogen is applied to the pasture (Wilcox & Hoff, 1974; Kelly, 1979). Ammonium fertilizers tend to lower magnesium levels while nitrate fertilizers tend to raise them. The differences may be due to an effect on soil acidity (Kelly, 1979). Hypomagnesaemic tetany of cattle is typical of what Payne (1970) calls a 'production disease' which involves a disturbance in the input/ output equation. In this case Mg input from the herbage and its subsequent availability to the cow does not meet the output or loss of Mg in the faeces, milk production and that used in growth.
The role of fertilization in causing 'tetany proneness' of a pasture can be more indirect than simply affecting the Mg availability to the plant or its uptake by the animal. The botanical composition of the pasture is important. Some herbs and clovers are believed to reduce the 'tetany proneness' of a pasture either because they have some protective factor or because they have a relatively high Mg content (t'Hart, 1960). One of the almost universal effects of high N on ryograss/clover swards is to increase the grass contribution and to reduce the white clover until it may be completely eliminated (Davies & Thomas, 1971).
Increased N fertilization increases the sodium level in spinach and this, it is believed, could be a problem to health especially as K is often decreased, (Meneely, 1973). Sodium deficiency states in dairy cattle and poultry in Denmark have been related to changes in the form of nitrogen fertilization, an increase in the use of K fertilizers and a reduction in Na application (Nielsen, 1969). The decline in herbage iodine content in the Netherlands since 1961 was believed by Hartmans (1974) to be associated with a more intensive use of N fertilizer with a consequent diluting effect of the I and a lesser occurrence of legumes and herbs in the pasture. N fertilization can also reduce other minerals in plants (e.g. Co, Cu. Mo and Mn; Pope, 1971). However, much of the N effect on the mineral composition of pastures may be due to alterations in their botanical composition (Pope, 1971).
b) Potassium fertilizers
Although the role of N in inducing agricologenic disease is well known, large quantities of other commercial fertilizers can also induce disease. High levels of K in herbage as a result of K fertilization is important in the induction of grass tetany because as K is raised so the level of Mg is lowered in the herbage (Reid & Horvath, 1980) and its apparent availability in the diet is also lowered as the Na: K ratio in the rumen is of significance in Mg absorption (Martens & Rayssiguier, 1980). The importance of the Na: K ratio in magnesium absorption can probably be explained on the basis of the interrelationships between these ions and Na: K ATPase activity. The activity of this enzyme, essential for the active transport of a number of substances, appears to be inhibited by high K concentrations (Martens & Rayssiguier, 1980).
Kemp and t'Hart (1957) have shown that where the ratio K/(Ca+Mg) in the forage was less than 2.2, there were few tetany cases (0.77% of 4658 cows) whereas with a ratio greater than 2.2 the incidence was much higher (6.66% of 1908 cows). High potash fertilization of pastures can also depress herbage concentrations of calcium (Kemp & Guernik, 1978; Reid & Horvath, 1980) and sodium (Rahman et al., 1960; McNaught, 1959; Reid & Horvath, 1980). Dietary sodium deficit may also occur from consumption of young grass, which has a low Na content, and leads to a compensatory increase in salivary K. This will further reduce the Na:K ratio in the rumen and exacerbate hypomagnesaemia (Martens - Rayssiguier, 1980). If low Na levels are maintained for any length of time then Na deficiency would certainly develop in the milking cows (Underwood, 1981). Mg dressings can also lower Ca levels, particularly on sandy soils Kemp & Guernik, 1978).
c) Phosphate fertilizers
Heavy applications of phosphates can significantly increase the molybdenum content of herbage and this in turn can lead to copper deficiency in cattle grazing the pasture (Stout et al., 1951) as Mo impairs the utilization of copper by the animal (Suttle, 1968; Underwood, 1981). Pope (1971) discussed the evidence for a marginal S status of sheep in Wisconsin as a result of the increased use of high analysis P fertilizers, rather than single superphosphate, on crops, with a consequent high rate of S depletion of the soil. Similar interactions between nutrients can occur in animals grazing natural pastures, for pastures throughout the world may be deficient in one mineral or another and grazing such pastures may lead to various disorders. For example, copper toxicosis with toxaemic jaundice has been reported in sheep grazing subterranean clover pastures in Australia. The toxicosis was not due to a high level of Cu in the pastures but due to a low level of Mo which led to copper accumulation in the liver. The interactions between the various nutritionally important minerals are copmplex and increases in one or more of these by fertilizing generally has an adverse effect on one or more of the other minerals (Kemp, 1971).
d) Effect of fertilizers on availability of complex substances
Fertilizer treatment can influence the plant's levels of more complex substances. For example, vitamin C was reduced as NO3~levels in the plant increased and so higher vitamin C levels were found in plants after application of organic rather than synthetic sources of N (Senft et al., 1982). Lairon et al. (1982) also reported significant differences between the composition of plants fertilized by organic and mineral methods. Some of the substances affected by fertilization may be toxic. For example, although it is well known that kale contains goitrogenic factors, its goitrogenicity can be influenced by the fertilizer treatment. The goitrogenic effect of kale, as measured on rabbits, was greater after treatment of the soil with Chilean nitrate of soda than after ammonium sulphate, nitrochalk or after no fertilizer treatment (Allcroft & Salt, 1961). Bloomfield et al. (1962) have suggested that high levels of dietary NO3 may be goitrogenic and Horn et al. (1974) reported that thyroid dysfunction occurred in lambs born from ewes maintained on orchard grass pasture or hay fertilized with high levels of N although N fertilization had no effect on the I concentration in the plants. On the other hand, Wojtych et al. (1973) found the levels of goitrogens in kale and winter rape decreased with increasing N fertilization. It is noteworthy that Allcroft & Salt (1961) and Horn et al. (1974) used a biological assessment of goitrogenicity while Wojtych et al. (1973) measured the concentration of goitrogenic chemicals.
Many animals and humans have been poisoned by cyanogenic plants (Steyn, 1977; Clarke et al., 1981), the cyanogenicity of which can be altered by agricultural practice. The cyanide content of sorghum was found to be increased by N fertilization (Gray et al., 1968; Shaikh & Zende, 1971). Both authors found that potash did not affect the HCN content but conflicted in their findings on the effect of phosphorus, the former group finding an increase whilst the latter team found a decrease with increasing P levels.
Numerous cases of poisoning by naturally occurring oxalates in food plants have occurred (James 1972; Steyn, 1977; Clarke et al., 1981) and oxalates have been reported to be increased by over-fertilization with N fertilizers (Schuphan, 1964). Jones & Ford (1972) found that the mean oxalate concentration in the tropical grass Setaria sphacelata was increased by 5870 when N as urea was applied at a high rate compared to a low rate of application.
Fertilization does not always result in increases in toxic substances in the plants. The most important environmental factor influencing the content of the oestrogenic substance formononetin in subterranean clover is the supply of phosphate and moderately severe deficiencies of phosphate, sulphur and N can almost double the concentration of the oestrogen (Everist, 1974). Shoo & Rains (1971) found that increasing levels of phosphorus and sulphur in the soil induced significant decreases in the concentration of formononetin in subterranean clover.
In light of the recent interest in the role of dietary fibre in preventing disease it is of interest to note that it has been observed that increasing the amounts of fertilizer increases the water content and so lowers the crude fibre content of plants (Schuphan, 1970).
e ) Organic fertilizers
Although properly treated slurry and well composted manures are an essential form of soil enrichment used by organic farmers, improperly treated material especially raw slurry, can be a potential source of disease and can contaminate water courses (Strauch, 1983). Potentially pathogenic bacteria, e.g. Salmonella dublin, can survive for many weeks in raw slurry (Rankin & Taylor, 1969) and outbreaks of parasitic disease in cattle (cysticercosis) have been reported after application of human slurry to pasture (MacPherson et al., 1978). Recently, agricologenic disease has been seen in sheep in regions of intensive pig production where the pastures have been treated with liquid manure from these enterprises. Sheep are particularly sensitive to Cu excess and have suffered Cu toxicity after grazing herbage treated with pig slurry (E. Boehnke, 1983, personal communication). Although the use of chemical disinfectants is becoming increasingly important in intensive animal production, and they are known to be capable of reducing gas production during slurry fermentation (Thiemann & Willinger, 1983; Hilpert et al., 1983), very little is known of the effects of disinfectants in slurry on plants and the soil (Strauch, 1982).
Excessive use of organic manures can also lead to problems especially when supplemented with N fertilizers. Kemp & Geurnik (1978) reported that cases of NO3- poisoning occurred regularly after feeding turnips, forage rape, hay or wilted silage which had been grown in fields excessively dressed with organic manure, frequently supplemented with N fertilizer. The NO3- content of these roughages could rise to over 6% dry matter content.
The mineral fertilizers used by organic farmers are also not without danger if used unwisely. Aluminium poisoning in cattle has been reported after using red Senegal rock phosphate on acid soils in the west of England (D.R. Stickland 1982, personal communication) and cases of poisoning of sheep and cattle have been reported after the use of basic slag, usually in dry weather a week or so after the animals had been on pasture which had been fairly heavily treated Crowley & Murphy, 1962; Barden & Paver, 1961).
The practice of liming can alter the mineral content of plants. Pope (1971) reported that Co, Cu. Zn and Mn of herbage was reduced by liming while Mo was increased. Such changes could, under some circumstances, lead to disease in the consumers.
The content of potentially poisonous compounds in plants can also be altered by the use of herbicides. The herbicides 2,4-D, 2,4,5-T and MCP induce the accumulation of nitrates by plants (Schuphan, 1964, Everist, 1974 - Clarke et al 1981). According to Clarke et al. (1980) sugar beet plants appear to be particularly sensitive. Air dried leaves from plants sprayed with 2,4-D were found to contain 4.5% KNO3 on a dry matter basis, an amount considered to be well above the minimum lethal concentration in animal fodder. Untreated plants contained 0.22%. Weeds not normally consumed by cattle e.g. pigweed, ragweed and jimson weed become palatable after 2, 4-D spraying and these are toxic to grazing animals due, at least in part, to their high nitrate levels.
Herbicides have also been reported to increase the cyanide content of plants (Clarke et al., 1981). On the other hand, decreases in the content of oestrogens in red subterranean clover have been reported after spraying with sublethal doses of paraquat and this was not due to its defoliating effect (Rossiter & Barrett, 1970).
Increasingly the diets fed to intensively produced animals contain synthetic nutrients and in a summary of his work Schneider (1967) has shown that the resistance of a population to infectious disease could be determined by whether the diet was natural or synthetic. In studies on the interaction of cultures of Salmonella typhimurium with various populations of mice he found that in one group of mice, a mixed population of host genotypes (random-bred, unselected), infected with mixed strains (virulent and avirulent) of S. typhimurium those animals fed a natural diet all lived whereas those on a ration of semi-synthetic materials containing the correct proportions of all factors known to be essential for normal life all died. He believed that some natural foods contained a Salmonellosis Resistance Factor produced as a result of interaction between the plant and microbial life during growth and this factor must be fed at the time of infection; animals became susceptible within 24 hours of withdrawal from the diet.
The way in which the natural food is produced may also influence the health of the consumer. In his pioneering work McCarrison (1926) showed that as an addition to a basal diet wheat grown with cattle manure gave significantly better growth rates in rats than wheat grown with chemical fertilizers, and millet grown with cattle manure and added to a basal diet of rice for pigeons led to a slower rate of loss of body weight and a delay in the time of death, largely from polyneuritis, than when chemically fertilized millet was used. He believed that the differences were due to a higher vitamin content of the food produced with cattle manure.
Simple chemical comparisons of organically and conventionally produced food often fail to produce meaningful differences but the fact remains that several workers have found significant differences in the health and performance of animals fed the differently produced foods. Most of these studies have measured the animals' fertility. Schiller and colleagues (in Vogtmann, 1979) claim to have found a correlation between the intensive use of mineral fertilizers and increased infertility in dairy cattle. Stables & Bounds (1969), using the Milk marketing Board's records, found that applications of 100+ units N/acre were coupled with a fall in fertility of cows. Aehnelt & Hahn (1973) found that the sperm quality of bulls at breeding stations fed on fodder from chemically fertilised pastures was significantly worse than those fed on fodder from pastures fertilized predominantly with manure compost. These observations were extended by experiments to measure the reproductive performance of rabbits fed diets of hay, carrots or kohlrabi with feed concentrates to complete the ration. When biodynamically or extensively grown produce was used reproductive performance was better than when intensively produced food was used. Again with rabbits Gottschewski (1975) observed that although the total born was lowest in a group of dams fed fresh organic produce compared with groups fed fresh conventional or a commercial pelletted diet, stillbirths and postnatal losses were smaller in the former group so that the number alive per litter was the same for the organic and pelletted feed groups; the litter size in the group fed fresh conventional feed was lower.
Not all workers have found differences in fertility between groups fed organically or conventionally fertilized food (Scheunert et al., 1934; Miller & Dema 1958; Scott et al., 1960). The latter workers studied the breeding of mice fed wheat from the various sections of the Soil Association farm at Haughley organic; mixed, e.g. organically manured but with supplementary chemical fertilizers; and stockless, i.e. chemically fertilized) and a commercial diet. The wheat diet, however, was not supplemented and was obviously deficient as reproduction in all the wheat-fed groups was much worse than the group fed the commercial diet. Growth was also slow on the wheat diets (Greaves & Scott 1959).
McSheehy (1977) also failed to find any differences between the breeding performances of mice fed on diets of flour produced from wheat from the various sections at Haughley, from a neighbouring intensive farm and a commercial laboratory diet. In this experiment the flour diets were supplemented with vitamins and minerals. The only difference detected was in the weights of animals derived from parents fed from the mixed section which were heavier than those fed on the other diets. Hahn et al., (1971), however, found greatly improved ovulation and fertilization rates and greater uterine size in rabbits fed hay pellets from unfertilized grassland compared to those fed hay pellets from grassland managed intensively. This occurred despite the fact that the growth rates of animals on these diets was much worse than those fed standard rabbit pellets, although growth on the extensive diet was better than that on the intensive one. The authors considered that the intensively produced hay contained anti-oestrogenic compound.
Finally, it is necessary again to emphasize the fact that it may be important for organic manures to be properly prepared to give optimum results. Aehnelt & Hahn (1973) have stated that non-biologically prepared organic fertilizers such as slurry and liquid manure in massive quantities can unfavourably influence the quality of food produced.
Economic pressures are such that nowadays many farmers, especially conventional ones, go to great lengths to maximise yields. This invariably involves intensification, either by concentrating larger numbers of animals on the same area of pasture or confining, often indoors in controlled environment houses, large numbers of animals.
Poorer health has been recorded as a concomitant of larger herd size. For example, it was noted by Booth (1973, in Halpin, 1975) that in mastitis control programmes the level of mastitis, as estimated by milk cell counts of 129 Friesian herds, was much below average in herds of 20 cows or less and rose markedly in herds with more than 80 cows. Similar trends have been recorded with other diseases. In lower Saxony between 1964-1969 as a result of a veterinary campaign there was an 84% reduction in bovine leucosis in smaller herds (of less than 20 cattle) while larger herds could only manage 55% reduction (Schmidt, 1972). In large herds there is a greater opportunity for contact between different animals, communal feeding and probably less direct supervision of the animals all of which might be expected to make disease control more difficult.
The immunoglobulins provided to the newborn in colostrum are an important source of neonatal protection against disease. The levels of immunoglobulin in colostrum drop rapidly in the hour after birth and delay in the calves suckling, as can happen with bad management, can reduce the level of intake (Boehnke, 1983). Moreover older cows have more colostrum and a higher concentration of immunoglobulins than younger cows. Unfortunately the mean age of cows under intensive dairy production is rather low (Boeknke, 1983).
Habituation to humans (socialization) by close contact, which is more likely to happen in small herds than in large ones, has also been reported to increase disease resistance. Chickens that were talked to, offered food and handled gently showed more than a 60% reduction in the prevalence of death and pericarditis when challenged with Escherichia cold compared to an ignored group (Gross & Siegel, 1982). They also had a better feed conversion efficiency. A greater resistance to Mycoplasma gallisepticum was also found in socialized chickens compared to ignored chickens by Gross & Siegel (1979) and socialized rabbits had less atherosclerosis when cholesterol was added to their feed than rabbits that were ignored (Nerem et al., 1980).
There is no doubt, however, that intensive husbandry under carefully controlled conditions has led to a reduction in a number of diseases, particularly some parasitic ones where the control of faeces removal and the elimination of intermediate hosts can be facilitated. For example, removal of exposure to the infective organisms in the soil has led to reduction in acute swine erysipelas Switzer, 1968). Halpin (1975) points out the advantages of housing animals: animals that are housed are not at the mercy of the elements, cannot so easily fall and injure themselves, have no access to poisonous plants or toxic chemicals, do not stray and lie injured in ditches nor die sick and unattended in distant hills. Most of all they are protected from helminth diseases'. On the other hand intensive grazing systems, dense stocking in loose housing and the maintenance of poultry in the crowded conditions of deep litter systems has increased the chances of parasitic infection and increased the reliance on drugs to control the diseases (Blount & Garside, 1966; Gould, 1966; Richardson & Watson, 1971). In fact Gould (1966) believed that parasitism was the greatest problem in intensive grassland management.
Certain diseases have become more common than they used to be, e.g. fowl pox, respiratory diseases, mycoplasmosis of poultry, Newcastle disease, avian encephalomyelitis (Garside &Blount, 1966),myofibrillar hypoplasia(congential splay leg) of pigs (Thurley et al., 1967; Melrose, 1973) and some 'new' diseases appear to have developed with the increase in intensification, e.g. 'kinky back' liver and kidney syndrome, Gumboro disease, infectious avian nephrosis and turkey Y disease (Blaxland, 1967).
Certain kinds of diseases are promoted by intensivism (partly from Halpin, 1975):
a) Respiratory diseases; e.g. infectious bronchitis virus in the fowl and parainfluenza III in the housed calf. These are intensified by confinement because of the ready air-borne transmission in the crowded and moist environment of confinement houses. They are difficult to control and can lead to the more dangerous secondary infections by bacteria e.g. Pasteurella and Mycoplasma.
b) The enteric diseases, e.g. swine dysentery, coliform scours and transmissible gastroenteritis of pigs. These increase because of the possibility of close contact with faeces although they could be controlled by strict hygiene. Bacteria less pathogenic than, for example, Salmonella may take advantage of animals streseed under conditions of close confinement and so cause disease.
c) Behavioural problems such as cannibalism and feather plucking in poultry ,Blaxland, 1967), navel sucking and tongue rolling in calves, wool nibbling in sheep and tail biting, fighting, bar biting and epileptiform tonguing in pigs Fraser 1983).
d) Disease or injury caused by the physical surroundings. For example, lack `of bedding and slippery floors make leg injuries to veal calves more likely. Slatted floors used for beef production in the U.K. can predispose towards feet problems, particularly arthritic conditions, although this appears not to be a problem in the tropics (Preston & Willis 1974). Boehnke (1983, personal communication) has suggested that a combination of subclinical rumen acidosis, caused by prolonged concentrate feeding, which could produce a mild form of laminitis, and use of slatted floors may lead to the foot problems in cattle that he sees so commonly today. The use of slatted floors for chickens increases the chances of physical injury and predisposition towards staphylococcal arthritis (Dalton 1966). In a substantial survey of the disease incidence in tied and loose housed dairy cattle in Sweden, Ekesbo (1966) concluded that loose housing cowsheds, where the animals had soft bedding in the lying area and free access to the open air, gave the lowest total incidence of disease and injury of all types of housing. Closed cowsheds with slatted floors or concrete floors with no bedding in the lying area gave the highest incidence of disease and injury, irrespective of whether the animals were tied or free. Blom (1983) has recently reviewed the relationship between traumatic injuries and foot diseases and housing systems, and suggests that animals kept under traditional loose housing systems with bedding are less predisposed to these conditions than animals kept under more conventional intensive conditions.
Intensive production cannot be achieved without mechanization, and mechanical breakdowns and constructional errors are inevitable and can lead directly to various disease conditions (Dalton, 1966). Feeding and watering may be irregular under intensive systems of management, even when automated, and this may lead to problems in grazing animals, which are adapted to more or less continuous intake of food (Payne, 1970). Improper ventilation of confinement houses can cause problems or exacerbate existing ones. As well as influencing respiratory diseases the accumulation of toxic gases can cause other diseases, e.g. Carnaghan (1958) described an outbreak of keratoconjunctivitis in broiler chicks probably due to the presence of ammonia.
The lack of movement that is often associated with intensive confined systems can lead to increases in a variety of diseases. For example, Robertson & Laing (1965) found that bloat and lameness were more common when cattle were individually tied than when they were yarded. Laminitis was reported to be increased in highly fed cattle tied permanently in bytes with hard floors (King, 1966). The incidence of minor digestive upsets increases in tied-up ruminants (Halpin, 1975) although more serious infection due, for example, to Salmonella contracted from faecal contact were found to be lower in tied cattle than in cattle kept loose in an enclosure (Richardson & Watson, 1971). The lack of exercise in caged chickens is believed to contribute to the increased incidence of fatty degeneration of the liver, nephritis and other diseases (Blount & Garside, 1966).
The importance of exercise during pregnancy has been stressed by Backstrom (1973). Although close confinement of sows at farrowing reduced piglet mortality the effects were beneficial only when confinement was for a relatively short period. Prolonged restraining during pregnancy resulted in poorer piglet production and more sow ill health than when the sows were allowed to exercise. Sommer (1979) found that the restraining of sows during pregnancy resulted in a prolonged duration of parturition.
Siegel (1983) has pointed out that domesticated species can adapt to the environments of most modern intensive production units and they do so by neural and hormonal feedback mechanisms. These involve raised corticosteroid levels as part of a general stress reaction which can lead to a reduction in antibody levels and hence to a reduction in resistance to disease. Examples given by Siegel include mice infected with the nematode Trichinella spiralis where increased numbers of larvae migrated to the muscles when the animals were -grouped in such a way that fighting took place, as compared to animals kept in individual cages. Resistance of chickens to Mycoplasma gallisepticum, Newcastle disease, haemorrhagic enteritis, or Marek's disease was depressed in conditions of intense social conflict. Many other examples of the effect of social stress on immune functions and disease resistance are given by Kelley (1980).
Sometimes, however, disease resistance is apparently increased under conditions of stress. Siegel (1983) cites examples which include an increase in resistance to poliomyelitis in monkeys and Escherichia cold and Staphylococcus infection in domestic birds under conditions of high levels of behavioural stress. The apparent contradiction, however, reflects the way in which symptoms are produced in the various diseases. The role of environmental stresses on disease resistance and immune function is reviewed by Kelley (1980).
Significant improvements in the reproductive performance of farm animals have accompanied the development of intensive husbandry and the desire to maximize yield, but such high levels of performance, brought about by selection or by artificial manipulation, often strain the mother leading to various diseases e.g. multiple pregnancies in the ewe are associated with an increased incidence of vaginal prolapse and intestinal herniation (King, 1966). Similarly, the increase in growth rate associated with intensive feeding regimes has been reported to be deleterious to the health of the animals. For example, Skinner (1981) reported that Hereford bulls kept on a high plane of feeding for 76 weeks had a greater percentage of abnormal sperm than those on a diet in which concentrates were restricted. The life span of both cows and rats has been reported to be reduced as a result of overfeeding (McCay et al., 1943; Schultz, 1969). Some problems associated with the 'barley beef' system are mentioned later.
Intensification and the attempt to maximise yield has led to changes in the food input for animals whether they are kept in controlled environments or in intensive grazing systems. A number of these changes lead to imbalances in the input/
output ratio of nutrients and can lead to what Payne (1970) terms 'production diseases'. In his paper Payne divides these diseases into various groups depending on the size of the input/output ratio. Disease may occur when the input is inadequate for tile output. For example, the parturient paresis complex of dairy cows associated mainly with hypocalcaemia in the lactating cow appears to arise from the inability of certain cows to meet the massive demands of lactation for calcium. This condition was apparently first recognized at the time of the first scientific selection of cows for high milk yield under improved farm husbandry. Hypomagnesaemia in cattle, which is particularly liable to occur on improved, highly fertilized pasture, is due to an input/output imbalance of magnesium and has already been discussed.
In ketosis, imbalances occur in both directions because an inadequate input of glucose is combined with excessive production of ketone bodies. This disease occurs in sheep in late pregnancy and in cattle in full lactation and both conditions entail peak demands on energy metabolism, in which the need for glucose is high and is often not satisfied. Energy is then supplied from other intermediates resulting in production of excessive ketone bodies as by-products. The position is exacerbated the more foetuses the sheep has and the higher the yield of the cow where glucose is required for lactose synthesis. In fact, many high yielding cows are unable to consume sufficient feed to meet the demands of maximum milk production and may enter a negative energy and protein balance (Hibbitt, 1973).
These examples of comparatively well known metabolic disorders seem to have occurred at an early stage of intensification of agriculture and increased production. Other examples, however, have appeared comparatively recently on farms where high production has been sought from unusual and sometimes very abnormal diets and in which input exceeds output resulting in accumulation of potentially toxic metabolites (Payne, 1970). Acidosis is a condition which results mainly from excess lactic acid production in the rumen associated with introduction of rapidly fermentable carbohydrates into the~diet. It is a characteristic of feeding high cereal diets, especially in the 'barley beef' system where the change from the normal diet high in roughage to large quantities of rapidly fermentable carbohydrate foodstuffs occurs rapidly. Other pathological symptoms have been associated with the lactic acid acidosis of high grain, low roughage diets including bloat, liver abscesses (Wilson, 1966; Melrose, 1973), renal necrosis (King, 1966) and urolithiasis (Wilson, 1966), displaced abomasums, laminitis and lumen parakeratosis (Miller, 1979) Similar conditions occur in sheep fed high grain diets, and calves reared in confined spaces on milk substitutes and without access to hay or straw suffer bloat (Wilson, 1966). As Miller (1979) has emphasized, fibre can be considered as an essential nutrient.
A further example given by Payne (1970) of an abnormal diet leading to metabolic disturbance is a diet containing large quantities of soluble nonprotein nitrogen such as urea that leads to problems associated with nitrogen metabolism, especially ammonia poisoning. The factors affecting the probability of urea toxicity are discussed in NRC (1976)'and the general field of ammonia toxicity in ruminants is reviewed by Lewis & Buttery (1973). Although urea is often regarded as being almost synonymous with nonprotein nitrogen many other sources are available (NRC, 1976; Miller, 1979). In fact substantial quantities of 'NPK are fed to dairy cattle as part of natural feeds. Waldo (1968) states that 10~30% of fresh forage is NPN. Ammoniated products and feeds such as ammoniated rice hulls, beet pulp and citrus pulp are often used as sources of NPN for dairy cattle (NRC, 1976; Miller, 1979) but problems can arise from their use. High levels of ammoniated molasses in the feed have produced nervous symptoms resulting, for example, in cattle running wild (NRC, 1976). Some ammonium salts are relatively toxic and feeds containing them are unpalatable Conrad & Hibbs, 1968).
Athough the concept of agricologenic disease is essentially only applicable to those organisms which are directly associated with an agricultural system, i.e. the plants, animals and people which form part of the system, it is possible, by stretching the concept somewhat, to apply it to the general environment of farmland and, in particular, to the soil. Many accounts, such as those of Jacks & Whyte (1939) and Hyams (1952), have described the damaging impact that .man's activities, and especially his farming activities, have had in many areas of the world over the centuries. It is particularly apt that two of the main sections in Hyams' book should be entitled 'Man as a Parasite on the Soil' and 'Man as a Disease of Soils'. Unfortunately in spite of the widespread knowledge and understanding of this historical process of the deterioration of soils, even to the point of desertification, there seems to be little evidence that, on a wide scale, this knowledge is being applied to protect the world's soils, that most important of all humanity's assets.
Some of the more important impacts of man's agricultural activities on the soil and the environment that can be considered under this more broadly based `definition of agricologenic disease are briefly:
I erosion is a widespread, major problem in world agriculture, resulting from the application of unsuitable agricultural practices or from the increasing pressure of population on the land. Sometimes the loss of soil is so extensive that it is unlikely that it can be maintained for long without serious loss of productivity (Council for Environmental Quality, 1980). For example, serious erosion problems are found in parts of Australia (Conacher & Conacher, 1983), the U.S.A. (Pimentel & Krummel, 1977; Wittwer, 1978; 0ffice of Technology Assessment, 1982) and Canada (Rennie, 1979), particularly in association with intensive production of crops such as maize. In the U.S. Corn Belt average annual soil loss from erosion exceeds 18 tonnes per hectare (Berg, 1979) which is about twice the maximum tolerable rate, the so-called T-value that will sustain a reasonably high~ level of soil productivity. In some areas of the U.S.A. erosion rates are far in excess of the above averages (Office of Technology Assessment, 1982). Continuing high rates of erosion of topsoil are likely to result in yield declines of 30°70 or more (Parr et al., 1983).
Very closely correlated with the process of soil erosion is the loss of organic matter from the soil and the consequent deterioration of soil structure and fertility (see p. 279). Although there are many factors affecting the levels of soil organic matter, systems of continuous cropping, particularly of crops such as maize and soybeans, tend especially to result in severe reduction in organic matter. This trend may also result from regular burning of crop residues. The deterioration of soils due to soil erosion and loss of organic matter has frequently been masked by the increasing use of fertilizers (Council for Environmental Quality, 1980). Many examples of such soil deterioration have been described by Eckholm (1976).
The processes of soil deterioration and loss may be greatly reduced, even reversed, in agricultural systems which regularly utilise techniques such as crop rotations and green manuring (Council for Environmental Quality, 1980).
Problems such as salinization, alkalization and waterlogging usually occur in arid or semi-arid regions where irrigation is used to increase productivity. Frequently in these situations there is a gradual build-up of salts in the soil, in the water table or in the water draining from the cropland, and this may result in the eventual loss of the land to crop production (Office of Technology Assessment, 1982). Examples of these problems from Asia, Africa and America have been given by the Council for Environmental Quality (1980).
The unecological use of land, particularly in arid and other marginal areas is resulting in a steady encroachment of the world's deserts over the surface of the earth (Eckholm & Brown, 1977; Council for Environmental Quality, 1980 Grainger, 1982). One third of the earth's land is arid or semi-arid and more than 20% of this land, spread over some 100 countries, is directly threatened by desertification. Something in the region of 6 million hectares of land per year is being turned into desert by this process and, if it continues unabated, it is likely that by the year 2000 deserts will occupy more than three times the area they covered in 1977. Desertification is caused by overcultivation, overgrazing deforestation and the careless irrigation of fragile soils and their associated) ecosystems, eventually rendering them useless for agriculture or human habitation.
Much soil deterioration and the destruction of the vegetation cover in developing Countries, often leading to desertification, should not be considered as an agricologenic process per se. It is frequently the result of population pressures causing overgrazing, utilisation of any woody material or manure for fuel, and the spread of cultivation on to unsuitable hillsides and watersheds.
Improper use of fertilizers and other agrochemicals can aggravate rather than alleviate problems of soil deterioration and declining fertility. Furthermore, even with careful application adverse effects of these chemicals have been observed in the general ecosystem and particularly in aquatic and marine systems (Council for Environmental Quality, 1980).
Increasing use of fertilizers tends to pollute both surface and ground water particularly with nitrates. Such pollution may not only upset the biological balance In both fresh-water and marine environments but may also increase levels of nitrate in drinking water such that they pose a hazard to human health N.A.S. 1977, 1978; Wilkinson & Greene, 1982; Foster et al., 1982).
As agriculture has become more intensive and more mechanized so its impact on the rural environment has increased. There has been a continuing process of removal of hedgerows and woodland, enlargement of fields, canalization of streams, the increasing incidence of monoculture, etc.--such that the environment has become ecologically impoverished (Shoard, 1980).
There can be little doubt that, as modern agriculture has developed and become more intensified, so have the number and amount of recognised pests and diseases increased. According to Yarwood (1970): 'Between 1926 and 1960 the number of recorded diseases of our principal crops increased about threefold . . . Some of the increase . . . is due to the activities of man in increasing the numbers, prevalence and destructiveness of diseases'. Similarly, Horsfall (1979) recorded that the rapid rise of organic pesticides in the late 1940's was accompanied by a rapid rise in related disease; and he was impressed by the number of iatrogenic diseases, although this by no means reflected the whole problem. Griffiths (1981) stated that 'The existence of iatrogenic disease cannot be refuted'.
If, as has been done here, one widens the concept from that of the fairly narrowly-defined iatrogenic disease to the much more broadly-based agricologenic disease, then the increase in the number of problems directly arising as a result of the developing complexity of the husbandry system is potentially very large. The present review has only considered the more obvious impacts of the husbandry system upon crops and animals and, by stretching the concept somewhat it has been possible to extend the idea of agricologenic disease to include soils and the environment. Although it is difficult within the present scope to make a proper comparison between conventional and biological systems and to assess the 'agricologenic disease potential' of each, it is plain that the majority of examples of agricologenic disease quoted above arise from the application of conventional husbandry. Assessment of a wider literature than is indicated here confirms that conventional agriculture does have a much greater impact upon plant and animal health than do alternative systems, and this because of three particular factors:
1. Conventional agriculture tends to simplify the system to a greater extent than biological agriculture. Since increasing simplification of ecosystems frequently also increases their instability, this may account for some of the increase in disease, etc.
2. Conventional agriculture tends to introduce more factors which are foreign to the ecosystem than does the biological alternative.
3. Conventional agriculture frequently imposes stress upon the system because of its continual search for maximum productivity rather than the optimal productivity which is the preferred goal of biological agriculture.
In relation to these three factors, Lovett (1980) has drawn attention to the fact that the development of modern conventional agriculture during the past fifty years has been accompanied by considerable increases in mechanization and in the use of agrochemical energy. However, 'in the overall context of agriculture this phase has been brief' and it is now 'becoming clear that the duration of a grossly exploitative phase of agriculture is limited'. He also considers that in certain intensive monoculture operations, such as cotton production, the environmental disturbance is so great that 'the economical and biological validity of the systems is very much in question'. Lovett believes that the only long term solution to the problems which arise from intensive conventional agriculture is to minimise the environmental impact by 'restoring diversity in agricultural systems to make them more akin to natural ecosystems and thereby enhance their stability and productivity ....'.
The concept of stress in relation to agricultural systems has been discussed by Coleman & Ridgway (1983) in their review of 'stress tolerance', which can be defined as 'the reduced susceptibility of plants to pests due to the manipulation of non-genetically controlled physiological properties of the plant'. It can also be simply described as 'plant health' or disease resistance, rather diffuse concepts which are not easily definable but which nevertheless have long as been considered as being found in crops produced by biological/organic methods. Coleman & Ridgway (1983) detail how such factors as rates of fertilizer, source and balance of nutrients, soil properties, water management, crop rotations, and pesticide applications may influence the susceptibility of plants to pests. Much of the first section of this review describes how the modification of these factors, as agricultural systems have intensified, has resulted in agricologenic disease, presumably as a lowering of stress tolerance in crops produced by such methods.
The apparent success of biological farmers in enhancing stress tolerance in their crops and thus reducing pest incidence, is mentioned by Friend (1983). He states:
'One of the most interesting contributions of biological agriculture in the area of pest management is also the least understood. Many biological farmers -- certainly three fourths of the sample I interviewed in Western Europe several years ago maintain that they have few pest problems, yet they take little direct action to control pests (Friend 1978). At this point, the one common explanation offered by proponents of biological agriculture is the notion that 'a healthy soil produces healthy plants' and that pests will selectively graze unhealthy plants, an 'old saw' that was never proved and was commonly discounted by agricultural scientists. Recent work by the French parasitologist Chaboussou (1977, 1980) and, more recently, by researchers at the University of California, (Toscano et al., 1982) has begun to identify some of the mechanisms of adverse effects on pest resistance resulting from pesticide and possibly fertilizer use. Toscano et al. (1982), focusing on iceberg lettuce, found that 'insurance' treatments with several common classes of pesticides disrupted crop photosynthesis and transpiration, resulting in lower yields. Chaboussou (1977, 1980) found that not only pesticide applications but also nutrient imbalances and various combinations of the two could depress protein synthesis and increase the proportion of less complex 'intermediate metabolites', which would, in turn, be more attractive to sucking insects (Ferree, 1979). Both reports suggest promising areas of research for the future that may offer some explanation of biological farmers' relative success with pest problems'.
A recent extensive and well-documented study comparing conventional and biological systems of corn production and suggesting that crops produced by the latter are more stress tolerant ,has been summarised by Lecheries (1981). In the present context this study showed 1) that organically grown corn was more resistant to Diploic stalk rot and to lodging, and 2) in poor seasons organic corn farms performed relatively better than their conventional counterparts.
The concept of stress tolerance is also applicable to animal production since many of the problems described in the second section of this review, and in particular such things as metabolic diseases, are frequently directly related to increasing intensiveness of the production system especially more intensive rousing and dietary changes (e.g. reduced roughage/increased concentrates in ruminants).
Although most aspects of agricologenic disease tend to appear fairly quickly after the agricultural changes which trigger them off, their developmental time scale can vary quite considerably, and there is the possibility of the development of long-term 'chronic' reactions in the future, particularly in humans who are at the end of the agricultural food chain and who have a long enough life span to allow the development of diseases which may require extended 'incubation periods'. The development of such an aspect of agricologenic disease would very much parallel the growth of the so-called 'western diseases' (Trowel! & Burkitt, 1981), resulting from the increasing consumption in the western diet of food containing decreased levels of fibre and increased levels of refined carbohydrates. Examples of western diseases are diverticular disease, dental caries, diabetes, obesity and coronary thrombosis (Cleave, 1974). Agricologenic disease of this nature could arise from:
1. Long-term consumption of food containing raised levels of nitrates as a result of high nitrogen fertilization for maximum yield; also mineral imbalances resulting from fertilizer applications (see p. 377)--as most food is now grown with moderate to high inputs of fertilizers any resulting imbalances are likely to be widespread. Problems of the latter type are most likely to arise with trace elements. For example, widespread chromium deficiencies have been described in the U.S. (Tipton & Cook, 1963; Tipton et al., 1965), although in this case the deficiency is probably more closely related to food processing rather than food production methods.
2. Long-term intake of food containing small amounts of agrochemical residues such as pesticides. Although the recommended daily intakes of such substances may not often be greatly exceeded, very little is known about the effect on the human organism of regular ingestion of these chemicals over many years; neither is much known about the possible synergistic effects of the ingestion of several of such chemicals over long periods. Cases have been reported of individuals who have become allergic to traces of agrochemicals in food (Randolph, 1962) and who are affected by pesticide residues at or below the recommended daily intakes.
An example of agricologenic disease in this category concerns the nematicide dibromochloropropane (DBCP). This pesticide was widely used, in California in particular, from the late 1950's to control nematodes in a wide variety of crops. A number of studies in the 1970's showed that it had serious anti-fertility effects and genetic effects, and also produced cancer in rats and mice, and it was banned in the U.S. in 1978. However, two decades of extensive use had resulted in it contaminating the ground water, and thus the water supply, in certain areas of California, exposing the residents of those areas to long-term, low level doses of DBCP. The subsequent epidemiological study of one such area (Jackson et al., 1982) strongly suggested that there were increased levels of certain cancers in the exposed population, thus: 'Statistically significant trends of increasing risk with increasing DBCP exposure were noted for male stomach cancer, total stomach cancer and total Iymphoid leukemia'. The most commonly occurring cancers in the earlier rat and mouse studies were, significantly, also found in the stomach.
Cleave (1974) has shown that it normally requires an exposure of 20 to 30 years to a faulty diet before many of the western diseases become fully manifest in a population. Modern, intensive systems are only a very recent phenomenon in the history of agriculture, being less than 40 years old and having achieved their full development only within the last 15 to 20 years. Therefore, if, as has been suggested here, there is a parallel between western diseases and agricologenic disease, it is possible that more human-related agricologenic disease may develop in the near future.
It was pointed out in the introduction that all agricultural systems are artificial, simplified ecosystems when compared with their natural background, but even a single crop species such as a monocrop in a large field gives rise to a highly complex situation when the soil is included as part of the ecosystem. However, by using soluble mineral fertilizers as its source of fertility, conventional agriculture tends to bypass many of the processes which are normally associated with the development of soil fertility and thus to greatly simplify the normal soil-crop interactions. Similarly, conventional systems introduce foreign factors into agriculture by the widespread use of synthetic pesticides and other agrochemicals. Such materials are totally foreign to natural ecosystems and, when used in significant quantities, can disrupt the relatively balanced web of relationships which is normally found even in an agricultural situation.
It is not surprising, therefore, that the greatest agricologenic impact occurs with conventional agriculture which is continually striving to maximise its output using technologies which tend to put stress on the crops and animals being produced. A much smaller incidence of agricologenic disease is likely to occur in a system of biological agriculture, which seeks to produce the optimal sustainable output utilising techniques based on ecological principles.
Up to the present most of the problems that have resulted from simplification of the agricultural system have been overcome by 'technological fixes 'resulting from further research and development. Indeed, agricultural science may be able to provide the answers to many such problems in the future, having already done so in numerous instances in the past. But will society be prepared to pay the price for them, both in terms of cash and in the impact that further developments along similar lines may have upon the health of the environment, and of plants, animals and man? The increasing disquiet in society about the impact of modern, conventional agriculture's techniques would suggest that the price may prove to be too high.
The authors wish to express their thanks to the following for their constructive criticisms of this paper and for suggestions for its modification and improvement: Prof. E. Boehncke, Dr. R. Daniels, Prof. J.V. Lovett and Dr. D.H. Scarisbrick. Nevertheless, the final responsibility for its content, and for any errors, etc., remains with the authors.
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