Principles of helminth control

Veterinary Parasitology, 6 (1980) 1 8 5 - 2 1 5 © Elsevier Scientific Publishing Company, Amsterdam -- Printed in The Netherlands

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Control PRINCIPLES OF HELMINTH

CONTROL

R.V. B R U N S D O N

WaUaceville Animal Research Centre, Research Division, Ministry of Agriculture and Fisheries, Private Bag, Upper Hurt (New Zealand) (Accepted 25 September 1978)

ABSTRACT Brunsdon, R.V., 1980. Principles of helminth control. Vet. Parasitol., 6: 185--215. In this review of recent research on prophylactic control, the discussion primarily refers to gastro-intestinal nematodes of sheep and cattle. Eradication of most helminth infections is not practical. Rather the aim of control, is to ensure that parasite populations do not exceed levels compatible with economic production. At present most parasite control is 'protective' in orientation and is based almost entirely on the regular use of anthelmintics. While usually affording protection against serious disease and mortality, such treatments are frequently not effective in preventing the exposure of animals to high levels of pasture infestation. Consequently, production losses still occur as a result of re-infection in the interval between treatments. In contrast, recently developed preventive control programmes against parasitic gastroenteritis emphasise the principle that effective control must be based on measures designed to prevent or limit contact between parasite and host. The strategies of such preventive control are: (1) to prevent the build-up of dangerous numbers of larvae on pastures; (2) to anticipate the periods during which large numbers of larvae are likely to occur and to remove susceptible animals from heavily contaminated pastures before these periods. These aims can be achieved using three interrelated approaches: by grazing management, by the use of anthelmintics and by dependence on the acquisition of immunity. Potentially, the most efficient control requires the complete integration of all three facets. Effective, integrated control is dependent upon a detailed understanding of the sequential interrelationships between the various sources of pasture contamination, the availability of infective larvae and the build-up and decline of infections; a knowledge of the time course of events is also of paramount importance. The essential requirement of integrated control is the provision of 'safe' pasture for susceptible animals at appropriate times. Safe pasture can be produced by a variety of stock and pasture management manipulations and maintained by the use of strategic anthelmintic treatments prior to the anticipated occurrence of conditions favourable for the free-living development of the parasites. In some climatic areas, an alternative to a change to safe pasture is the use of 'critical', strategic anthelmintic treatments at times when re-infection is negligible. Systems of parasitological monitoring (e.g. faecal egg counts or pasture sampling), and forecasting on the basis of meteorological data and computer simulation provide a different approach to preventive control. Advocates suggest that such techniques allow the selection of appropriate treatment and management strategies. However, the practical value of such aids, in some circumstances, has been questioned. Because of the requirement for planned grazing in modern parasite control systems, de-

186 cisions on the i m p l e m e n t a t i o n of these c a n n o longer be separated f r o m o t h e r m a n a g e m e n t considerations. It is essential that the m e t h o d s of disease eradication, the costs and their benefits, be analysed in the broadest c o n t e x t and in relation to whole husbandry systems. This will involve a trans- or multi-disciplinary approach and will require the closest co-operation b e t w e e n helminthologists and various other specialists.

INTRODUCTION

In recent years there have been several excellent reviews of the epidemiology and control of nematode infections of grazing animals (Michel, 1969b, 1976b; Gordon, 1973). This paper is not intended to be a comprehensive review but deals primarily with those recent contributions which provide bases for integrated preventive control of parasitic gastro-enteritis in young susceptible sheep and cattle. Many of the principles discussed also apply to other helminth infections. The eradication of most helminth infections is not practical and, generally, such a course is not required in order to control economically important helminth diseases of livestock. Rather, the aim of control is to ensure that parasite populations do not exceed levels compatible with economic production. This objective is achieved by three interrelated approaches: by grazing management, by the use of anthelmintics, and by the utilization of natural or artificially induced immunity. Potentially, the most efficient control requires the complete integration of all three facets. This is possible only on the basis of a full understanding of the epidemiology of infections. Over the years there have been numerous statements and re-statements of various principles and recommended practices for the control of trichostrongylid infections. These have ranged from the application of military principles of tactics and strategies by Hall (1934) to the view of Whitlock (1955) that the basic problem is one of ecological imbalance. The latter author believes that the first step in the development of satisfactory control procedures must be the search for the factors predisposing disease outbreaks. While overall patterns of larval availability are governed by climate, the sum of husbandry practices largely determines the level of parasite hazard of a particular husbandry system. In this paper, emphasis is given to the principle that the author considers to be of paramount importance in the formulation and implementation of modern control procedures, viz., that effective control must be based on the application of knowledge of the life cycles, larval ecology and epidemiology to husbandry practices designed to prevent or limit contact between parasite and host. Subordinate principles to this are, firstly, that control measures should be specifically designed to suit local environment and climatic conditions and, secondly, they must be designed to meet the special t y p e of husbandry involved. It is perhaps ironic that the most significant recent advances in helminth control have been the result of a renewed appreciation of this long accepted principle. The renewed interest in this basic approach follows almost t w o decades during which research has, to a large extent, lacked a problem-solving

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orientation and in which, consequently, progress toward improved control systems was erratic. This situation was probably occasioned by the advent of the broad spectrum anthelmintics and the false sense of security which they engendered. It is n o w obvious that, despite the vastly improved efficacy of anthelmintics and the widespread recommendation of a multiplicity of curative, tactical and so-called preventive drenching programmes, production losses from helminth disease have remained disconcertingly high. The results of recent studies hopefully herald a return to the truly strategic use of anthelmintics, long advocated by Gordon (1948, 1957) b u t largely ignored, in which the primary objective is to prevent or reduce pasture contamination rather than to remove worms which in many cases have a very short life expectancy. The extremely slow evolution, to date, of efficient, functional preventive control systems is rather surprising in view of the fact that an awareness of the requirements for such systems was evident more than a quarter of a century ago as indicated by Russell (1949} : " I t w o u l d s e e m t h a t a n e w a p p r o a c h is b e i n g m a d e t o t h e c o n t r o l o f n e m a t o d e parasites. T h e e m p h a s i s is n o w o n p a s t u r e h y g i e n e , a c h i e v e d b y c o m b i n i n g t h e intelligent use o f a n t h e l m i n t i c s w i t h c o n t r o l l e d grazing in such a way as t o p r o t e c t y o u n g animals f r o m h e a v y i n f e s t a t i o n s a n d a t t h e same t i m e t o build-up t h e i r resistance t o parasitic disease. " T h e same principles m a y be applied t o practically all h e l m i n t h i n f e c t i o n s a n d as b e t t e r a n t h e l m i n t i c s b e c o m e available a n d m o r e k n o w l e d g e of t h e life cycles a n d b i o n o mics o f t h e various parasites are acquired, t h e r e is every r e a s o n t o h o p e t h a t t h e t r e m e n d o u s losses d u e t o parasitism of f a r m livestock will be greatly r e d u c e d . " STRATEGIES OF PREVENTIVE CONTROL, DESIRED LEVELS OF CONTROL, AND ASSESSMENT OF ECONOMIC BENEFITS

Continuing extension of our understanding of the epidemiology of infections is leading to a new appreciation of the potential benefits which may accrue from the more rational and efficient use of anthelmintic treatment as one component of a comprehensive, preventive control programme. At present, most parasite control is 'protective' in orientation and is based almost entirely on the regular use of anthelmintics. While usually affording protection against serious disease and mortality, such treatments are frequently not effective in preventing the exposure of animals to high levels of pasture infestation. Consequently, production losses can still occur as a result of reinfection in the interval between treatments. In contrast, the two strategies of preventive control are: (1) To prevent the build-up of dangerous numbers of larvae on pastures by limiting the deposition of contamination at certain periods. (2) To limit the acquistion of infection by anticipating the periods during which large numbers of larvae are likely to occur, and to remove susceptible animals from heavily contaminated pastures before these periods. These objective can be achieved only b y the complete integration of the three facets of control mentioned earlier. The essential requirement of inte-

188 grated control is the provision of 'safe' pasture for susceptible animals at appropriate times. Safe pasture may not be parasite-free b u t has t o o few infective larvae on it to be directly damaging to susceptible animals. (In the context of preventive control strategies, the author prefers the term 'safe' to that of 'clean' pasture because of the misleading 'parasite-free' implications of the latter term.) Indications of greatly improved production responses resulting from integrated control (Brunsdon, 1976a) suggest the need for a re-appraisal of criteria on which to base decisions on the level of control desired. However, the measurement of loss due to helminths and of the benefits of control is far from simple. Gordon (1973) has emphasised the point that in assessing the economics of parasitic disease and its control it is essential n o t only to consider the simple parameter of 'profit gained' but also to include 'loss avoided' (e.g., loss of breeding stock) and the cumulative effects. Michel (1971) has pointed out that within a particular production system as currently practised, helminthosis may have no harmful consequences. However, if infection were controlled, other more advantageous production systems could be employed. Thus, while in existing circumstances helminthosis is not in itself the cause of loss, a certain 'opportunity cost' is being incurred. Michel (1971) quotes as an example that in Britian there are compelling reasons why dairy heifers should calve at the same time of year as that in which they were born. When it was normal for heifers to calve at 33 months, ostertagiasis did not present a problem. However, helminthiasis is one of the limiting factors which prevents heifers from growing sufficiently rapidly to calve at 21--24 months. Frequently, parasitic disease is not recognised unless it represents a gross departure from the normal. Poor growth due to helminthiasis, but attributed to poor nutrition, is often the normal situation. When the full consequences of subclinical infections are known, the levels of infection compatible with economic production may prove to be much lower than currently accepted. In the context of increasing intensification of farming enterprises, decisions on the level of control desired, choice of methods and the assessment of the costs and the benefits of control must be made in relation to the complete husbandry system and be based on a comprehensive economic analysis of alternative control systems. Banks et al. (1966) argue that the use of c o m m o n indices of economic merit of an anthelmintic (or control system), such as mean liveweight or gross wool weight is quite fallacious. They believe that the only real index of economic benefit is an estimate of the net return from various schemes in comparison with a control group, based on a properly conducted trial. This view is supported by Anderson et al. (1976) who emphasise that the object of economic analysis is to provide the decision maker with information which will enable him to make the 'best bet' decision under the circumstances. Anderson et al. (1976) included an economic analysis in a field study to evaluate systems for the control of helminthiasis in weaned lambs. Partial farm budgeting (Morris, 1969) was the method of economic analysis used and included a sensitivity analysis. An important finding was that the most profitable

189 system was one that gave an intermediate level of parasite control, whereas a scheme which achieved only limited control yielded a low financial return, and a scheme which achieved the best control at high cost would provide economically satisfactory returns only when wool and sheep prices are high. DEFICIENCIES IN TRIAL DESIGN AND THE SIGNIFICANCE OF LARVAL CHALLENGE The magnitude of liveweight gain responses to anthelmintic treatment recorded in some recent trials suggests that earlier studies may have considerably underestimated the economic importance of trichostrongylid infection. The reason for this is that many of the earlier trials contained an inherent design deficiency (often unavoidable) in that treated and control animals grazed together, frequently on previousl]/contaminated pasture. The results of recent observations emphasise the important effects of the level of larval challenge upon the treatment response of animals and, consequently, the need for treatment groups to be run separately. Brunsdon (1976a) showed that, in three successive weaning/drenching trials, the mean liveweight gain response of lambs which were drenched and moved to safe pasture was almost eight-fold greater than that of lambs which were drenched but remained on the same pasture (previously grazed by both the lambs and their dams). Anderson (1972) found that during a period of high larval availability there was no significant weight gain response in 2-tooth wethers to fortnightly anthelmintic treatment but, soon after the larval availability decreased to low levels, weight gains of the treated animals increased. More recently, Bryan {1976) observed a significant weight gain advantage to calves drenched monthly and exposed to only a negligible level of larval challenge on pasture, compared with the weight gain of calves similarly drenched b u t exposed to a much higher level of larval challenge. It would appear that, following anthelmintic treatment, there are t w o distinct reasons for production loss associated with high larval challenge. The first is simply the result of the rapid rate of infection or reinfection of suscentible animals. The importance of this is illustrated by the results of Brunsdon (1976a), who concluded that the level of production response achieved by anthelmintic treatment of lambs at weaning depends largely on the rate of reinfection from the various sources of pasture infection available in the early post-weaning period. The higher the rate of reinfection the lower is the response to treatment. The second reason for production loss associated with larval challenge is that of apparent stimulation of the host immune response in older resistant animals. Durie and Elek (1966) showed that the reaction of sensitised calves to further challenge with Oesophagostomum radiatum was detrimental to host growth rate under field conditions. Bryan (1976) attributed an increase in the weight gain of beef calves to a reduction in larval nematode challenge and a consequent reduction in the host immune response.

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Barger et al. (1973) and Barger and S o u t h c o t t (1975a) showed that there is a reduction in wool growth of up to 18% from sheep resistant to Trichostrongylus colubriformis when such sheep are exposed to infection with larvae of this species. The reduction in wool growth was shown to occur in both sheep confined indoors and in grazing sheep. Within the limits of the latter study there was no evidence of a relationship between the intensity of the larval challenge and the reduction in wool growth rate. Anderson (1972, 1973) found that plasma pepsinogen levels were more closely related to the level of larval challenge in older resistant sheep than in younger, non-resistant weaners. Anderson (1973) is of the opinion that the relationship between intake of larvae and abomasal damage, as reflected b y plasma pepsinogen concentrations, is not a simple one. Rather, his findings suggest that the abomasal damage is preceded by the development of a hypersensitive state which may be the result of a high rate of larval intake; if the intake is low the occurrence of damage will depend on pre-conditioning by a previous infection. Anderson's (1973) results would appear to be supported by those of Reid and Armour (1975), who found that serum pepsinogen values in ewes remained elevated throughout the grazing season and were always higher than those of their lambs. The latter authors believe that their finding suggests that the ewe, although allowing few parasites to establish, was under considerable challenge in the autumn. It would seem that the effects of larval challenge on resistant animals could be avoided only by means of virtually worm-free pastures as suggested by Barger and Southcott (1975a). Even if such pastures could be prepared under farming conditions, they would probably be used more profitably to provide grazing for the younger and more susceptible portion of the flock. THE EPIDEMIOLOGICAL BASIS OF CONTROL

Effective, integrated control is dependent upon a detailed understanding of the sequential interrelationships between the various sources of pasture contamination, the availability of infective larvae and the build-up and decline of infections; a knowledge of the time course of events is also of paramount importance. The interrelationships will differ according to farm t y p e and climate. In relation to sheep, Thomas (1974a) has pointed out that in temperate regions there is increasing evidence that the epidemiology of trichostrongylid infection involves only a small number of generations. In general, the same observation applies to cattle. The actual number of generations is primarily climate dependent, and in cooler areas only one or two generations may be possible in the grazing season. Recently, improved understanding of the time sequence of events affecting the availability of infective larvae on pasture has facilitated more effective recommendations for the integrated control of trichostrongylid infection, by means of a combination of pasture and grazing management and anthelmintic treatment.

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Sheep

Pre-weaning Before weaning, spring-born lambs are exposed to two sources of nematode infection, namely, larvae derived from eggs deposited by their dams during the post~parturient rise in faecal egg output, and residual populations of overwintered larvae. In the post-weaning period, untreated lambs are exposed to a further source of infection derived from contamination resulting from their own worm burdens (self-augmentation, auto-infection) acquired from the first two sources. In accordance with the basic premises of preventive control outlined in the previous section, there are two strategies available for control of infection in the young lamb. In the first, the egg o u t p u t of the ewe is suppressed by anthelmintic treatment given either before or after lambing. In the second, lambs are moved in early to mid-summer from pasture on which they and the ewes grazed to that time. The choice between the two strategies will depend on whether the ewes and lambs initially graze a clean pasture (new pasture) or one on which there is an overwintered infestation (Boag and Thomas, 1973). When ewes lamb on clean pastures the sole source of infection for the lamb is the post-parturient rise in worm egg o u t p u t of ewes derived from previously acquired worms. To take full advantage of the virtually clean pasture it is highly desirable to drench ewes to prevent contamination of the lambing paddock (Boag and Thomas, 1973). On contaminated pasture the residual infestation provides the initial source of infection for the lambs and, equally importantly, a source of re-infection for the ewes during the peri-parturient period. In such circumstances, a single anthelmintic treatment, either pre- or post-lambing, may not eliminate the post-parturient rise but merely reduce or postpone the event (Arundel and Ford, 1969; Arundel, 1971; Boag and Thomas, 1973; Brunsdon, 1974). Sewell (1973) analysed the results of some of the earlier, published studies on the peri-parturient treatment of ewes and showed the procedure to be far from efficient, especially against Ostertagia spp. There has been little evidence to support pre- or post-lambing drenching from the point of view of pre-weaning parasitological or production responses in lambs born and reared on contaminated pasture. Leaning et al. (1970) found that a single pre-lambing drench resulted in a significant increase in the weaning weights of lambs and in carcass weights, but Cumberland (1969), Lewis and Stauber (1969), Donelly et al. (1972), Boag and Thomas (1973), Donald and Waller (1973), and Brunsdon (1974) found that the procedure had no effect on the weight gain of lambs up to weaning at approximately 12 weeks. More recently a number of studies have been conducted to define the relative roles of residual overwintered infection and the post-parturient contamination in determining the post-weaning build-up of infection in lambs. In particular, attention has been given to establishing the time course of the build-up of pasture infestations in relation to the timing of anthelmintic treatments and/or

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the stratigic removal of lambs from contaminated pasture. In the British Isles it has been shown that the post-parturient rise is the principal source of the disease producing generation of worms in lambs (Heath and Michel, 1969; Boag and Thomas, 1971; Thomas and Boag, 1972; Gibson and Everett, 1973a). Ewe contamination produces a mid-summer (July) peak of larvae on pasture, which results in disease-producing worm burdens in lambs causing an appreciable o u t p u t of worm eggs in their faeces. This in turn gives rise to a second and rather lower peak of herbage infestation in the autumn (Boag and Thomas, 1971). Michel (1976b) believes that the latter peak might not represent as frequent a cause of disease in the lambs as the July peak, b u t is likely to be the major source of infection in the following year, either as overwintered larvae on pasture or inhibited larvae within the host. Where an overwintered infestation is present on the pasture, lambs pass eggs much sooner and make a significant contribution to the disease producing infestation (Michel, 1976b). Gibson and Everett (1973a, b, 1975a, b, 1976) conducted a series of field/plot trials in which they simulated the post-parturient rise contamination b y O. circumcincta and also different levels of residual, overwintering pasture infection. The results demonstrate the different patterns of larval availability resulting from the t w o sources and also the effect of time of lambing, temperature and rainfall on the subsequent build-up of infections in the lambs. Gibson and Everett (1973a) concluded that, on pasture receiving postparturient contamination, the danger to lambs would be from early June onwards. If weaning is possible at that time the lambs should be drenched and moved to safe pasture. On pasture where only residual infestation is present, serious worm burdens will not occur until auto-infection begins in mid-August. In these circumstances intervention can be delayed until late July. However, the authors emphasise the point that the latter situation would arise only when the suppression of the post-parturient rise has been successful. In Australia, Donald and Waller (1973) also found that lambs exposed to residual infestation became infected earlier than those exposed only to ewe contamination, but lamb egg o u t p u t made no contribution to numbers of larvae on pasture before weaning. Subsequently, the lambs exposed to ewe contamination suffered clinical disease 5 weeks after weaning. Lambs exposed only to overwintered infection also developed severe clinical disease but this was delayed until 9 weeks after weaning.

Post-weaning In Australia, Donald et al. (cited in Donald, 1974) c o n d u c t e d a factorial design trial comparing drenching versus no drenching at weaning with movement onto clean or infected pastures. They found that drenching and moving onto clean pasture at weaning provided complete protection from parasitic disease throughout a wet summer without the need for any further measures. In that trial, the clean pasture was experimentally produced by grazing sheep which were drenched fortnightly to prevent contamination. However, Donald

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and Waller (1973) have pointed o u t that in Australia, where grazing is on permanent grassland and pastures are grazed throughout the year, it would be u n c o m m o n for ewes to lamb in the spring on genuinely clean pastures. Because of the prolonged survival of infective larvae over winter, special efforts would be required to produce such pastures. This would involve the prevention of contamination during at least the autumn and early winter. Nevertheless, their results suggested that clean pastures for weaning might be produced by preventing their contamination during spring, as, by the time lambs are due to be weaned, overwintered infection will have fallen to minimal levels. A similar grassland farming situation is found in New Zealand, where Brunsdon (1976a) conducted a series of trials over 3 years to evaluate responses to a weaning anthelmintic treatment of lambs subsequently grazed on pasture contaminated with trichostrongyle larvae from different sources, as shown in Table I. Because in New Zealand, as in Australia, the elimination of overwintered larvae is not practicable, exposure to residual pasture infection was included as a factor c o m m o n in all treatment groups. The results show that in the summer period (December to March) an appreciable liveweight gain advantage (mean for three trials 6.3 kg) resulted from the anthelmintic treatment of lambs at weaning if the treatment was accompanied by a move to safe pasture, i.e., pasture not grazed by ewes and lambs between the start of lambing and weaning. However, when lambs were drenched but n o t moved, the live weight gain response was small (mean for three trials 0.8 kg). The results also demonstrate that a move to safe pasture at weaning without anthelmintic treatment will provide a level of control and production response similar to or better than anthelmintic treatment alone (lambs not moved). The effects of the above treatments (Table I) on faecal egg counts are shown in Fig.1. A consistent pattern of liveweight gain response to the various treatments suggests that the three available sources of pasture infection have an additive effect in determining the level and pathogenicity of infection acquired in the post-weaning period. The results indicate that of the three sources of infection, TABLE I Experimental design of drenching trials of lambs at weaning Group No. 1 2 3 4

Treatment at weaning

Source of infection after weaning**

Drenched, moved to safe pasture* Not drenched, moved to safe pasture Drenched, not moved Not drenched, not moved

(a) (a) and (b) (a) and (c) (a), (b), (c)

*Pasture grazed only by cattle between commencement of lambing and weaning. **Sources of infection: (a) residual (overwintering) larvae; (b) contamination from worm burdens existing in lambs at weaning; (c) contamination from ewes and lambs prior to weaning.

194

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Dec

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Feb 12000

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<. m 6000

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Nov 1973

Nov 1972

Dec

Jan 1973

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F i g . 1 . Mean faecal egg counts for treatment groups in New Zealand lamb weaning/drenching trials (refer Table I ) . A - - - • G r o u p 1 - - drenched, moved to safe pasture; • • Group 2 - - not drenched, moved to safe pasture; ~ - - - ~ Group 3 - - drenched, not moved; G o Group 4 - - not drenched, not moved.

that derived from contamination deposited by the ewes and lambs before weaning is the most important. However, in the absence of this latter source, i.e., when lambs are moved to safe pasture at weaning, the worm burdens carried by lambs at that time provide a significant source of further infection by means of self-augmentation. Under New Zealand conditions, Vlassoff (1973) has found that the seasonal availability of trichostrongyle larvae on pasture follows a basic two peak pattern, i.e., late spring/early summer and autumn. In terms of the magnitude of the peaks the pattern is the reverse of that reported for the British Isles (Boag and Thomas, 1971; Gibson and Everett, 1973a), in that the second (autumn) peak is by far the greater and is the cause of most clinical trichostrongyle disease which occurs in autumn and early winter. Vlassoff (1973) found that lambs acquire their initial infections from overwintered larvae and/or larvae derived from the post-parturient rise in faecal egg output of the ewe, and are

195 re-infected in late summer and autumn by larvae derived from their own contamination. Larvae from eggs deposited on pasture during summer and early autumn develop to the infective stage b u t remain in the faeces and/or soil until sufficient moisture is available for translation. Thus, the larvae appear on the herbage en masse following the first appreciable period with a positive moisture index (rainfall minus evaporation) in late summer/early autumn. In this way, auto-infection is the principal cause of clinical trichostrongyle infection and, by comparison with the situation in the British Isles, presents an additional factor to be considered in the post-weaning control of infection. The regular occurrence of the autumn peak and knowledge of its origin have facilitated the development of a system of control based on the integration of anthelmintic treatment and grazing management (discussed in detail later). Current New Zealand recommendations for integrated control include an anthelmintic treatment given to 6-month-old lambs at the beginning of autumn (early March) accompanied by a move to pasture not grazed by the lambs during summer (December to March). This treatment is additional to the drench and move advocated for weaning. In trials in Victoria, Australia, Anderson (1972, 1973) used successive groups of 'tracer' sheep and demonstrated a marked seasonal pattern in the availability of infective larvae on pasture. Trichostrongylus spp. and Ostertagia spp. were abundant from June to October but at other times of the year the numbers of larvae virtually disappeared from the pasture. Anderson (1973) also showed that the majority of the larvae available during winter are derived from eggs deposited in late summer and autumn rather than in winter. As a result of this finding, it was possible to recommend a system of control, using only two drenches, which takes full advantage of the hot, dry summer conditions which are unfavourable for the development and survival of larvae (to be discussed in detail later). In a summer rainfall region of Australia, Southcott et al. (1976) also employed tracer sheep to monitor the development and availability of pasture infestation. These authors found that, for H. contortus, larval availability from deposition was rapid in summer and slow in autumn. Ostertagia spp. presented a marked contrast, with curtailed development in summer and contamination in autumn producing high levels of infection on pasture in late winter and early spring. Of the other species studied, intestinal Trichostrongylus spp. showed a similar pattern of development to H. contortus in summer but, as with Ostertagia spp., autumn contamination could produce infection peaks in late winter and spring. Autumn and winter conditions favoured the development of T. axei and peak infestations occurred in spring. Nematodirus spp. developed mainly in summer. All species were capable of overwintering on pasture and, with the possible exception of T. axei, a persistence of infection of at least 12 months was demonstrated. The results of these studies, in two distinct climatic areas of Australia, illustrate the need for different approaches to strategic control under different climatic conditions. Particularly with regard to Ostertagia spp. infections,

196 Anderson et al (1976) were able to achieve satisfactory control in the Mediterranean-like climate of Victoria by treating sheep with anthelmintics at the beginning, and again towards the end, of the hot, dry summer period. Southcott et al. (1976) point out that this technique has less chance of being effective in summer rainfall or variable rainfall zones where the reduction of autumn contamination may more certainly be achieved by using an anthelmintic treatment in conjunction with alternate grazing. Cattle

There is no significant post-parturient rise in the faecal egg o u t p u t of breeding cows, and most spring-born calves acquire their initial trichostrongyle infection from larvae that have overwintered on pasture. In England, Michel (1969a) showed that, in the case of Ostertagia ostertagi, the time which elapses between contamination of pasture and the appearance of infective larvae on herbage is long for pasture contaminated in spring and that this interval decreases as the season advances. Michel et al. (1970) concluded that the interval decreased from 3 months for contamination deposited in March to 2 weeks for contamination deposited in July. This means that the accumulated contamination deposited by calves during spring and early summer becomes available as infective larvae over a very short space of time from mid-summer when numbers rise rapidly; populations of larvae are negligible before this time and usually present no hazard to the grazing animal. Rose (1970) identified a number of causes which explain the sudden increase in herbage infestation in July. The pattern was subsequently confirmed by Kloosterman (1971) in The Netherlands, D o w n e y (1973) in Ireland, Nilsson and Sorelius (1973) in Sweden, Pecheur and Pouplard (1974) in Belgium, and Henriksen (1974) and Henriksen et al. (1976a, b) in Denmark. In England, the demonstration and understanding of the regularity of the pattern of larval availability was the result of a number of epidemiological studies {summarised by Michel and Lancaster, 1970), which made possible the recommendation of a successful, simple control system based on the movement of calves to safe pasture in mid-summer accompanied by an effective anthelmintic treatment. Michel and Lancaster {1970) list a number of assumptions on which the validity and success of the control measures depend, viz: (a) That the residual pasture infection in the spring will be low and that the resulting worms in the calves will n o t be sufficiently numerous to cause disease. (b) That the new season's larvae will not appear on the herbage before July. (c) That contamination of the pasture after the middle of July is relatively ineffective in creating a herbage infestation. (d) That anthelmintic treatment when the calves are moved will materially postpone the appearance of infestation on the pasture to which the calves are transferred. The simplicity and effectiveness of the recommended control procedure

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provide an excellent example of the benefits of a complete understanding of the epidemiology of an infection and knowledge of the time course of events (see next section). In New Zealand, the pattern of larval availability differs from that recorded in Europe and is n o t quite so regular and clearly delineated. Over a period of 5 years, A. Vlassoff (personal communication, 1977) has observed that between 100 and 500 larvae/kg herbage overwinter each year. Summer levels fluctuate between 300 and 4500 larvae/kg. A mid-summer peak may or may n o t occur. The maximum larval count occurs in May and ranges from 1600 to 12 000 larvae/kg. Usually a high level is maintained until June or July but by September numbers return to the spring level. The residual level of larvae on pasture in the spring does n o t appear to be dependent on the magnitude of the autumn larval peak. In contrast, Kloosterman et al. (1974) found that, in The Netherlands, the level of overwintering herbage infestation was related to the level of contamination in the preceding grazing season. Compared with the situation in Europe, the extended period providing conditions favourable for larval development in New Zealand (i.e., summer, autumn and early winter) presents additional difficulties for control based on management. Brunsdon (1972) examined the control system (drench and move) advocated by Michel (1969a). In that trial, 5-month-old calves were given two anthelmintic treatments, one week apart, in mid-summer (late January) and moved at that time to safe pasture. At 12 months of age, the mean liveweight gain of these animals was similar to that of a similar group drenched at monthly intervals throughout (8 drenches). Subsequent trials of this design (R.V. Brunsdon, unpublished data, 1974) showed that this procedure could not be guaranteed to prevent clinical disease in autumn and winter. However, the results of more recent studies (R.V. Brunsdon and A. Vlassoff, unpublished data, 1977) suggest that satisfactory control can be achieved b y a system involving two drenches, each accompanied b y a move to safe pasture. The first drench is given at the beginning of summer (December) and the second drench in autum (late March). Safe pasture for each move is that n o t grazed by calves during the preceding 3 months. THE PRODUCTION OF SAFE PASTURE

The concept of combining drenching with the movement of stock to safe pasture is not new. However, as Donald (1974) has pointed out, the criteria on which pastures can be judged to be effectively safe and the measures required to produce them have not been adequately defined and in many cases are still uncertain. Practical considerations also require that, in control procedures involving the removal of animals from contaminated pasture before it becomes infective, provision must be made for the efficient utilization of the pasture after it becomes highly infective and cannot be grazed by susceptible animals. The production of safe pastures depends on the prevention of significant

198 contamination of those pastures during critical periods. This can be achieved in a variety of ways, as described below.

The production of safe pasture by grazing and pasture management All contamination is avoided by eliminating grazing from certain areas of the farm for specified periods In this context, fodder crops, new pasture, hay and silage aftermaths all, initially, provide safe pasture. The simple expedient of 'resting' or 'spelling' pasture has often been recommended as a means of producing safe pasture. However, Donald (1969) contends that within the generally accepted limits of pasture spelling, i.e., up to 8 weeks, this procedure probably contributes little to the control of trichostrongylid infection. This view is based on the comparatively recent realization and demonstration t h a t the development, migration and survival times of infective larvae are often much longer than has previously been believed. In many circumstances, the numbers of infective larvae on the herbage when infection rates are high may reflect levels of egg o u t p u t in the relatively remote past (Donald, 1967, 1968; Michel, 1969a; Rose, 1970; Anderson, 1973; Southc o t t e t al., 1976). It would now appear that, under some climatic conditions, the production of safe pasture by 'spelling' would require an interval of 3 months or more before being regrazed. Rotational grazing is a specialised form of pasture spelling. Although this procedure has been recommended for many years as a means of control of nematode infections, a satisfactory system has not yet been developed. Efficient pasture utilization dictates that the grazing interval cannot be longer than 6--8 weeks and recent studies have shown that a rotation interval of this order does not convey any benefit in parasite control over set stocking (Gibson and Everett, 1968; Smeal et al., 1969; Levine et al., 1975). Under some climatic conditions rotational grazing systems may return animals to a much higher rather than a reduced level of pasture infestation. Because of the concentration of stock on a succession of small areas, an abnormally high level of pasture infection will result on those paddocks contaminated during extremely favourable conditions for larval development.

Contamination is reduced to an acceptable level by dilution Michel (1976a, b) has pointed out that in even moderately intensive grazing, where all the herbage grown is consumed by the stock, there is an almost constant relationship between the weight of herbage grown and the quantity of faeces with which it is contaminated. Accordingly, the chance that the herbage infection will remain below a critical level is increased as the average worm egg count of faeces is decreased. This may be achieved by grazing helmintholigically inert (resistant) stock with the susceptible animals. This concept is exemplified in the case of the single suckled calf running with its dam, or by calf rearing systems in which the cows and calves graze together or

199

in a close sequence. The cows, which consume several times as much grass and pass several times as much faeces as the calves, pass very few worm eggs. In the Ruakura system (McMeekan, 1947), in which calves graze rotationally ahead of the dairy herd the factor of dilution is about one in twelve (Michel, 1976a, b). In a modification of the Ruakura system for the intensive rearing of dairy heifer replacements (Leaver, 1970), calves graze ahead of an equal number of heifers which means that the dilution factor is only one in three. Downey and Fallon (1973) have examined a system of rotating calves ahead of a relatively small number of cows. A ratio of one cow to six calves was successful in a year of low worm infection, but the dilution effect proved inadequate in a year when infection levels were high. The results so far obtained suggest that a system based on this concept is a practical possibility. Yet another adaptation of the dilution principle involves set stocking one or two calves on each paddock of the farm (Brunsdon and Adam, 1975). Michel (1976a, b) is of the opinion that the effect of helminthologically inert stock is to prevent the creation of heavy herbage infestations solely by the dilution of contamination. He questions the long and popularly held view (Taylor, 1957) that such stock remove and destroy infective larvae from pasture in a manner analogous to vacuum cleaning. Michel (1976b) believes that resistant stock do not selectively remove larvae from herbage. Hence the concentration of larvae per unit weight of herbage would be unaltered by grazing or could increase where infective larvae are concentrated toward the base of the herbage. Southcott and Barger (1973) believe that such a conclusion is correct only if larvae are distributed randomly over the pasture area. However, they point out that neither the distribution of infective larvae on the pasture nor the grazing of the animal is likely to be random (Crofton, 1963), particularly where different host species are probably avoiding their own faeces and pursuing their own food preferences. Under these circumstances the vacuum cleaning analogy may be appropriate. Arundel and Hamilton (1975) examined the effects of mixed grazing of sheep and cattle on worm burdens in lambs. In their trial, ewes and lambs grazed either alone at different stocking rates or with steers at four ratios in which sheep comprised from 30 to 70% of the animal equivalents. The total worm burdens were low due to the management and treatment of the flock and parasites were not shown to have affected productivity. Nevertheless, the results show that mixed stocking reduced the number of parasites either specific for or best adapted to sheep, such as Ostertagia circumcincta and Nematodirus spathiger. The species of these genera that are c o m m o n in cattle were either present in sheep only at the highest proportion of cattle in the ratio as for O. ostertagi, or were absent, e.g., N. helvetianus. The parasites 'best suited' to cattle, e.g., Cooperia oncophora and Trichostrongylus axei, increased significantly as the proportion of cattle in the stocking ratio increased. No check was made on the parasites present in the cattle. There is some evidence (Herlich, 1965; Smith and Archibald, 1969) that mixed grazing may confer an immunological benefit, in that species of nema-

200 todes adapted to one host may stimulate immunity when ingested by another host and y e t not exert a detectable pathogenic effect.

Contamination is reduced by alternate grazing Alternate grazing is the term usually given to the practice of sequentially stocking a pasture with different species. As with mixed grazing, the major aim is to reduce residual pasture infestation to low levels and to limit further contamination harmful to the alternate host. Southcott and Barger (1973) note that, while alternate grazing has been recommended and theoretically justified b y many authorities, it is only recently that the practice has been experimentally evaluated. In a 5-year study in Norway, Helle (1971) examined the effect of an annual alternation of sheep and cattle on sheep parasites. In the case of species that normally overwinter on pasture, viz., Ostertagia spp. and Nematodirus spp., the alternation reduced the pasture availability of these species to negligible levels. However, this procedure had no effect on populations of species which do not normally survive the winter, viz., H. contortus, Trichostrongylus spp. and Cooperia curticei. In t w o trials in Australia, Southcott and Barger (1975) and Barger and Southcott (1975b) have assessed the decontamination of sheep and cattle pasture by varying periods of grazing by the alternate host. Grazing sheep pastures with yearling cattle for 6, 12 or 24 weeks resulted in reductions in numbers of H. contortus and Trichostrongylus colubriformis in test lambs. In comparison with continuous grazing by sheep, numbers of Nematodirus spp. were only reduced after 24 weeks grazing b y cattle. Cattle pastures grazed by sheep for 6 weeks showed no reduction in numbers of O. ostertagi or C. oncophora in test calves. After 12 weeks with sheep, numbers of O. ostertagi though not of C. oncophora were reduced, and after 24 weeks of alternate grazing both of these species were reduced. There was little evidence of transmission of cattle parasites to sheep. The only cattle nematode found in test lambs was C. oncophora after cattle had been on the pasture for 24 weeks. Numbers of this parasite were low and unlikely to be of economic significance. The transmission of sheep parasites to cattle was a more c o m m o n occurrence involving H. contortus and T. colubriformis. These trials provide evidence that the alternation of cattle and sheep could be an effective method of preparing parasitologically safer pastures. Contamination is reduced by the strategic, sequential grazing o f resistant animals o f the same species The grazing of older, non-breeding, resistant stock along with young, susceptible animals has long been advocated on the basis of a mainly theoretical assumption of a beneficial reduction in the level of infective larvae on pasture (Taylor, 1957, 1961). However, apart from the incorporation of adult cattle in calf rearing systems (see above) and general recommendations for mixed or

201

alternate grazing, there have not been specific control recommendations regarding the use of resistant stock. Gordon (1973) remarked that the use of adult non-breeding sheep for alternate grazing with young sheep merits attention. Rather surprisingly, the potential advantages of the planned management of the grazing of resistant stock have not been adequately evaluated experimentally. Biirger (1976) surveyed trichostrongyle infections in autumn (September) on a considerable number of pastures grazed exclusively by cows or by calves. He found significantly higher numbers of larvae of the genera Ostertagia, Cooperia and Nematodirus on calf pastures than on cow pastures. On the basis of this finding, Biirger (1976) suggested that, in the absence of available clean pasture, improved control of trichostrongyle infection during the late summer and autumn might be achieved by the transfer of calves to cow pastures at that time. In New Zealand, R.V. Brunsdon and A. Vlassoff (unpublished data, 1975) examined the effect on larval availability of grazing older sheep during the summer months on pasture to be grazed by Iambs during the autumn. In the first trial, two paddocks were grazed on a daily rotation by ewes and lambs from the commencement of lambing (late August) until weaning (early December). From that time until the beginning of autumn (early March) one of the paddocks (Paddock 1) was grazed by lambs while the other (Paddock 2) carried only 2-tooth wethers at an equivalent stocking rate. At the beginning of autumn the lambs and 2-tooths ('seed' animals) were removed and the paddocks re-stocked with two similar groups of lambs of common origin and grazing history. Both groups of experimental lambs were drenched at that time, and lambs on Paddock I (grazed by lambs during summer) received a further two drenches at 28-day intervals. Three autumn drenches comprise the minimum recommended drenching schedule under New Zealand conditions (Brunsdon and Adam, 1975) for situations in which control based on grazing management is not possible. Mean faecal egg counts and levels of infective larvae on pasture are shown in Fig.2. On the paddock grazed by 2-tooth wethers during summer, there was a 92.7% reduction in the peak level of infective larvae during autumn. The above trial was repeated in the following year with the only difference that, during the summer, Paddock 2 (Paddock 1 of the previous year) was grazed by weaned ewes instead of the 2-tooth wethers. The results are shown in Fig.3. On the paddock grazed by the ewes during the summer there was a 98% reduction in the peak level of larvae during autumn. In both trials there was a significant live-weight gain advantage to the lambs grazing Paddock 2 during autumn and winter although these animals received only one drench (= drench + move) compared to the three drenches given to the other group (= 3 drenches + not moved). Similar trials (R.V. Brunsdon and A. Vlassoff, unpublished data, 1976) with spring-born dairy calves showed that grazing by yearling cattle (versus grazing by calves) during summer resulted in a 60% reduction in the peak level

202

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Figs 2 a n d 3. Mean faecal egg c o u n t s a n d levels o f infective t r i c h o s t r o n g y l i d larvae o n p a s t u r e in trials t o c o m p a r e i n t e g r a t e d c o n t r o l w i t h c o n t r o l based solely o n d r e n c h i n g .

203 of infective larvae on pasture in a u t u m n (O. ostertagi and C. oncophora). Nevertheless, this reduction was n o t sufficient to prevent clinical worm infection in late winter, in calves drenched once only at the beginning of autumn (drench + move). The faecal egg count from the yearling cattle (maximum mean count, 71 eggs/g) was higher than would be expected from mature cattle, and was considered to be the basic cause of the breakdown in control. In a subsequent trial, 2-year-old steers were used to prepare safe pasture with the result that a 96.8% reduction in larval availability was achieved.

The production of safe pasture by means of anthelmintic treatment As has been remarked earlier, the aims of preventive anthelmintic treatment are best achieved when the anthelmintic is given in conjunciton with the transfer of stock to safe pasture. Whilst such treatments do not themselves produce safe pasture, t h e y assist in the maintenance of a low level of infection for a considerable period. An alternative to a change to safe pasture (per se ) is the use of 'critical' strategic anthelmintic treatments which achieve the same effect by suppressing contamination at times when free-living development is minimal. This ensures that immediate reinfection is low and the greatest proportion of the worm population is exposed to the anthelmintic (Southcott et al., 1976). In this way, critical treatments can be used to enhance or reinforce natural discontinuities in pasture infestation resulting from climatic factors. Anderson (1972, 1973) has shown that two such treatments used in conjunction with the seasonal decontamination of pastures resulting from the dry summer period in Victoria, Australia, will produce safe grazing for autumn and winter. Since weather conditions vary from year to year the times of drenching must be related to actual weather patterns. The first drench is given when pasture is noticeably drying off (October-December) and the other in midsummer (January--March). In one trial, Anderson (1973) found that the two treatments reduced the worm egg o u t p u t of treated sheep to one-tenth that of untreated sheel~ for a period of 18 weeks between October and March. In a later study, Anderson et al. (1976) demonstrated the parasitological and economic advantages of this m e t h o d of control over a traditional drenching programme. In many farming situations, particularly in specialised, intensive rearing systems, manipulations of grazing management are frequently limited, and the control of parasites must depend solely on the use of anthelmintics. In England, Potts et al. (1974) have demonstrated a strategic use of anthelmintics which provides a feasible alternative to the movement of calves to clean pasture in order to avoid the summer (July) rise of infective larvae. In their study, calves were treated on four occasions at fortnightly intervals commencing after being turned out in spring (April). Compared to the numbers of larvae recovered from pasture grazed by untreated calves, the treatments resulted in a 97% reduction in the peak summer levels of infective larvae and were reflected in a 35.7%

204

greater weight gain. This study provides an excellent example of the prophylactic use of anthelmintics in which the primary aim is to reduce pasture contamination rather than to eliminate worm burdens per se. EXAMPLES OF FULLY INTEGRATED CONTROL SYSTEMS -- ADVANTAGES AND THE REQUIREMENTS FOR HIGH ANTHELMINTIC EFFICACY

The foremost example of practical, integrated control involving grazing management is that now recognised as the 'Weybridge System', initially advocated in the British Isles by Michel (1969a) for the control of parasitic gastro-enteritis in calves. Under this system, calves remain on the same pasture during the first half of the grazing season and are moved to aftermaths before the disease producing generation of larvae appears on the harbage. An essential requirement is that calves are not subsequently brought back to pasture which they contaminated in the first half of the season. The timing of the move is critical and is recommended for 15 July (Michel, 1976a). If the calves are left on the contaminated pasture later than this they may be exposed to heavy infection. If they are moved to the aftermath too soon they could build-up a dangerous infestation there. Michel (1976a) recommends that in any case further precautions should be taken to prevent this. Either calves should be moved again in mid-August to further aftermaths or to land previously grazed by adult stock or they should be given an effective anthelmintic treatment when they are moved in July to prevent or postpone contamination of the aftermath. The results of Henriksen et al. (1976a) in Denmark, although based on small numbers of calves, clearly demonstrate the marked benefits of the summer 'drench and move' system compared with the results of regular anthelmintic treatments where animals remain on the same pasture. In New Zealand an integrated control system for mixed trichostrongyle infections of lambs has been advocated (Brunsdon and Adam, 1975; Brunsdon, 1976b), based on established sequential interrelationships between pasture contamination, the availability of infective larvae and the build-up of infections in young sheep (Brunsdon, 1970, 1974, 1976a; Vlassoff, 1973, 1976). The principal interrelationships are indicated in Figs 4 and 5 and the sequence of events is as follows: (1) The post-parturient rise in faecal egg count of the breeding ewe is the main source of contamination contributing to the spring peak of larvae on pasture. (2) Larvae from this source result in the first generation of worms which accumulate in the lambs during summer. (3) Eggs deposited by lambs in late February and early March are the source of the large autumn peak of infective larvae on pasture. (4) These larvae produce the second generation of worms in lambs -- that which causes clinical disease in autumn and winter. A proportion of these larvae also overwinter on pasture to provide a source of infection for ewes and lambs in the spring.

205 5¸

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206 (5) Most of the eggs depostied in the autumn (from the second generation worms) fail to develop because of progressively declining temperatures. This regular sequence and pattern of infection facilitates integrated control and emphasises the importance of t w o strategic control periods, viz., late November/early December (weaning) and late February/early March. The recommended control system comprises a drench during both periods, each treatment being accompanied by a grazing change to safe pasture. The definition of safe pasture is different for each of the grazing changes, viz: November/December -- pasture not grazed by ewes and the lambs from the c o m m e n c e m e n t of lambing until weaning. February/March -- pasture not grazed by lambs since weaning. The rationale of the procedure is as follows: (1) A drench and move in late November/early December means that worm burdens acquired before weaning are eliminated and that immediately after weaning the drenched lambs are exposed to only a low level of residual pasture infestation. Exposure to the second half of the spring peak is avoided. Because of dry summer conditions, the subsequent level of auto-infection is very low and of little significance before March. (2) A drench and move in late February/early March eliminates worm burdens acquired during summer and removes the drenched lambs from exposure to the normal autumn peak. On the safe pasture, little cycling and build-up of infection occurs because of the low temperatures in late autumn and winter. The suggested procedure means that, for the purposes of grazing young stock, farms should be divided into two sectors. The first sector to be used August to December; the second December to March; and then the first sector is used again from March to August. Each area, or parts thereof, may be grazed by older resistant stock when not occupied by young animals. In addition to this basic recommendation there are t w o further considerations for the long-term planning of the grazing management: (1} On properties where Nematodirus spp. infection in lambs presents an annual problem attempts should be made to avoid rearing lambs to weaning on the same ground in successive years (Nematodirus spp. differ from the other parasites in that infection is transmitted directly [via the pasture] from one season's lambs to the next). (2} It is desirable (but not essential) that lambs should not be reared to weaning on areas grazed by hoggets (sheep 6--12 months old) during the previous autumn and winter. Such areas probably carry a higher level of overwintering infection than those grazed by other stock. Under integrated control the frequency of mustering and drenching is reduced and animals are exposed to greatly reduced levels of infective larvae on pasture; the use of anthelmintics is much more efficient and production responses can be expected to be greater. In addition to its general applicability, this approach has a particular relevance to the control of disease resulting from the acquisition of large burdens of inhibited larvae (e.g., Ostertagia ostertagi) which may be unaffected by currently available anthelmintics.

207 It is suggested that when the hazard of (i.e., exposure to) serious helminth infection is eliminated from a particular production system b y planned grazing management, aspects of husbandry which might normally affect levels of infection may become relatively unimportant in a parasitological sense. Assuming the exposure of susceptible animals to a regular, seasonal peak of infective larvae is completely avoided by the prior movement of stock to safe pasture, then the size of the peak is of little consequence. It follows that other husbandry/management factors, e.g., stocking rate, which might normally affect the level of exposure of animals, are of much less importance than in traditional systems. In contrast to the effectiveness of integrated control systems, it was pointed out by Michel (1969a) in relation to O. ostertagi, that in view of the pattern of larval availability, a programme of prophylactic dosing, e.g., at monthly intervals, is inefficient. While herbage infestation is low the anthelmintic is largely wasted and after herbage infestation has risen to a high level, and the calves are ingesting larvae in great numbers, periodic dosing will not eliminate all of the production losses resulting from heavy infection. Eggs resulting from infection acquired between treatments will, at certain times, augment the existing pasture infestation. The success of integrated, preventive control whether based on the 'drench and move' concept or on 'critical' anthelmintic treatments, depends largely on negligible reinfection after treatment and on the high efficacy of the anthelmintic in order to minimise subsequent pasture contamination. In this context, the 'epidemiological' or 'hygienic' use of anthelmintics requires a reduction of worm egg o u t p u t to a very low level over an extended period. Although the minimum levels of residual worm egg o u t p u t required to ensure the success of preventive control schemes remain undefined, recent studies (Anderson and Dobson, 1975; R.V. Brunsdon and A. Vlassoff, unpublished data) suggest that currently recommended therapeutic dose rates may need to be increased, for hygienic purposes, in both integrated and routine preventive anthelmintic treatments. THE ROLE OF MONITORING AND FORECASTING IN PREVENTIVE CONTROL In contrast to the view that the primary objective of control should be to remove the hazard of serious helminth infection from systems of stock management there is the approach which Michel (1976b) has termed "scientifically guided opportunism". This is the use of monitoring and forecasting systems to provide a basis for the issue of warnings as to when precautionary measures should be taken. Michel (1976b) questions the use of such systems both on fundamental grounds and on feasibility. The use of large numbers of faecal egg counts as a basis for advice on control has been recommended b y Ross and Woodley (1968) and Neumann and Kitsch (1970) for parasitic gastro-enteritis in calves. Michel (1976b), however, doubts the value of such monitoring on the basis that the egg o u t p u t of populations of

208

Ostertagia ostertagi tends to follow a stereotyped pattern and usually reaches a peak when worm burdens are low. Ross and Woodley (1968) also recommend the monitoring of faecal egg counts as an aid to the control of nematodiriasis in lambs. However, as noted by Michel (1976b), the most damaging effect of Nematodirus infections frequently occurs before the parasites reach patency. Monitoring of faecal egg counts is also suggested by Stampa and Linde (1972) as an aid to the control of trichostrongylosis in sheep. Forecasts of helminth disease on the basis of meteorological data have the same objectives as monitoring systems, i.e., to predict the incidence of a parasitic disease or the timing of some event (Michel, 1976b). The first notable success was that of the fascioliasis forecasting m e t h o d devised by OUerenshaw and Rowlands (1959). Ross (1970) advocated a forecasting system for fascioliasis in Northern Ireland based on the number and distribution of wet days (i.e., days in which more than 1 mm of rain falls). The same author (Ross, 1975) later examined the application of the 'wet day' system for Scotland and found that the validity of the system was confirmed but that a slight adjustment of the incidence criteria was indicated. With this system, predictions are made in relation to a 'standard year'. Ross (1970) suggested that, on economic grounds, a forecasting system should specify both years of very low incidence to allow saving of normal control methods, and years of very high incidence to avoid heavy losses due to disease. In the British Isles, Ollerenshaw and Smith (1966, 1969) demonstrated a relationship between temperatures in spring and the incidence of nematodiriasis and were able to show that the incidence could be predicted on the basis of the mean one foot earth temperature for March. Smith and Thomas (1972) using this criterion were able to predict the hatching of Nematodirus battus and the spring peak of larval availability. However, the latter authors cautioned that, while the overall relationship between peak larval availability and the incidence of nematodiriasis is clear, a number of factors influence the relationship and if these change the relationship with weather may become less precise. They attribute variation in severity of disease in different seasons largely to the age of lambs and their grass intake at the time of peak hatch. Thomas (1974b) has advocated a system for predicting the date on which larvae of sheep gastro-intestinal nematodes appear on herbage in the summer. The basis of this forecast is the expectation that the rise in herbage infestation will occur when the total of 6-h 'wet' periods after 15 April reaches 100. In New Zealand, Vlassoff (1975) has demonstrated that the timing of peak availability of trichostrongyle larvae on pasture in a u t u m n can be predicted on the basis of the first positive 5-day moisture index (rainfall minus evaporation) after 1 March. In recent years there has been some interest in the development of mathematical simulation models in the belief that these will assist in improving the precision of forecasting. Barger et al. (1972) constructed a model to simulate populations of Haemonchus contortus on pasture. Over a 2-year period, predicted patterns of larval concentration on the pasture showed substantial agree-

209 ment with measured values. Gettinby et al. (1974) developed a model for predicting the development pattern of the liver fluke, Fasciola hepatica, from temperature data. The theoretical pattern was in broad agreement with the observed pattern. The basic objectives of the systems of monitoring, forecasting and simulation have been variously stated as being to assist in the development, selection and timing of appropriate management strategies for parasite control. Nevertheless, even if a forecast or prediction can be issued early enough to enable suitable action to be taken, their role in the efficient control of disease may be questionable in some circumstances. Michel (1971, 1976a, b) has emphasised that, while the forecast may be of considerable assistance in deciding on the use and/or timing of a specific treatment, e.g., anthelmintic or molluscide, its use in determining the modification of management such as a change of pasture is not necessarily compatible with efficient husbandry. He points o u t that provision, in the form of an alternative pasture, would have to be made every year in anticipation of the eventuality that a warning might be issued. To keep both options open is less than efficient. It would be far better to incorporate a change of pasture as a feature of the management system every year even if in some years it might be unnecessary. It would seem preferable to avoid a particular parasite hazard by means of grazing management, rather than to depend on annual predictions or forecasts, as to its timing and/or severity, as a basis for preventive treatment. APPLICATION O F T H E PRINCIPLES O F C O N T R O L , P R O B L E M S O F I M P L E M E N T A TION A N D E X T E N S I O N

Michel (1976b) has drawn attention to the fact that there is some conflict of opinion between parasitologists as to h o w advice on control of parasites should reach the farmer. One view is that the procedures to be employed on a particular farm should be 'made to measure'. This would require what Gordon (1973) terms 'an epidemiological excursion' on the part of the adviser -- an assessment of all relevant factors pertaining to that farm. The alternative view is that the adviser should advocate one of a number of 'ready made' grazing systems and that the farmer need know little of helminthiasis. Michel (1976b) believes that, in the long term, the second approach is the only viable one. It is possible, however, that the most effective approach may prove to be one of compromise between these t w o views. Bawden (1976) states that the sum of management practices determines the potential worm problem and that, accordingly, the parasite hazard on individual properties is an individual problem. Nevertheless, he believes that awareness of the general principles of control should enable a broad strategy to be worked out with 'individual' practices, based on experience or observations, superimposed. Although, within a single climatic zone, it is possible to recommend a single management strategy for integrated control, practical considerations may limit the application of this under some individual farm conditions. In this way a model scheme may only be practicable for part of a season and thus requires

210 the support of a compromise or contingency drenching programme. This situation is exemplified by the problems of implementation of the integrated system recommended for the control of parasitic gastro-enteritis in lambs in New Zealand which experiences a regular climatic pattern (refer pp. 204--206). The complete system of t w o drenches and two moves to safe pasture comprises a weaning or summer phase and an autumn phase separated by an interval of 12 weeks (based on weaning at approximately 12 weeks of age at the beginning of December). Both the interval and date of the March treatment and grazing change are critical. If the lambs are left on the summergrazed pasture later than the beginning of March, they m a y be exposed to a high level of larval intake resulting from auto-infection. If they are moved to new pasture earlier they could build-up heavy infestation there because of the longer period of favourable conditions (late summer/early autumn) after the change. Thus, because the length of the interval cannot be safely extended or shortened without additional treatments, recommendations are made for compromises to accommodate certain management constraints and difficulties likely to be encountered (especially on sheep only farms) as follows: (1) In the case of early weaning (e.g., in the first 2 weeks of November) the summer phase of control can be extended by advancing the recommended weaning drench and move to safe pasture, and then giving an additional drench in summer (late January). (2) In the event of shortages of safe pasture. (a) Where, regularly, there is insufficient safe pasture available to complete the summer phase of control. (b) When unforeseen summer feed shortages occur (e.g., drought years) and, as a consequence, non-safe pasture must be grazed. In both these situations an additional summer drench is required 3--4 weeks after c o m m e n c e m e n t of grazing non-safe pasture. (c) In the autumn phase, where lambs are required to graze pasture previously contaminated by them during the summer (i.e., non-safe) an additional drench should be given before June. By means of such compromises, the objectives and potential rewards of integrated control can be safeguarded. The successful promotion of schemes for the preventive control of helminths requires that discussions with, and advice given to, farmers should encompass three primary aspects (assuming the advantages of the proposal have been demonstrated). Firstly, the basic principles and rationale should be explained. Secondly, a model scheme should be proposed and an outline given of the various ways and means by which the objectives (e.g., the production of safe pasture) may be achieved. Thirdly, a number of 'permissible' compromise procedures should be suggested, which would overcome foreseeable management difficulties. It will then remain the responsibility of the individual farmer and his advisers to establish (within the suggested guidelines) the most practical procedure appropriate to his particular management system. Apart from practical considerations, it may be expected that acceptance and

211

application of a new control procedure will be governed by factors other than its success. Tromba (1965) has noted that economic considerations and established patterns of animal husbandry are of major importance in the acceptance or rejection of innovations. If these are not clearly superior or are not dictated by health hazards, they cannot be expected to supplant existing methods readily. It would seem that, to be fully effective, scientific development should perhaps be accompanied by a parallel programme of social education. In this context, an important factor affecting farmer acceptance and implementation of integrated control is what can be termed 'farmer peace of mind'. This is particularly true of new systems involving a reduction in traditional drenching frequency. It is suggested that the reluctance of farmers to accept such systems, because of lack of confidence, can be overcome by suggesting that, initially, they superimpose their traditional drenching programme over the recommended system. New Zealand experience has indicated that, in such circumstances, farmers have of their own volition omitted some of the traditional drenches because of the improved appearance and thrift of the animals. Because of the requirement for planned grazing management in modern parasite control systems, the implementation of these can no longer be considered in isolation from other farming operations. Michel (1976a) emphasises the point that helminthiasis, particularly gastro-intestinal nematode infection, is very clearly associated with certain grazing practices and can be controlled by avoiding these. The aim should be to develop production systems from which the hazard of helminthiasis has been eliminated, rather than to attempt to impose specific control measures which might not be compatible with agricultural realities. The development of such systems, and assessment of costs and benefits, can be accomplished only in relation to whole husbandry programmes and will require a trans- or multidisciplinary approach (Spedding, 1969; Bawden, 1972, 1976). This will require a re-orientation of thinking by both advisory and research personnel.

REFERENCES Anderson, N., 1972. Trichostrongylid infections of sheep in a winter rainfall region. I. Epizootiological studies in the western district of Victoria, 1966--67. Aust. J. Agric. Res., 23: 1113--1129. Anderson, N., 1973. Trichostrongylid infections of sheep in a winter rainfall region. II. Epizootiological studies in the western district of Victoria, 1967--68. Aust. J. Agric. Res., 24: 599--611. Anderson, N. and Dobson, R.J., 1975. Anthelmintic efficiency related to strategic control schemes for helminthiasis in sheep. Aust. Vet. J., 51: 67--70. Anderson, N., Morris, R.S. and McTaggart, I.K., 1976. An economic analysis of two schemes for the anthelmintic control o f helminthiasis in weaned lambs. Aust. Vet. J., 52: 174-180. Arundel, J.H., 1971. The effect of a single anthelmintic treatment at varying intervals before lambing on the peri-parturient rise of faecal nematode egg counts in ewes. Aust. Vet. J., 47: 275--279.

212 Arundel, J.H. and Ford, G.E., 1969. The use of a single anthelmintic treatment to control the post-parturient rise in faecal worm egg count of sheep. Aust. Vet. J., 45: 89--93. Arundel, J.H. and Hamilton, D., 1975. The effect of mixed grazing of sheep and cattle on worm burdens in lambs. Aust. Vet. J., 51 : 436--439. Banks, A.W., Hall, C. and Korthals, A., 1966. Economics of anthelmintic treatment. Field trial in sheep in South Australia. Aust. Vet. J., 42: 116--127. Barger, I.A. and Southcott, W.H., i975a. Trichostrongylosis and wool growth. 3. The wool growth response of resistant grazing sheep to larval challenge. Aust. J. Exp. Agric. Anita. Husb., 15: 167--172. Barger, I.A. and Southcott, W.H., I975b. Control of nematode parasites by grazing management - - I. Decontamination of cattle pastures by grazing with sheep. Int. J. Parasitol., 5: 39--44. Barger, I.A., Benyon, P.R. and Southcott, W.H., 1972. Simulation of pasture larval populations of Haemonchus contortus. Proc. Aust. Soc. Anita. Prod., 9: 38--42. Barger, I.A., Southcott, W.H. and Williams, V.J., 1973. Trichostrongylosis and wool growth. 2. The wool growth response of infected sheep to parenteral and duodenal cystine and cysteine supplementation. Aust. J. Exp. Agric. Anita. Husb., 13: 351. Bawden, R.J., 1972. Drenching rationalised. Chiasma, 10: 64--70. Bawden, R.J., 1976. The Organisation of Parasitological Research into Field Problems. Abstracts of Papers, Annual General Meeting, Australian Society for Parasitology, May 17--18, p. 7. Boag, B. and Thomas, R.J., 1971. Epidemiological studies on gastro-intestinal nematode parasites of sheep. I. Infection patterns on clean and autumn contaminated pasture. Res. Vet. Sci., 12: 132--139. Boag, B. and Thomas, R.J., 1973. Epidemiological studies on gastro-intestinal nematode parasites of sheep. The control of infection in lambs on clean pasture. Res. Vet. Sci., 14: 11--20. Brunsdon, R.V., 1970. Seasonal changes in the level and composition of nematode worm burdens in young sheep. N . Z . J . Agric. Res., 13: 126--148. Brunsdon, R.V., 1972. The potential role of pasture management in the control of trichostrongyle worm infection in calves with observations on the diagnostic value of plasma pepsinogen determinations. N.Z. Vet. J., 20: 214--220. Brunsdon, R.V., 1974. An evaluation of the parasitological and production responses to a single pre-lambing anthelmintic treatment of ewes. N . Z . J . Exp. Agric., 2: 223--230. Brunsdon, R.V., 1976a. Responses to the anthelmintic treatment of lambs at weaning: the relative importance of various sources of contamination in trichostrongyle infections. N.Z.J. Exp. Agric., 4: 275--279. Brunsdon, R.V., 1976b.,Grazing management in parasite control. Proceedings of the 6th Seminar of the New Zealand Veterinary Association, Sheep Society, pp. 74--82. Brunsdon, R.V. and Adam, J.L. (Editors), 1975. Internal Parasites and Animal Production. New Zealand Society of Animal Production, Editorial Services Ltd., Wellington, Occasional Publication No. 4. 53 pp. Bryan, R.P., 1976. Helminth control in Queensland beef cattle: comparison of part paddock and whole paddock treatment in the wallum of south eastern Queensland. Aust. Vet. J., 52: 267--271. Biirger, H.J., 1976. Trichostrongyle infestation in autumn on pastures grazed exclusively by cows or b y calves. Vet. Parasitol., 1: 359--366. Crofton, H.D., 1963. Nematode Parasite Population in Sheep and on Pasture. Commonw. Inst. Helminthol., St Albans, Tech. Commun., 35, 104 pp. Cumberland, G.L.B., 1969. In: 1968--69 Annual Report of Research Division, Department of Agriculture, New Zealand, p. 147. Donald, A.D., 1967. Populations of strongyloid infective larvae in pastures after sheep are removed from grazing. Aust. Vet. J., 43: 122--124. Donald, A.D., 1968. Ecology of the free-living stages of nematode parasites of sheep. Aust. Vet. J., 44: 139--144.

213 Donald, A.D., 1969. The control of sheep helminths. Grazing management and control of parasitism. A discussion of general principles. Victorian Vet. Proc., Year 1968--69, 27: 34--36. Donald, A.D., 1974. Some recent advances in the epidemiology and control of helminth infection in sheep. Proc. Aust. Soc. Anita. Prod., 10: 148--155. Donald, A.D. and Waller, P.J., 1973. Gastro-intestinal nematode parasite populations in ewes and lambs and the origin and time course of infective larval availability in pastures. Int. J. Parasitol., 3: 219--233. Donnelly, J.R., McKinney, G.T. and Morley, F.H.W., 1972. Lamb growth and ewe production following anthelmintic drenching before and after lambing. Proc. Aust. Soc. Anita. Prod., 9: 392--395. Downey, N.E., 1973. Nematode parasite infection of calf pasture in relation to the health and performance of grazing calves. Vet. Rec., 93: 505--514. Downey, N.E. and Fallon, R., 1973. Intensive calf grazing: management systems for fewer worms and better gains. Farm F o o d Res., 4: 102--105. Durie, P.H. and Elek, P., 1966. The reaction of calves to he|minth infection under natural grazing conditions. Aust. J. Agric. Res., 17: 91--103. Gettinby, G., Hope-Cawdery, M.J. and Grainger, J.N.R., 1974. Forecasting the incidence of Fascioliasis from climatic data. Int. J. Biomet., 18: 319--323. Gibson, T.E. and Everett, G., 1968. A comparison of set stocking and rotational grazing for the control of trichostrongylosis in sheep. Br. Vet. J., 124: 287--298. Gibson, T.E. and Everett, G., 1973a. Residual pasture larval infection and the spring rise as sources of Ostertagia circumcincta infection in lambs. J. Comp. Pathol., 83: 583--588. Gibson, T.E. and Everett, G., 1973b. The effect of the postparturient faecal egg count on the worm burden of lambs and on their weight gain. Br. Vet. J., 129: 448--455. Gibson, T.E. and Everett, G., 1975a. Ostertagia circumcincta infection in lambs originating from larvae which survived the winter. Vet. Parasitol., 1: 77--83. Gibson, T.E. and Everett, G., 1975b. An experimental investigation of the postparturient rise of faecal egg count of Ostertagia circumcincta as a source of infection for lambs. Vet. Parasitol., 1: 85--89. Gibson, T.E. and Everett, G., 1976. The effect of weather in modifying the pattern of pasture larval contamination with Ostertagia circumcincta. Int. J. Biomet., 20: 49--55. Gordon, H.McL., 1948; The epidemiology of parasite diseases, with special reference to studies with nematode parasites of sheep. Aust. Vet. J., 24: 17--44. Gordon, H.McL., 1957. Helminthic diseases. Adv. Vet. Sci., 3: 287--351. Gordon, H.McL., 1973. Epidemiology and control of gastrointestinal nematodes of ruminants. Adv. Vet. Sci., 17: 395--437. Hall, M.C., 1934. A manual of tactics and strategy of warfare on parasites. Section III. The Application of military principles in the war on parasites. North Am. Vet., 15: 24--33. Heath, G.B.S. and Michel, J.F., 1969. A contribution to the epidemiology-of parasitic gastro-enteritis in lambs. Vet. Rec., 85: 305--308. Helle, O., 1971. The effect on sheep parasites of grazing in alternate years by sheep a n d , cattle. A comparison with set-stocking, and the use of anthelmintics with these grazing arrangements. Acta Vet. Scand., Suppl. 33, 59 pp. Henriksen, Sv.Aa., 1974. Parasitologiske graesmarksundersogelser i Danmark. (Parasitological examinations on pasture in Denmark. ) Proc. 12th Nord. Vet. Congr. Reykjavik. Henriksen, Sv.Aa., J~rgensen, R.J., Sejrsen, K.R., Brolund Larsen, J. and Klausen, S., 1976a. Ostertagiasis in calves. I. The effect of control measures on infection levels and body weight gains during the grazing season in Denmark. Vet. Parasitol., 2: 259--272. Henriksen, Sv.Aa., Benholm, B.R. and Nielsen-Englyst, A., 1976b. Unders~gelser vedr~rende lobe-tarmstrongylider hos kvaeg. II. Saesonvariationer i L3-kontaminationen pa graesgange. (Investigations in the herbage infestation with infective larvae. ) Nord. Vet. Med., 2 8 : 2 0 1 - - 2 0 9 (with English abstract). Herlich, H., 1965. Immunity and cross immunity to Cooperia oncophora and Cooperia pectinata in calves and lambs. Am. J. Vet. Res., 26: 1037--1041. Kloosterman, A., 1971. Observations on the epiderniology of trichostrongylosis of calves. Meded. Landbouwhogesch., Wageningen, 71: 1--114.

214 Kloosterman, A., Baas, R.J. and Van der Brink, R., 1974. Significance of overwintered pasture infection for trichostrongylosis in calves. Tijdschr. Diergeneeskd., 99: 1053-1059. Leaning, W.H.D., Cairns, G.C., McKenzie, J.K. and Hunter, W.R., 1970. Drenching of pregnant ewes and its effect on their wool production and lamb growth rate. Proc. N.Z. Soc. Anim. Prod., 30: 52--64. Leaver, J.D., 1970. A comparison of grazing systems for dairy herd replacements. J. Agric. Sci., Camb., 75: 265--272. Levine, N.D., Clark, D.T., Bradley, R.E. and Kantor, S., 1975. Relationship of pasture rotation to acquisition of gastrointestinal nematodes by sheep. Am. J. Vet. Res., 36: 1459--1464. Lewis, K.H.C. and Stauber, V.V., 1969. The effects of pre-lambing anthelmintic drenching on production of ewes and the development of worm parasitism in lambs. Proc. N.Z. Soc. Anita. Prod., 29: 177--191. McMeekan, C.P., 1947. New Zealand pasture: its value for milk and meat production. Aust. Vet. J., 23: 105--114. Michel, J.F., 1969a. Observations on the epidemiology of parasitic gastro-enteritis in calves. J. Helminthol., 43: 111--133. Michel, J.F., 1969b. The epidemiology and control of some nematode infections of grazing animals. Adv. Parasitol., 7: 211--282. Michel, J.F., 1971. Some reflections on the study of epidemiological problems in veterinary parasitology. In: Centraal Diergeneeskundig Institut, Facts and Reflections: a Symposium. The Institute, Lelystad, pp. 19--29. " Michel, J.F., 1976a. The hazard of nematode infection as a factor in the management of cattle. ADAS (Agric. Dev. Advis. Serv.)20: 162--177. Michel, J.F., 1976b. The epidemiology and control of some nematode infections in grazing animals. Adv. Parasitol., 14: 355--397. Michel, J.F. and Lancaster, M.B., 1970. Experiments on the control of parasitic gastroenteritis in calves. J. Helminthol., 44: 107--140. Michel, J.F., Lancaster, M.B. and Hong, C., 1970. Field observations on the epidemiology of parasitic gastro-enteritis in calves. Res. Vet. Sci., 11: 255--259. Morris, R.S., 1969. Assessing the economic value of veterinary services to primary industries. Aust. Vet. J., 45: 295--300. Neumann, H.J. and Kitsch, H., 1970. Neuzeitliche Bekiimpfung der Weideparasiten in Schleswig-Holstein. Tieraerztl. Umsch., 25: 233--238. Nilsson, O. and Sorelius, L., 1973. Trichostronylidinfektioner hos nStkreatur i Sverige. (Trichostrongyle infections in cattle in Sweden.) Nord. Vet. Med., 2 5 : 6 5 - - 7 8 (with English abstract). Ollerenshaw, C.B. and Rowlands, W.T., 1959. A method of forecasting the incidence of fascioliasis in Anglesey. Vet. Rec., 71: 591--598. Ollerenshaw, C.B. and Smith, L.P., 1966. An empirical approach to forecasting the incidence of nematodiriasis over England and Wales. Vet. Rec., 79: 536--540. Ollerenshaw, C.B. and Smith, L.P., 1969. Meteorological factors and forecasts of helminth disease. Adv. Parasitol., 7: 283--323. Pecheur, M. and Pouplard, L., 1974. Observations sur l'~pid~miologe de la trichostrongylose des bovins. Ann. Med. Vet., 118: 429--457. Potts, J.M., Jones, R.M. and Cornwell, R.L., 1974. Control of bovine parasitic gastroenteritis by reduction of pasture larval levels. In: Proc. 3rd Int. Congr. Parasitol., Munich, 1974, 2 : 7 4 7 - - 7 4 8 (abstract). Reid, J.F.S. and Armour, J., 1975. Seasonal variations in the gastro-intestinal nematode populations of Scottish hill sheep. Res. Vet. Sci. 18: 307--313. Rose, J.H., 1970. Parasitic gastro-enteritis in cattle. Factors influencing the time of the increase in worm population of pastures. Res. Vet. Sci., 11: 199--208. Ross, J.G., 1970. The Stormont "wet day" forecasting system for fascioliasis. Br. Vet. J., 126: 401--408.

215 Ross, J.G., 1975. A study of the application of the Stormont "wet day" fluke forecasting system in Scotland. Br. Vet. J., 131: 486--497. Ross, J.G. and Woodley, K., 1968. Parasitic disease forecasts: experiences in Northern Ireland. Rec. Agric. Res. (Northern Ireland), 17: 23--29. Russell, A., 1949. The control of parasites (helminths). Vet. Rec., 61: 238--239. Sewell, M.M.H., 1973. The influence of anthelmintic treatment of ewes on the relative proportions of gastro-intestinal nematode parasites in their lambs. (Corresp.). Vet. Rec., 92: 371--372. Smeal, M.G., Farleigh, E. and Major, G.W., 1969. Effect of a rotational grazing system on nematode infection in sheep. Aust. Vet. J., 45: 554--557. Smith, H.J. and Archibald, R.McG., 1969. Development of cross immunity in lambs by exposure to bovine gastrointestinal parasites. Can Vet. J., 10: 286--290. Smith, L.P. and Thomas, R.J., 1972. Forecasting the spring hatch of Nematodirus battus by the use of soil temperature data. Vet. Rec., 90: 388-392. Southcott, W.H. and Barger, I.A., 1973. Alternate grazing for control of worm parasites. Proc. Third World Conf. Anim. Prod., 1973, pp. 246--250. Southcott, W.H. and Barger, I.A., 1975. Control of nematode parasites by grazing management -- II. Decontamination of sheep and cattle pastures by varying periods of grazing with the alternate host. Int. J. Parasitol., 5: 45--48. Southcott, W.H., Major, G.W. and Barger, I.A., 1976. Seasonal pasture contamination and availability of nematodes for grazing sheep. Aust. J. Agric. Res., 27: 277--286. Spedding, C.R.W., 1969. The eradication of parasitic disease. Vet. Rec., 84: 625. Stampa, S. and Linde, S., 1972. A contribution towards the diagnosis of trichostrongylosis in flocks of sheep under field conditions. J.S. Aft. Vet. Med. Assoc., 43: 95--99. Taylor, E.L., 1957. An account of the gain and loss of the infective larvae of parasitic nematodes in pastures. Vet. Rec., 69: 557--563. Taylor, E.L., 1961. Control of worms in ruminants by pasture management. Outlook Agric., 3: 139--144. Thomas, R.J., 1974a. The epidemiology and control of trichostrongylid infections of sheep in temperate areas. Proc. 3rd Int. Congr. Parasitol., 2 (Sect. B17): 740--741. Thomas, R.J., 1974b. The role of climate in the epidemiology of nematode parasitism in ruminants. In: A.E.R. Taylor and R. Muller (Editors), Symposia of the British Society for Parasitology. Vol. 12, pp. 13--32. Thomas, R.J. and Boag, B., 1972. Epidemiological studies on gastro-intestinal nematode parasites of sheep. Infection patterns on clean and summer-contaminated pasture. Res. Vet. Sci., 13: 61--69. Tromba, F.G., 1965. Biological control of helminthic diseases. Vet. Med., 60: 69--74. Vlassoff, A., 1973. Seasonal incidence of infective trichostrongyle larvae on pasture grazed by lambs. N.Z.J. Exp. Agric., 1: 293--301. Vlassoff, A., 1975. The role of climate in the epidemiology of gastro-intestinal nematode parasites of sheep and cattle. In: Symposium on Meteorology and Food Production, 14--15 October, 1975. New Zealand Meteorological Service, Wellington, pp. 171--176. Vlassoff, A., 1976. Seasonal incidence of infective trichostrongyle larvae on pasture: the contribution of the ewe and the role of the residual pasture infestation as sources of infection to the lamb. N.Z.J. Exp. Agric., 4: 281--284. Whitlock, J.H., 1955. Trichostrongylidosis in sheep and cattle. Proceedings Book, Am. Vet. Med. Assoc., 92nd Annual Meeting, Mineapolis, August 15--18, 1955., pp. 123--131.