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The ecological basis of parasite control: Nematodes
Veterinary Parasitology, 11 (1982) 9--24 Elsevier Scientific Publishing Company, Amsterdam -- Printed in The Netherlands
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THE ECOLOGICAL BASIS OF PARASITE CONTROL: NEMATODES
R.J. THOMAS
Dept. of Agriculture, The University, Newcastle upon Tyne, NE1 7RU (Gt. Britain)
ABSTRACT Thomas, R.J., 1982. The ecological basis of parasite control: nematodes. Vet. Parasitol., 11: 9--24. In veterinary parasitology the major ecological interest is in production ecology, which concentrates on those aspects of the interaction of host, parasite and environment which determine the size of the host's parasite population and thus the risk to the production process. Control aims at reducing this population by breaking the life cycle in two ways: (a) at the host level -- by anthelmintic treatment to eliminate the parasite and perhaps more importantly to remove the source of environmental contamination (b) at the environmental level -- by segregating susceptible hosts from the infective stage of the parasite. The application of control measures requires an understanding of the parasite population pattern in the host and in the environment, and of the factors influencing the population. If these factors can be separated out and quantified by the use of systems analysis then the host--parasite system can be analysed and modelled. Such a model could be used in simulation studies on control strategies, and to indicate productive lines of research. The adult parasite population in the host and egg production are largely controlled by immunological factors, in particular the peri-parturient rise in egg output, and these physiological factors are difficult to quantify. However, the development and transmission of the external larval population can be extensively subdivided and studied experimentally, and utilisable data is becoming increasingly available for modelling purposes. The key factors governing the infective population are temperature and moisture and these have been used to develop models of the population pattern in the external environment. More sophisticated models have been constructed to predict population size as well as pattern and this approach is likely to dominate future ecological studies. INTRODUCTION
Ecology (from the Greek word for a house) has been defined as the study of populations in relation to one another and to their environment, and the ecological basis of parasite control is therefore a very broad subject. In fact we run the risk pointed out by Watt (1971) that " I f we do n o t develop a strong theoretical core that will bring all parts of ecology back together we shall all be washed out to sea in an immense tide of unrelated information". The aim of this paper is to suggest that the answer to this problem is the application of systems analysis t o parasite ecology and in particular to production ecology, i.e., those aspects of the interaction of host, parasite and environment
0304-4017/82/0000--0000/$02.75 © 1982 Elsevier Scientific Publishing Company
10 which influence the production processes. There is a good deal of evidence that the effect on production is generally proportional to the size of the worm burden and our chief interest must therefore be in an analysis of those ecological factors which determine the size of the parasite population in relation to the nematodes of major importance in cattle, sheep and pigs. For a general review of the epidemiology and control of helminths of livestock, reference should be made to the excellent series of papers at the last W.A.A.V.P. Meeting (Armour, 1980; Morley and Donald, 1980; Brunsdon, 1980).
Internal environment determines:
(a) adult population (b) adult fecundity
egg output -+ contamination rate
External environment determines:
(a) larvaepopulation x (b) larval transmission ~
larval input --* infection rate
Fig. 1. Population increase. Most of these nematodes have a direct life cycle and the parasite population naturally falls into two divisions, the population in the host and the population in the external environment, responsible, respectively, for the contamination rate and infection rate which together determine population size (Fig. 1). The host/parasite system is a dynamic set of inputs and outputs and disease results from an imbalance of these, thus an analysis of the factors influencing input an( o u t p u t should form the basis of rational control programmes. More importantly it offers the possibility of mathematical modelling of the system, which can be used both to improve our understanding of the system itself, and to formulate and test alternative control strategies (Gettinby, 1974). THE PARASITE POPULATION IN THE HOST The ecological importance of the host is as the source of environmental contamination, and the relevant factors are those influencing the size, persistence and fecundity of the adult parasite population. These are largely physiological factors concerned with the suitability of the host as a parasite environment, and can be subvided into those controlling the population itself and those controlling egg output.
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Population size The size of the adult population depends on the successful invasion by the infective stage, its development to the adult, and the subsequent longevity of the adult stage (Fig. 2).
Determined by:
(a) larval establishment/development (b) adult survival environmental 1. 2.
~
influences
L 3 age/physiology Host species/nutrition/immunity
Fig. 2. Adult population.
Parasite establishment Nematode parasites show a relatively high degree of host specificity, and this is of particular importance in sheep and cattle where the relative specificity of the two dominant parasites Ostertagia ostertagi and O. circumcincta has been the basis of alternate grazing systems for parasite control (Southcott and Barger, 1975). However, it has been suggested that adaptation of O.ostertagi to sheep may occur as a result of this practice (Bisset, 1980). Another possible problem is the emergence of other species as important pathogens, such as O. crimensis in sheep (Bisset, 1980), and O. leptospicularis in cattle (El Saqir et al., 1981). Thus changes in specificity will influence parasite establishment and need to be carefully monitored (Borgesteede, 1981).
Parasite development Development from infective stage to adult is generally rapid and uniform, except where interrupted by inhibition at the early fourth stage (Michel,1974), attributed generally to physiological factors in the infective larva under the influence of external environmental conditions, similar to those operating in diapause in insects (Armour and Bruce, 1974). However, under experimental conditions the percentage "take" of ingested larvae is relatively low -- less than 50% even in fully susceptible animals, and is density dependent, declining as the infective dose is increased, and the same is probably true in field infection. This innate loss is probably due to normal physiological factors such as variatior in the rate of passage of material through the gut, or failure to exsheath
12 TABLE I
Nematodirus spp. field infection: post mortem worm counts Slaughter date
Lambs
Yearlings
Adults
Larvae
Adults
Larvae
April 27
246 661
287 709
0 0
5 40
May 11
1838 5533
42 271
0 0
290 1100
May 25
5736 5066
1074 96
1 0
190 0
(Dakkak et al., 1981). B e y o n d this is the controlling influence of the immune reaction of the host to repeated infection. Immunity tends to limit the size of the adult population by eliminating developing stages (Urquhart et al., 1962), and by reducing the survival of adults in the presence of continuous infection so that a constant turnover of the population occurs (Michel, 1963; Waller and Thomas, 1978). The effect of immunity on population build-up is shown in Table I which compares immune yearling sheep and susceptible lambs exposed to the same field challenge. The role of nutrition in influencing the size of the worm burden is less clear. There is general agreement that poor nutrition is associated with high infection levels, b u t whether this is a direct physiological effect or indirect through interference with the host immune response has n o t been adequately investigated (Whitlock, 1949; Symons and Steel, 1978).
Parasite fecundity (Fig. 3) The parasite species determines the individual rate of egg production, varying from 1:1 for Haemonchus contortus to 18:1 for Nematodirus spp. (Kates, 1947). This, together with the population size and persistence will give a figure for potential egg output, and since the latter t w o are controlled by immunity then immunity must play a major role in moderating egg output. Nutrition, and particularly changes in diet, m a y have an effect (Brunsdon, 1964; Herbert et al. 1969), b u t probably the most important source of variation is that associated with the reproductive cycle, namely the peri-parturient rise in egg output. This appears to be specifically related to lactation (Connan, 1968; O'Sullivan and Donald, 1970), and with the level of circulating prolactin, and may, therefore, be hormonal in origin although it is usually attributed to relaxation of resistance (Anderson et al., 1978). The rise is particularly characteristic of nematode infections in sheep (Crofton, 1958) and pigs
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Determined by: (a) parasite species (b) adult numbers (c) adult persistence environmental I. 2.
~
influences
Host immunity Host physiology/reproductive state
Fig. 3. Adult fecundity.
(Thomas and Smith, 1968), but is extremely variable. This is probably due to its complex origin, a combination of increased larval establishment, increased maturation of inhibited larvae and increased egg production of existing adults, each of which may vary in importance in different situations. Thus, although a great deal is known about the peri-parturient rise it remains extremely difficult to quantify. CAN WE MODEL THE POPULATION IN THE HOST AND THE RESULTING CONTAMINATION RATE?
Bradley (1972) considers the host factors influencing the parasite population to be density dependent, tending to stabilise the host--parasite system, and Shad (1977) considers developmental arrest to be part of this regulatory function. It is their failure to operate which allows the population to increase, thus increasing the disease risk and the contamination rate. Unfortunately, host factors are complex interacting physiological phenomena, of which immunity is undoubtedly the most important, and these cannot be broken down into simple units, and therefore are very difficult to quantify. Nevertheless, several attempts have been made to model the worm population and with some success, although the parameters used have been relatively simple. Ractliffe et al. (1969) described a model of the sheep/H, c o n t o r t u s interaction based on the development time and death rate of the larval stages and adults, the reproductive rate, and a relationship between egg production and erythrocyte loss. Using this model the effects of variation in the major parameters influencing the haematocrit could be studied and their relative importance assessed. More recently Gettinby et al. (1979) have produced a prediction model for bovine ostertagiasis in calves which incorporates the parasite populations in the host and on pasture and this will be referred to later. Systems analysis and mathematical modelling looks to be a feasible technique in the non-immune, non-reproductive young animal, and fortunately this is
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the age group most at risk from helminth disease. Model development would enable us to evaluate alternative strategies for contamination control, and to predict the rate of increase of populations to disease outbreak level and the timing of preventive treatment. In situations where immunity and/or the reproductive cycle are operative, modelling is much more complex and a great deal of quantitative information is required before it can be usefully attempted. The between-breed and withinbreed differences in immunity which have been extensively reported in sheep and cattle (Armour, 1980), and the variation in response to vaccination demonstrated in lambs by Dineen et al. (1978) are attracting increasing interest, and selective breeding for resistance is suggested to be a feasible proposition in Australia (Le Jambre, 1978). Modelling techniques could prove useful in planning selective breeding programmes. THE PARASITE POPULATION IN THE EXTERNAL ENVIRONMENT
A major part of the life cycle of one-host parasites is passed in the external environment, and this is the source of larval input into the host. The external environment itself may vary from arctic to tropic, and from irrigated pasture to concrete, while the production and transmission of the infective stage also involves a series of events with different environmental requirements (Figs. 4 and 5), so that the process from contamination to host re-infection involves a complex of interacting and highly variable factors. In contrast to the host factors, Bradley (1972) states that the environmental or extrinsic transmission factors are density-independent and tend to destabilise the host--parasite system. They therefore have a positive effect on the parasite population outside the host and are a major influence on the disease risk. Fortunately, despite their complexity these factors can be extensively subdivided and reduced to relatively simple c o m p o n e n t s which can be quantified with varying degrees of accuracy.
I.
Egg survival
2.
Egg development
3.
Survival of embryonated eggs
4.
Hatching
5.
Larval development to infective stage
6.
Infective stage survival
7.
Larval migration
8.
Infection
Fig. 4. Stages in larval production/transmission.
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1. Climate - long term and seasonal effects 2. Weather - short term fluctuations: (a) Temperature/rainfall (b) Humidity, wind, sunlight, cloud etc
3. Physical conditions Herbage - type, length Soil structure Soil organisms
Fig. 5. Factors affecting larval production/migration.
The process from egg o u t p u t to larval input can be divided into two main areas, larval development and larval transmission. The factors influencing development are likely to be basically the same whether the infective stage is free-living or remains within the egg, but transmission factors are likely to be rather different for these two situations. The larval population
The larval population results from a series of stages between egg and infective larva, classed by Andersen et al. (1970) as egg survival, development and hatching, larval development and larval survival, the population size depending on the overall balance between production rate and mortality rate. Each stage tends to have its own specific requirements, e.g., the undeveloped egg is more susceptible to desiccation than the e m b r y o n a t e d egg (Waller and Donald, 1970), and the pre-infective larvae more susceptible than the infective form (Andersen et al., 1966). However, these increased susceptibilities may be offset by the fact that undeveloped eggs are largely f o u n d in freshly dropped faeces with a high moisture content, and preinfective stages tend to develop in faeces under the influence of rainfall. The environmental distribution of eggs and larvae is therefore of critical importance, for example in pasture between faeces, herbage and soil, and the importance of soil as a larval reservoir is n o w recognised (Persson, 1974; Duncan, 1979; Armour et •al., 1980). An expected complication is the variation in requirements between species, but less expected is the within-species variation reported for phenotypes of H. contortus by Le Jambre and Whitlock (1973), which enables a larval population to have a relatively wide range of temperature tolerance, and this requires further investigation.
16 Larval transmission
The extent to which free-living larvae migrate actively as opposed to passive dissemination is uncertain, while for infective eggs only the latter effect is operative. Probably larval m o v e m e n t is responsible for :migration out of faeces onto herbage in the immediate vicinity of the deposition site and results in high numbers being found close to the faeces (J~brgensen, 1980). Other agencies, such as earthworms, insects and farm animal activity are probably responsible for the wider distribution of larvae. Michel (1969) suggested that vertical migration was of little significance, but if soil is to be considered an important reservoir, then vertical migration becomes an essential part of the transmission process (Fincher and Stewart, 1979). We really k n o w very little a b o u t the behaviour of parasitic nematode larvae (Croll, 1972) despite the importance of directional m o v e m e n t in increasing host--parasite contact. Host behaviour, and the influence of management on behaviour, might be expected to have a marked impact on the uptake of infection, and there is evidence to suggest that the acquisition of larvae by grazing animals is lower than would be anticipated from random herbage sampling (Waller et al., 1981). Selective grazing and the avoidance of contaminated herbage m a y be partly responsible for the differences in worm burden at different stocking rates, particularly of those species with resistant infective larvae (Morley and Donald, 1980). This is perhaps more likely to be important in cattle grazing where the faecal pat m a y persist for a long time than in sheep grazing where faecal breakdown is more rapid. Rooting behaviour in pigs influences the uptake of Ascaris eggs, and this behaviour is itself modified by feed availability. PARASITE POPULATION PATTERNS Given the complexity of the interaction of parasite species, stage and environment involved in the process from contamination to larval uptake, the possibility of discerning general patterns of larval population and host infection would seem to be remote. However, there is a tendency towards stability in any host--parasite system (Odum, 1971), and in recent years it has been shown that such general patterns do occur under natural conditions in a range of environments and for a variety of parasites and hosts: sheep (Thomas and Boag, 1972; Donald and Waller, 1973), cattle (Armour, 1970) and pigs {Rose and Small, 1980). The c o m m o n e s t pattern is one of increased contamination rate in spring resulting in maximum larval availability in mid-summer to autumn, and peak late s u m m e r / a u t u m n host infection levels (Fig. 6). While this pattern is most apparent for those parasites with free-living infective larvae, there is some evidence for it where infection occurs via an infective egg (Stevenson, 1979). The most likely explanation for this tendency towards a general pattern of population fluctuation is the dominance of environmental temperature and moisture in determining the development, survival and transmission of the
17 I
2500
2000
........ Ewe egg o u t p u t ---
Lamb egg o u t p u t
--
P a s t u r e larval le
,I000
i" I I I
BOO
15oo
600 CD
61000
4o0~-
oh Ld
8 500
20O
.........r £ - - ' ; ' J ' : T : : Ape
May
dun
..... July
, v Aug
2-Sept
Fig. 6. Epidemiologieal pattern: sheep nematodes.
larval population (Levine, 1963). In its simplest form their effect may be explained on the basis that moisture is essential for development to occur, while in the presence of adequate moisture, temperature will determine the rate of development. Thus these two factors may be considered to determine the basic cycle c f parasite populations, and all other factors to influence the within-pattern variations in timing and the size of the peaks and troughs of numbers. This encourages the optimistic view that it should be possible to model the major patterns of population based on these t w o dominant factors, b u t with the pessimistic caution that the multitudinous subsidiary factors may be largely responsible within the overall pattern in determining the points at which the parasite population becomes a production problem. THE CONSTRUCTION OF POPULATION MODELS
We are faced with two possible choices in model building. One is the simple approach of modelling the parasite pattern based on these two factors of temperature and moisture. The other is a more complicated attempt to incorporate as many variables as possible in a sophisticated model which will n o t only indicate population pattern, b u t also population size and therefore the potential disease risk at any particular point in time.
Modelling the parasite pattern Given that the egg and larval habitat is soil and vegetation, meteorological data obviously do n o t measure the temperature and moisture conditions in the micro-habitat. However, equally obviously there is b o u n d to be a relationship between the two, and if the effect of atmospheric temperature and rainfall on the micro-habitat is reasonably direct, then these two parameters, which are widely recorded in routine meteorological work and in a very standard form, can be substituted for the much more difficult micro-climatic measurements. Instead of attempting to correlate macro- and micro-climate data the aim is
18 TABLE II Relationship of climate to ruminant nematodes* Climate
Typical locality
Dominant trichostrongylid
A
Tropical: rain, hot all year
Haemonchus
B
Dry steppe: (> 18°C) (< 18°C) Temperate: -3 ° C to 18° C moist all year, hot summer moist all year, warm summer Cold: below -3 ° C to above 10°C Polar: below 10°C
Equatorial Africa/ America Texas Idaho
C
D E
Haemonchus Ostertagia
Washington DC England, Germany Canada
Haemonchus Ostertagia
Arctic
None
Trichostrongylus
*From Levine, 1978 to correlate the macro-climate data with larval popul at i on measurements in an empirical way. A table (Table II) taken f r om Levine (1978) indicates the relationship between climate and r u m i n a n t n e m a t o d e s which determines their geographical distribution, and this t y p e of correlation led G o r d o n (1948) to devise bioclimatographs to explain n o t only species distribution, b u t also seasonal disease risk u n d er the apt slogan " w o r m s work by the weather". Levine and Andersen (1973) a t t e m p t e d a r e f i n e m e n t of the correlation based on relative transmission potential to express the availability of infection. In a slightly different approach Ollerenshaw and Rowlands (1959) correlated weather patterns with liver fluke disease incidence to devise the fluke forecasting system which is widely used in c ont r ol programmes, and Ollerenshaw and Smith (1969) suggested a similar m e t h o d of forecasting the incidence of ostertagiasis in cattle, and in sheep (Ollerer~shaw et al., 1978). These correlations t end only to per m i t general conclusions to be drawn, but the very specific influence of t e m p e r a t u r e on the hatching of N e m a t o d i r u s battus in Britain made it possible to derive a correlation between soil temperature and the appearance of a wave of infective larvae on pasture which was sufficiently precise to be used in forecasting the timing as well as the severity of disease outbreaks (Smith and Thomas, 1972). Since the pattern of seasonal larval availability for r u m i n a n t nem a t ode s is relatively constant in temperate conditions a similar correlation of weather conditions and peak larval activity has been a t t e m p t e d in Britain (Thomas, 1974; T hom as and Starr, 1978) and New Zealand (Vlassof, 1975), largely to encourage the practical application of integrated c o n t r o l programmes based on pasture m anagem ent and strategic anthelmintic t r e a t m e n t . In b o t h cases the correlation is between larval activity and rainfall rather than t e m p e r a t u r e , since while t e m p e r a t u r e contributes to
19
the basic larval pattern, moisture availability determines the balance between m e rate of development on the one hand, and the rate of drying which inhibits development and therefore is the more critical factor affecting the within-season timing of the larval peak. In a refinement of this approach Starr and Thomas (1980) have incorporated the temperature effect as well as moisture. The moisture status of the surface layer of pasture is calculated from rainfall and potential evapo-transpiration to give the time periods during which development can proceed. The daily larval development rate during these periods is then assumed to be proportional to the accumulation of daydegrees above a threshold temperature for larval development, i.e., the number of "heat units" available for development. The cumulative figures obtained for day-degrees from meteorological data have been compared with actual pasture larval counts over a ten-year period in North East England to identify the total day-degrees corresponding best to peak larval count, and for this particular area a day-degree c o u n t of 130 shows the best fit (Fig. 7). This process of summation of time and temperature above a minimum development threshold has been similarly used by Jones {1975) for plant parasitic nematode studies. Ostertagiasis 1978 actual/predicted
16 Accumulated degree days
o , , * e D e g r e e days
14
Wetness units P a s t u r e larval count
O
× 12
.eol
iS:i
c"
~
i [!!!i~ lo0-.4 .3 o
6 ?
o
50 "2 '~
~ 4
z0 2 I
April
IX4ay
June
July
|
August
September
Fig. 7. Ostertagiasis, 1978. Actual/predicted. F r o m Reviews in Agricultural Meteorology No. 1 (unpublished), copies from the Library, Meteorological Office, Bracknell.
This approach makes possible quite precise modelling of t h e parasite pop~lation pattern and its within-season variations, which has useful predictive value while obviating the need for detailed information on the ecology of eggs and larval stages. However, it is still largely qualitative, and while useful in
20 predicting periods of risk it will not provide any estimate of population size, and consequently of the likelihood and severity of disease outbreaks, except in the most general way.
Modelling the parasite population To model the size of the parasite population at any stage in the seasonal pattern requires precise and extensive ecological data, which has hitherto not been available, and it is to the credit of many parasitologists that the necessary information is steadily accumulating and increasingly in a form which is suitable for model building. Much of the early data was reviewed by Crofton {1963) and tended to concentrate on larval development and survival under experimental conditions. A significant contribution was made by Silverman and Campbell (1959) who clarified the influence of the faeces on the development of H. contortus larvae and drew attention to the fallacy of applying laboratory development rates to the field situation. More recent studies have tended to combine laboratory and field experiments, often in conjunction with field observations on the naturally occurring population patterns they are designed to explain. Many such studies have been carried out on the c o m m o n ruminant nematodes (see Michel, 1969, 1976), and to a small extent on the strongylid nematodes of pigs (Rose and Small, 1980). In contrast to the extensive literature on the ecology of nematodes with a free living infective stage, there is a marked lack of data on those species with an infective egg, such as the trichurids and ascarids, particularly in pigs. Such evidence as there is suggests that again temperature is a key factor in develo p m e n t (Burden and Hammet, 1979; Stevenson, 1979). However, the resistance of the infective egg to environmental conditions and the fact that host infection is purely passive, means that the epidemiology of infection is largely host-dependent, and control has no real ecological basis at present. A mathematical approach to the interpretation of field experimental data was initiated by Tallis and Donald (1964, 1970), studying the distribution of larvae on pasture. Levine and Andersen {1973) and Callinan (1977) have developed the use of relative translation potentials to predict pasture populations in relation to air and herbage humidity and soil temperature. Young et al. {1980a) in a very useful study, have shown that the hatching of eggs of O. circumcincta under alternating temperature conditions could be satisfactorily predicted from constant temperature experiments, thus very considerably easing the problems of data collection. In further work on O. ostertagi the same authors (Young et al., 1980b) were able to model larval development rate and death rate in dung pats as well as under controlled conditions. As might be expected they demonstrated a time lag in development due to environmental effects within the dung pat which will require further assessment. Parallel with these specific studies t w o more general models have been
21
attempted based on relatively limited data. Barger et al. (1972) constructed a model to simulate pasture larval populations of H. contortus in New South Wales. Meteorological data, herbage availability and sheep egg output were recorded, and a number of assumptions made to estimate development and survival from egg to infective larva. The predicted larval concentrations on pasture over a two-year period were compared with field observations and good agreement obtained. The model confirmed the critical role of moisture under favourable temperature conditions, and the authors considered it to be a useful tool in studying the effect of management factors on haemonchosis. More recently, Gettinby et al. (1979) have reported what appears to be the only model so far which predicts parasite populations both on pasture and in the host. Their prediction model for bovine ostertagiasis estimates larval development as previously described in terms of time and temperature above a development minimum, and incorporates a relatively low mortality rate, which perhaps assumes a quite rapid rate of ingestion by the host. Migration is determined by rainfall, and uptake based on herbage consumption. As pointed out earlier, the most difficult influence to estimate is that of immunity but this is avoided by considering only calves in their first grazing season, the group most susceptible to parasitism. Again good agreement was obtained between predicted and observed results for both parasite populations and for the occurrence of clinical disease, and it is suggested that such a model would be a valuable aid to the timing of within-season grazing management and treatment programmes. The success of these relatively simple models suggests that as more data become available, and therefore more variables can be accommodated with increasing accuracy, population modelling will become more precise and adaptable to a wider range of management and environmental situations. Morley and Donald (1980) point to the small extent to which control procedures have been tested in realistic production systems, and to the cost and difficulty of doing this. Developments in modelling the host/parasite/environment complex could help to solve these problems, but further progress will require more involvement of mathematicians in parasite ecology, for as stated by Patten (1971), the descriptive phase of ecology is being succeeded by the much more rigorous phase of systems ecology. Perhaps an appropriate closing quotation would be from Bawden (1978) -- "The emerging re-orientation of agricultural research associated with the development and application of systems ecology to production problems, and the appeals for higher order inter-disciplinary investigations implicit in protection ecology, provide the impetus to develop a perspective for parasite management". -- it probably sums up the purpose of this paper, and it is such a beautiful phrase! REFERENCES
Andersen, F.L., Wang, G.T. and Levine, N.D., 1 9 6 6 . E f f e c t o f temperature on survival o f the free-living stages o f Trichostrongylus colu briformis. J. Parasitol., 54 : 1 1 7 - - 1 2 8 .
22 Andersen, F.L., Levine, N.D. and Boatman, P.A., 1970. Survival of third-stage Trichos t r o n g y l u s c o l u b r i f o r m i s larvae on pasture. J. Parasitol., 56: 209--232. Anderson, N., Dash, K.M., Donald, A.D., Southcott, W.H. and Waller, P.J., 1978. Epidemiology and control of gastro-intestinal parasites of sheep in Australia. A.D. Donald, W.H. Southcott and J.K. Dineen (Editors). C.S.I.R.O., Melbourne, Australia, pp. 24--52. Armour, J., 1970. Bovine ostertagiasis: a review. Vet. Rec., 86: 184--190. Armour, J., 1980. The epidemiology of helminth disease in farm animals. Vet. Parasitol., 6: 7--46. Armour, J. and Bruce, R.C., 1974. The inhibition of development of Ostertagia ostertagi - a diapause p h e n o m e n o n in a nematode. Parasitology, 69: 161--174. Armour, J., Saqir, I.M., Bairden, K., Duncan, J.L. and Urquhart, G.M., 1980. Parasitic bronchitis and ostertagiasis on aftermath grazing. Vet. Rec., 106: 184--185. Barger, I.A., Benyon, P.R. and Southcott, W.H., 1972. Simulation of pasture larval populations of H a e m o n c h u s c o n t o r t u s . Proc. Aust. Soc. Anim. Prod., 9: 38--42. Bawden, J.R., 1978. A perspective for parasite management. Agric., Environ., 4: 43--55. Bisset, S.A., 1980. Goats and sheep as hosts for some common cattle trichostrongylids. Vet. Parasitol., 7 : 363--368. Borgesteede, F.H.M., 1981. Experimental cross-infections with gastro-intestinal nematodes of sheep and cattle. Z. Parasitenkd., 65: 1--10. Bradley, D.J., 1972. Regulation of parasite populations. Trans. R. Soc. Trop. Med. Hyg., 66: 697--708. Brunsdon, R.V., 1964. The effect on the persistence and pattern of nematode infection of the transfer of naturally infected sheep from pasture to pens. N.Z. Vet. J., 12: 105-107. Brunsdon, R.V., 1980. Principles of helminth control. Vet. Parasitol., 6: 185--216. Burden, D.J. and Hammet, N.C., 1979. The development and survival of Trichuris suis ova on pasture plots in the south of England. Res. Vet. Sci., 26: 66--70. Callinan, A.P.L., 1977. The translation potential of sheep nematodes in Western Victoria. Proc. 8th Int. Conf. W.A.A.V.P., Sydney, Australia, Abstr. 83. Connan, R.M., 1968. Studies on the worm populations in the alimentary tract of breeding ewes. J. Helminthol., 42: 9--28. Crofton, H.D., 1958. Nematode parasite population in sheep on lowland farms. V. Further observations on the post-parturient rise and a discussion of its significance. Parasitology, 48: 251--260. Crofton, H.D., 1963. Nematode parasite populations in sheep and on pasture. Tech. Commun. 35. Commonwealth Agric. Bureau, Farnham Royal, England, 101 pp. Croll, N.A., 1972. Behaviour of larval nematodes. Behavioural aspects of parasite transmission. E.U. Canning and C.A. Wright (Editors). Academic Press, London. Dakkak, A., Fioramonti, J. and Bueno, L., 1981. H a e m o n c h u s c o n t o r t u s third stage larvae in sheep: kinetics of arrival into the abomasum and transformation during rumeno-omasal transit. Res. Vet. Sci., 31: 384. Dineen, J.K., Gregg, P. and Lascelles, A.K., 1978. The response of lambs to vaccination at weaning with irradiated T r i c h o s t r o n g y l u s c o l u b r i f o r m i s larvae: segregation into 'responders' and 'non-responders'. Int. J. Parasitol., 8: 59--64. Donald, A.D. and Waller, P.J., 1973. Gastrointestinal 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. Duncan, J.L., 1979. Studies on the epidemiology of bovine parasitic bronchitis. Vet. Rec., 104: 274--278. E1 Saqir, I., Armour, J., Bairden, K., Dunn, A.M., Jennings, F.W. and Murray, M., 1982. Observations on the infectivity and pathogenicity of three isolates of Ostertagia spp. sens. lat in calves. Res. Vet. Sci., 32: 106--112. Fincher, G.T. and Stewart, T.B., 1979. Vertical migration by nematode larvae of cattle parasites through soil. Proc. Helminthol., Soc. Wash., 46: 43--46.
23 Gettinby, G., 1974. Assessment of the effectiveness of control techniques for liver fluke infections. In: M.B. Usher and M.M. Williamson (Editors), Ecological Stability, Chapman and Hall, London, pp. 89--97. Gettinby, G., Bairden, K., Armour, J. and Benitez-Usher, C., 1979. A prediction model for bovine ostertagiasis. Vet. Rec., 105: 57--59. Gordon, H. McL., 1948. The epidemiology of parasitic diseases, with special reference to studies with nematode parasites of sheep. Aust. Vet. J., 24: 17--45. Herbert, I.V., Lean, I.J. and Nickson, E.W., 1969. Dietary factors and the production of Oesophagostomum ova in breeding pigs. Vet. Rec., 84: 441--444. Jones, F.G.W., 1975. Accumulated temperature and rainfall as measures of nematode development and activity. Nematologia, 21 : 62--70. Jorgensen, R.J., 1980. Epidemiology of bovine dictyocaulosis in Denmark. Vet. Parasitol., 7: 153--167. Kates, K.C., 1947. Diagnosis of gastro-intestinal nematode parasitism of sheep by differential egg counts. Proc. Helminthol. Soc. Wash., 14: 44--53. LeJambre, L.F., 1978. The epidemiology and control of gastro-intestinal parasites of sheep in Australia. A.D. Donald, W.H. Southcott and J.K. Dineen (Editors). C.S.I.R.O., Melbourne, Australia, pp. 137--141. LeJambre, L.F. and Whitlock, J.H., 1973. Optimum temperature for egg development of phenotypes in Haemonchus contortus. Int. J. Parasitol., 3: 299--310. Levine, N.D., 1963. Weather climate and the bionomics of ruminant nematode larvae. Adv. Vet. Sci., 8: 215--261. Levine, N.D., 1978. The influence of weather on the bionomics of the free-living stages of nematodes. In: T.E. Gibson (Editor), Weather and Parasitic Animal Diseases. Tech. Note No. 159, World Met. Org. Geneva, Switzerland, pp. 51--57. Levine, N.D. and Andersen, F.L., 1973. Development and survival of Trichostrongylus colubriformis on pasture. J. Parasitol., 59: 147--165. Michel, J.F., 1963. T h e ' p h e n o m e n o n of host resistance and the course of infection of Ostertagia ostertag£ Parasitology, 53: 63--84. Michel, J.F., 1969. The epidemiology and control of some nematode infections of grazing animals. Adv. Parasitol., 7: 211--272. Michel, J.F., 1974. Arrested development of nematodes and some related phenomena Adv. Parasitol., 13 : 279--366. Michel, J.F., 1976. The epidemiology and control of some nematode infections in grazing animals. Adv. Parasitol., 14: 355--397. Morley, F.H.W. and Donald, A.D., 1980. Farm management and systems of helminth control. Vet. Parasitol., 6: 105--134. Odum, E.P., 1971. Fundamentals of Ecology. W.B. Saunders, Philadelphia, PA, 574 pp. 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., 1969. Meteorological factors and forecasts of helminthic disease. Adv. Parasitol., 7: 283--323. Ollerenshaw, C.B., Graham, E.G. and Smith, L.P., 1978. Forecasting the incidence of parasitic gastro-enteritis in lambs in England and Wales. Vet. Rec., 103: 461--465. O'Sullivan, B.M. and Donald, A.D., 1970. A field study of nematode parasite populations in lactating ewes. Parasitology, 61 : 301--315. Patten, B.C., 1971. Systems Analysis and Simulation in Ecology. Academic Press, London, 607 pp. Persson, L., 1974. Studies on the bionomics of eggs and infective larvae of Ostertagia ostertagi and Cooperia oncophora in soil. Zentralbl. Veterinarmed. B, 21: 318--328. Ractliffe, L.H., Taylor, H.M., Whitlock, J.H. and Lynn, W.R., 1969. Systems analysis of a host~parasite interaction. Parasitology, 59: 649--661. Rose, J.H. and Small, A.J., 1980. Observations on the development and survival of freeliving stages of Oesophagostomum dentatum both in their natural environments out-ofdoors and under controlled conditions in the laboratory. Parasitology, 81: 507--517.
24 Shad, G.A., 1977. The role of arrested development in the regulation of nematode populations. In: G.W. Esch (Editor), Regulation of Parasite Populations. Academic Press, New York, 111 pp. Silverman, P.H. and Campbell, J.A., 1959. Studies on parasitic worms of sheep in Scotland. Embryonic and larval development of Haemonchus contortus at constant temperatures. Parasitology, 39: 23--37. 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., 1975. Decontamination of sheep and cattle pastures by varying periods of grazing with the alternate host. Int. J. Parasitol., 5: 45--48. Start, J.R. and Thomas, R.J., 1980. Parasitic gastro-enteritis in lambs -- a model for estimating the timing of the larval emergence peak. Int. J. Biometeor., 24: 223--229. Stevenson, P., 1979. The influence of environmental temperature on the rate of development of Ascaris suum eggs in Great Britain. Res. Vet. Sci., 27 : 193--196. Symons, L.E.A. and Steel, J.W., 1978. The epidemiology and control of gastro-intestinal parasites of sheep in Australia. In: A.D. Donald, W.H. Southcott and J.K. Dineen (Editors). C.S.I.R.O., Melbourne, Australia, pp. 9--22. Tallis, G.M. and Donald, A.D., 1964. Models for the distribution on pasture of infective larvae of the gastro-intestinal nematode parasites of sheep. Aust. J. Biol. Sci., 17: 504-513. Tallis, G.M. and Donald, A.D., 1970. Further models for the distribution on pasture of infective larvae of the strongyloid nematode parasites of sheep Math. Biosci., 7 : 179--190. Thomas, R.J., 1974. The role of climate in the epidemiology of nematode parasitism in ruminants. In: A.E.R. Taylor and R. Muller (Editors), The Effects of Meteorological Factors upon Parasites. Symposia of the Brit. Soc. Parasitol., 12: 13--32. Thomas, R.J. and Boag, B., 1972. Epidemiological studies on gastro-intestinal nematodes of sheep. Infection patterns on clean and summer-contaminated pastures. Res. Vet. Sci., 13: 61--69. Thomas, R.J. and Smith, W.C., 1968. Anthelmintic treatment of sows with thiabendazole. Vet. Rec., 83: 489--491. Thomas, R.J. and Starr, J.R., 1978. Forecasting the peak of gastro-intestinal nematode infection in lambs. Vet. Rec., 103: 465--468. Urquhart, G.M., Jarrett, W.F.M. and Mulligan, W., 1962. Helminth Immunity. Adv. Vet. Sci., 7: 87--129. Vlassof, A., 1975. The role of climate in the epidemiology of gastro-intestinal nematode parasites of sheep and cattle. Symposium on Meteorology and Food Production. N.Z. Meteorol. Service, Wellington, pp. 171--176. Waller, P.J. and Donald, A.D., 1970. The response to desiccation of eggs of Trichostrongylus colubriformis and Haemonchus contortus. Parasitology, 61 : 195--204. Waller, P.J. and Thomas, R.J., 1978. Nematode parasitism in sheep in North-East England: the epidemiology of Ostertagia species. Int. J. Parasitol., 8: 275--283. Waller, P.J., Dobson, R.J., Donald, A.D. and Thomas, R.J., 1981. Populations of strongyloid nematode infective stages in sheep pastures: comparison between direct pasture sampling and tracer lambs as estimators of larval abundance. Int. J. Parasitol., 11 : 359--368. Watt, K.E.F., 1971. Dynamics of populations: a synthesis. In: H. den Boer and H. Gradwell (Editors), Dynamics of Populations. Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands, pp. 568--580. Whitlock, J.H., 1949. The relationship of nutrition to the development of trichostrongylidoses. Cornell Vet., 39: 146--182. Young, R.R., Anderson, N., Overend, D. Tweedie, R.L., Malafant, K.W.J. and Preston, G.A.N., 1980a. The effect of temperature on times to hatching of eggs of the nematode Ostertagia circumcincta. Parasitology, 81: 477--491. Young, R.R., Nicholson, R.M., Tweedie, R.L. and Schuh, H.J., 1980b. Quantitative modelling and prediction of development times of the free-licing stages of Ostertagia ostertagi under controlled and field conditions. Parasitology, 81: 493--505.
9
THE ECOLOGICAL BASIS OF PARASITE CONTROL: NEMATODES
R.J. THOMAS
Dept. of Agriculture, The University, Newcastle upon Tyne, NE1 7RU (Gt. Britain)
ABSTRACT Thomas, R.J., 1982. The ecological basis of parasite control: nematodes. Vet. Parasitol., 11: 9--24. In veterinary parasitology the major ecological interest is in production ecology, which concentrates on those aspects of the interaction of host, parasite and environment which determine the size of the host's parasite population and thus the risk to the production process. Control aims at reducing this population by breaking the life cycle in two ways: (a) at the host level -- by anthelmintic treatment to eliminate the parasite and perhaps more importantly to remove the source of environmental contamination (b) at the environmental level -- by segregating susceptible hosts from the infective stage of the parasite. The application of control measures requires an understanding of the parasite population pattern in the host and in the environment, and of the factors influencing the population. If these factors can be separated out and quantified by the use of systems analysis then the host--parasite system can be analysed and modelled. Such a model could be used in simulation studies on control strategies, and to indicate productive lines of research. The adult parasite population in the host and egg production are largely controlled by immunological factors, in particular the peri-parturient rise in egg output, and these physiological factors are difficult to quantify. However, the development and transmission of the external larval population can be extensively subdivided and studied experimentally, and utilisable data is becoming increasingly available for modelling purposes. The key factors governing the infective population are temperature and moisture and these have been used to develop models of the population pattern in the external environment. More sophisticated models have been constructed to predict population size as well as pattern and this approach is likely to dominate future ecological studies. INTRODUCTION
Ecology (from the Greek word for a house) has been defined as the study of populations in relation to one another and to their environment, and the ecological basis of parasite control is therefore a very broad subject. In fact we run the risk pointed out by Watt (1971) that " I f we do n o t develop a strong theoretical core that will bring all parts of ecology back together we shall all be washed out to sea in an immense tide of unrelated information". The aim of this paper is to suggest that the answer to this problem is the application of systems analysis t o parasite ecology and in particular to production ecology, i.e., those aspects of the interaction of host, parasite and environment
0304-4017/82/0000--0000/$02.75 © 1982 Elsevier Scientific Publishing Company
10 which influence the production processes. There is a good deal of evidence that the effect on production is generally proportional to the size of the worm burden and our chief interest must therefore be in an analysis of those ecological factors which determine the size of the parasite population in relation to the nematodes of major importance in cattle, sheep and pigs. For a general review of the epidemiology and control of helminths of livestock, reference should be made to the excellent series of papers at the last W.A.A.V.P. Meeting (Armour, 1980; Morley and Donald, 1980; Brunsdon, 1980).
Internal environment determines:
(a) adult population (b) adult fecundity
egg output -+ contamination rate
External environment determines:
(a) larvaepopulation x (b) larval transmission ~
larval input --* infection rate
Fig. 1. Population increase. Most of these nematodes have a direct life cycle and the parasite population naturally falls into two divisions, the population in the host and the population in the external environment, responsible, respectively, for the contamination rate and infection rate which together determine population size (Fig. 1). The host/parasite system is a dynamic set of inputs and outputs and disease results from an imbalance of these, thus an analysis of the factors influencing input an( o u t p u t should form the basis of rational control programmes. More importantly it offers the possibility of mathematical modelling of the system, which can be used both to improve our understanding of the system itself, and to formulate and test alternative control strategies (Gettinby, 1974). THE PARASITE POPULATION IN THE HOST The ecological importance of the host is as the source of environmental contamination, and the relevant factors are those influencing the size, persistence and fecundity of the adult parasite population. These are largely physiological factors concerned with the suitability of the host as a parasite environment, and can be subvided into those controlling the population itself and those controlling egg output.
11
Population size The size of the adult population depends on the successful invasion by the infective stage, its development to the adult, and the subsequent longevity of the adult stage (Fig. 2).
Determined by:
(a) larval establishment/development (b) adult survival environmental 1. 2.
~
influences
L 3 age/physiology Host species/nutrition/immunity
Fig. 2. Adult population.
Parasite establishment Nematode parasites show a relatively high degree of host specificity, and this is of particular importance in sheep and cattle where the relative specificity of the two dominant parasites Ostertagia ostertagi and O. circumcincta has been the basis of alternate grazing systems for parasite control (Southcott and Barger, 1975). However, it has been suggested that adaptation of O.ostertagi to sheep may occur as a result of this practice (Bisset, 1980). Another possible problem is the emergence of other species as important pathogens, such as O. crimensis in sheep (Bisset, 1980), and O. leptospicularis in cattle (El Saqir et al., 1981). Thus changes in specificity will influence parasite establishment and need to be carefully monitored (Borgesteede, 1981).
Parasite development Development from infective stage to adult is generally rapid and uniform, except where interrupted by inhibition at the early fourth stage (Michel,1974), attributed generally to physiological factors in the infective larva under the influence of external environmental conditions, similar to those operating in diapause in insects (Armour and Bruce, 1974). However, under experimental conditions the percentage "take" of ingested larvae is relatively low -- less than 50% even in fully susceptible animals, and is density dependent, declining as the infective dose is increased, and the same is probably true in field infection. This innate loss is probably due to normal physiological factors such as variatior in the rate of passage of material through the gut, or failure to exsheath
12 TABLE I
Nematodirus spp. field infection: post mortem worm counts Slaughter date
Lambs
Yearlings
Adults
Larvae
Adults
Larvae
April 27
246 661
287 709
0 0
5 40
May 11
1838 5533
42 271
0 0
290 1100
May 25
5736 5066
1074 96
1 0
190 0
(Dakkak et al., 1981). B e y o n d this is the controlling influence of the immune reaction of the host to repeated infection. Immunity tends to limit the size of the adult population by eliminating developing stages (Urquhart et al., 1962), and by reducing the survival of adults in the presence of continuous infection so that a constant turnover of the population occurs (Michel, 1963; Waller and Thomas, 1978). The effect of immunity on population build-up is shown in Table I which compares immune yearling sheep and susceptible lambs exposed to the same field challenge. The role of nutrition in influencing the size of the worm burden is less clear. There is general agreement that poor nutrition is associated with high infection levels, b u t whether this is a direct physiological effect or indirect through interference with the host immune response has n o t been adequately investigated (Whitlock, 1949; Symons and Steel, 1978).
Parasite fecundity (Fig. 3) The parasite species determines the individual rate of egg production, varying from 1:1 for Haemonchus contortus to 18:1 for Nematodirus spp. (Kates, 1947). This, together with the population size and persistence will give a figure for potential egg output, and since the latter t w o are controlled by immunity then immunity must play a major role in moderating egg output. Nutrition, and particularly changes in diet, m a y have an effect (Brunsdon, 1964; Herbert et al. 1969), b u t probably the most important source of variation is that associated with the reproductive cycle, namely the peri-parturient rise in egg output. This appears to be specifically related to lactation (Connan, 1968; O'Sullivan and Donald, 1970), and with the level of circulating prolactin, and may, therefore, be hormonal in origin although it is usually attributed to relaxation of resistance (Anderson et al., 1978). The rise is particularly characteristic of nematode infections in sheep (Crofton, 1958) and pigs
13
Determined by: (a) parasite species (b) adult numbers (c) adult persistence environmental I. 2.
~
influences
Host immunity Host physiology/reproductive state
Fig. 3. Adult fecundity.
(Thomas and Smith, 1968), but is extremely variable. This is probably due to its complex origin, a combination of increased larval establishment, increased maturation of inhibited larvae and increased egg production of existing adults, each of which may vary in importance in different situations. Thus, although a great deal is known about the peri-parturient rise it remains extremely difficult to quantify. CAN WE MODEL THE POPULATION IN THE HOST AND THE RESULTING CONTAMINATION RATE?
Bradley (1972) considers the host factors influencing the parasite population to be density dependent, tending to stabilise the host--parasite system, and Shad (1977) considers developmental arrest to be part of this regulatory function. It is their failure to operate which allows the population to increase, thus increasing the disease risk and the contamination rate. Unfortunately, host factors are complex interacting physiological phenomena, of which immunity is undoubtedly the most important, and these cannot be broken down into simple units, and therefore are very difficult to quantify. Nevertheless, several attempts have been made to model the worm population and with some success, although the parameters used have been relatively simple. Ractliffe et al. (1969) described a model of the sheep/H, c o n t o r t u s interaction based on the development time and death rate of the larval stages and adults, the reproductive rate, and a relationship between egg production and erythrocyte loss. Using this model the effects of variation in the major parameters influencing the haematocrit could be studied and their relative importance assessed. More recently Gettinby et al. (1979) have produced a prediction model for bovine ostertagiasis in calves which incorporates the parasite populations in the host and on pasture and this will be referred to later. Systems analysis and mathematical modelling looks to be a feasible technique in the non-immune, non-reproductive young animal, and fortunately this is
14
the age group most at risk from helminth disease. Model development would enable us to evaluate alternative strategies for contamination control, and to predict the rate of increase of populations to disease outbreak level and the timing of preventive treatment. In situations where immunity and/or the reproductive cycle are operative, modelling is much more complex and a great deal of quantitative information is required before it can be usefully attempted. The between-breed and withinbreed differences in immunity which have been extensively reported in sheep and cattle (Armour, 1980), and the variation in response to vaccination demonstrated in lambs by Dineen et al. (1978) are attracting increasing interest, and selective breeding for resistance is suggested to be a feasible proposition in Australia (Le Jambre, 1978). Modelling techniques could prove useful in planning selective breeding programmes. THE PARASITE POPULATION IN THE EXTERNAL ENVIRONMENT
A major part of the life cycle of one-host parasites is passed in the external environment, and this is the source of larval input into the host. The external environment itself may vary from arctic to tropic, and from irrigated pasture to concrete, while the production and transmission of the infective stage also involves a series of events with different environmental requirements (Figs. 4 and 5), so that the process from contamination to host re-infection involves a complex of interacting and highly variable factors. In contrast to the host factors, Bradley (1972) states that the environmental or extrinsic transmission factors are density-independent and tend to destabilise the host--parasite system. They therefore have a positive effect on the parasite population outside the host and are a major influence on the disease risk. Fortunately, despite their complexity these factors can be extensively subdivided and reduced to relatively simple c o m p o n e n t s which can be quantified with varying degrees of accuracy.
I.
Egg survival
2.
Egg development
3.
Survival of embryonated eggs
4.
Hatching
5.
Larval development to infective stage
6.
Infective stage survival
7.
Larval migration
8.
Infection
Fig. 4. Stages in larval production/transmission.
15
1. Climate - long term and seasonal effects 2. Weather - short term fluctuations: (a) Temperature/rainfall (b) Humidity, wind, sunlight, cloud etc
3. Physical conditions Herbage - type, length Soil structure Soil organisms
Fig. 5. Factors affecting larval production/migration.
The process from egg o u t p u t to larval input can be divided into two main areas, larval development and larval transmission. The factors influencing development are likely to be basically the same whether the infective stage is free-living or remains within the egg, but transmission factors are likely to be rather different for these two situations. The larval population
The larval population results from a series of stages between egg and infective larva, classed by Andersen et al. (1970) as egg survival, development and hatching, larval development and larval survival, the population size depending on the overall balance between production rate and mortality rate. Each stage tends to have its own specific requirements, e.g., the undeveloped egg is more susceptible to desiccation than the e m b r y o n a t e d egg (Waller and Donald, 1970), and the pre-infective larvae more susceptible than the infective form (Andersen et al., 1966). However, these increased susceptibilities may be offset by the fact that undeveloped eggs are largely f o u n d in freshly dropped faeces with a high moisture content, and preinfective stages tend to develop in faeces under the influence of rainfall. The environmental distribution of eggs and larvae is therefore of critical importance, for example in pasture between faeces, herbage and soil, and the importance of soil as a larval reservoir is n o w recognised (Persson, 1974; Duncan, 1979; Armour et •al., 1980). An expected complication is the variation in requirements between species, but less expected is the within-species variation reported for phenotypes of H. contortus by Le Jambre and Whitlock (1973), which enables a larval population to have a relatively wide range of temperature tolerance, and this requires further investigation.
16 Larval transmission
The extent to which free-living larvae migrate actively as opposed to passive dissemination is uncertain, while for infective eggs only the latter effect is operative. Probably larval m o v e m e n t is responsible for :migration out of faeces onto herbage in the immediate vicinity of the deposition site and results in high numbers being found close to the faeces (J~brgensen, 1980). Other agencies, such as earthworms, insects and farm animal activity are probably responsible for the wider distribution of larvae. Michel (1969) suggested that vertical migration was of little significance, but if soil is to be considered an important reservoir, then vertical migration becomes an essential part of the transmission process (Fincher and Stewart, 1979). We really k n o w very little a b o u t the behaviour of parasitic nematode larvae (Croll, 1972) despite the importance of directional m o v e m e n t in increasing host--parasite contact. Host behaviour, and the influence of management on behaviour, might be expected to have a marked impact on the uptake of infection, and there is evidence to suggest that the acquisition of larvae by grazing animals is lower than would be anticipated from random herbage sampling (Waller et al., 1981). Selective grazing and the avoidance of contaminated herbage m a y be partly responsible for the differences in worm burden at different stocking rates, particularly of those species with resistant infective larvae (Morley and Donald, 1980). This is perhaps more likely to be important in cattle grazing where the faecal pat m a y persist for a long time than in sheep grazing where faecal breakdown is more rapid. Rooting behaviour in pigs influences the uptake of Ascaris eggs, and this behaviour is itself modified by feed availability. PARASITE POPULATION PATTERNS Given the complexity of the interaction of parasite species, stage and environment involved in the process from contamination to larval uptake, the possibility of discerning general patterns of larval population and host infection would seem to be remote. However, there is a tendency towards stability in any host--parasite system (Odum, 1971), and in recent years it has been shown that such general patterns do occur under natural conditions in a range of environments and for a variety of parasites and hosts: sheep (Thomas and Boag, 1972; Donald and Waller, 1973), cattle (Armour, 1970) and pigs {Rose and Small, 1980). The c o m m o n e s t pattern is one of increased contamination rate in spring resulting in maximum larval availability in mid-summer to autumn, and peak late s u m m e r / a u t u m n host infection levels (Fig. 6). While this pattern is most apparent for those parasites with free-living infective larvae, there is some evidence for it where infection occurs via an infective egg (Stevenson, 1979). The most likely explanation for this tendency towards a general pattern of population fluctuation is the dominance of environmental temperature and moisture in determining the development, survival and transmission of the
17 I
2500
2000
........ Ewe egg o u t p u t ---
Lamb egg o u t p u t
--
P a s t u r e larval le
,I000
i" I I I
BOO
15oo
600 CD
61000
4o0~-
oh Ld
8 500
20O
.........r £ - - ' ; ' J ' : T : : Ape
May
dun
..... July
, v Aug
2-Sept
Fig. 6. Epidemiologieal pattern: sheep nematodes.
larval population (Levine, 1963). In its simplest form their effect may be explained on the basis that moisture is essential for development to occur, while in the presence of adequate moisture, temperature will determine the rate of development. Thus these two factors may be considered to determine the basic cycle c f parasite populations, and all other factors to influence the within-pattern variations in timing and the size of the peaks and troughs of numbers. This encourages the optimistic view that it should be possible to model the major patterns of population based on these t w o dominant factors, b u t with the pessimistic caution that the multitudinous subsidiary factors may be largely responsible within the overall pattern in determining the points at which the parasite population becomes a production problem. THE CONSTRUCTION OF POPULATION MODELS
We are faced with two possible choices in model building. One is the simple approach of modelling the parasite pattern based on these two factors of temperature and moisture. The other is a more complicated attempt to incorporate as many variables as possible in a sophisticated model which will n o t only indicate population pattern, b u t also population size and therefore the potential disease risk at any particular point in time.
Modelling the parasite pattern Given that the egg and larval habitat is soil and vegetation, meteorological data obviously do n o t measure the temperature and moisture conditions in the micro-habitat. However, equally obviously there is b o u n d to be a relationship between the two, and if the effect of atmospheric temperature and rainfall on the micro-habitat is reasonably direct, then these two parameters, which are widely recorded in routine meteorological work and in a very standard form, can be substituted for the much more difficult micro-climatic measurements. Instead of attempting to correlate macro- and micro-climate data the aim is
18 TABLE II Relationship of climate to ruminant nematodes* Climate
Typical locality
Dominant trichostrongylid
A
Tropical: rain, hot all year
Haemonchus
B
Dry steppe: (> 18°C) (< 18°C) Temperate: -3 ° C to 18° C moist all year, hot summer moist all year, warm summer Cold: below -3 ° C to above 10°C Polar: below 10°C
Equatorial Africa/ America Texas Idaho
C
D E
Haemonchus Ostertagia
Washington DC England, Germany Canada
Haemonchus Ostertagia
Arctic
None
Trichostrongylus
*From Levine, 1978 to correlate the macro-climate data with larval popul at i on measurements in an empirical way. A table (Table II) taken f r om Levine (1978) indicates the relationship between climate and r u m i n a n t n e m a t o d e s which determines their geographical distribution, and this t y p e of correlation led G o r d o n (1948) to devise bioclimatographs to explain n o t only species distribution, b u t also seasonal disease risk u n d er the apt slogan " w o r m s work by the weather". Levine and Andersen (1973) a t t e m p t e d a r e f i n e m e n t of the correlation based on relative transmission potential to express the availability of infection. In a slightly different approach Ollerenshaw and Rowlands (1959) correlated weather patterns with liver fluke disease incidence to devise the fluke forecasting system which is widely used in c ont r ol programmes, and Ollerenshaw and Smith (1969) suggested a similar m e t h o d of forecasting the incidence of ostertagiasis in cattle, and in sheep (Ollerer~shaw et al., 1978). These correlations t end only to per m i t general conclusions to be drawn, but the very specific influence of t e m p e r a t u r e on the hatching of N e m a t o d i r u s battus in Britain made it possible to derive a correlation between soil temperature and the appearance of a wave of infective larvae on pasture which was sufficiently precise to be used in forecasting the timing as well as the severity of disease outbreaks (Smith and Thomas, 1972). Since the pattern of seasonal larval availability for r u m i n a n t nem a t ode s is relatively constant in temperate conditions a similar correlation of weather conditions and peak larval activity has been a t t e m p t e d in Britain (Thomas, 1974; T hom as and Starr, 1978) and New Zealand (Vlassof, 1975), largely to encourage the practical application of integrated c o n t r o l programmes based on pasture m anagem ent and strategic anthelmintic t r e a t m e n t . In b o t h cases the correlation is between larval activity and rainfall rather than t e m p e r a t u r e , since while t e m p e r a t u r e contributes to
19
the basic larval pattern, moisture availability determines the balance between m e rate of development on the one hand, and the rate of drying which inhibits development and therefore is the more critical factor affecting the within-season timing of the larval peak. In a refinement of this approach Starr and Thomas (1980) have incorporated the temperature effect as well as moisture. The moisture status of the surface layer of pasture is calculated from rainfall and potential evapo-transpiration to give the time periods during which development can proceed. The daily larval development rate during these periods is then assumed to be proportional to the accumulation of daydegrees above a threshold temperature for larval development, i.e., the number of "heat units" available for development. The cumulative figures obtained for day-degrees from meteorological data have been compared with actual pasture larval counts over a ten-year period in North East England to identify the total day-degrees corresponding best to peak larval count, and for this particular area a day-degree c o u n t of 130 shows the best fit (Fig. 7). This process of summation of time and temperature above a minimum development threshold has been similarly used by Jones {1975) for plant parasitic nematode studies. Ostertagiasis 1978 actual/predicted
16 Accumulated degree days
o , , * e D e g r e e days
14
Wetness units P a s t u r e larval count
O
× 12
.eol
iS:i
c"
~
i [!!!i~ lo0-.4 .3 o
6 ?
o
50 "2 '~
~ 4
z0 2 I
April
IX4ay
June
July
|
August
September
Fig. 7. Ostertagiasis, 1978. Actual/predicted. F r o m Reviews in Agricultural Meteorology No. 1 (unpublished), copies from the Library, Meteorological Office, Bracknell.
This approach makes possible quite precise modelling of t h e parasite pop~lation pattern and its within-season variations, which has useful predictive value while obviating the need for detailed information on the ecology of eggs and larval stages. However, it is still largely qualitative, and while useful in
20 predicting periods of risk it will not provide any estimate of population size, and consequently of the likelihood and severity of disease outbreaks, except in the most general way.
Modelling the parasite population To model the size of the parasite population at any stage in the seasonal pattern requires precise and extensive ecological data, which has hitherto not been available, and it is to the credit of many parasitologists that the necessary information is steadily accumulating and increasingly in a form which is suitable for model building. Much of the early data was reviewed by Crofton {1963) and tended to concentrate on larval development and survival under experimental conditions. A significant contribution was made by Silverman and Campbell (1959) who clarified the influence of the faeces on the development of H. contortus larvae and drew attention to the fallacy of applying laboratory development rates to the field situation. More recent studies have tended to combine laboratory and field experiments, often in conjunction with field observations on the naturally occurring population patterns they are designed to explain. Many such studies have been carried out on the c o m m o n ruminant nematodes (see Michel, 1969, 1976), and to a small extent on the strongylid nematodes of pigs (Rose and Small, 1980). In contrast to the extensive literature on the ecology of nematodes with a free living infective stage, there is a marked lack of data on those species with an infective egg, such as the trichurids and ascarids, particularly in pigs. Such evidence as there is suggests that again temperature is a key factor in develo p m e n t (Burden and Hammet, 1979; Stevenson, 1979). However, the resistance of the infective egg to environmental conditions and the fact that host infection is purely passive, means that the epidemiology of infection is largely host-dependent, and control has no real ecological basis at present. A mathematical approach to the interpretation of field experimental data was initiated by Tallis and Donald (1964, 1970), studying the distribution of larvae on pasture. Levine and Andersen {1973) and Callinan (1977) have developed the use of relative translation potentials to predict pasture populations in relation to air and herbage humidity and soil temperature. Young et al. {1980a) in a very useful study, have shown that the hatching of eggs of O. circumcincta under alternating temperature conditions could be satisfactorily predicted from constant temperature experiments, thus very considerably easing the problems of data collection. In further work on O. ostertagi the same authors (Young et al., 1980b) were able to model larval development rate and death rate in dung pats as well as under controlled conditions. As might be expected they demonstrated a time lag in development due to environmental effects within the dung pat which will require further assessment. Parallel with these specific studies t w o more general models have been
21
attempted based on relatively limited data. Barger et al. (1972) constructed a model to simulate pasture larval populations of H. contortus in New South Wales. Meteorological data, herbage availability and sheep egg output were recorded, and a number of assumptions made to estimate development and survival from egg to infective larva. The predicted larval concentrations on pasture over a two-year period were compared with field observations and good agreement obtained. The model confirmed the critical role of moisture under favourable temperature conditions, and the authors considered it to be a useful tool in studying the effect of management factors on haemonchosis. More recently, Gettinby et al. (1979) have reported what appears to be the only model so far which predicts parasite populations both on pasture and in the host. Their prediction model for bovine ostertagiasis estimates larval development as previously described in terms of time and temperature above a development minimum, and incorporates a relatively low mortality rate, which perhaps assumes a quite rapid rate of ingestion by the host. Migration is determined by rainfall, and uptake based on herbage consumption. As pointed out earlier, the most difficult influence to estimate is that of immunity but this is avoided by considering only calves in their first grazing season, the group most susceptible to parasitism. Again good agreement was obtained between predicted and observed results for both parasite populations and for the occurrence of clinical disease, and it is suggested that such a model would be a valuable aid to the timing of within-season grazing management and treatment programmes. The success of these relatively simple models suggests that as more data become available, and therefore more variables can be accommodated with increasing accuracy, population modelling will become more precise and adaptable to a wider range of management and environmental situations. Morley and Donald (1980) point to the small extent to which control procedures have been tested in realistic production systems, and to the cost and difficulty of doing this. Developments in modelling the host/parasite/environment complex could help to solve these problems, but further progress will require more involvement of mathematicians in parasite ecology, for as stated by Patten (1971), the descriptive phase of ecology is being succeeded by the much more rigorous phase of systems ecology. Perhaps an appropriate closing quotation would be from Bawden (1978) -- "The emerging re-orientation of agricultural research associated with the development and application of systems ecology to production problems, and the appeals for higher order inter-disciplinary investigations implicit in protection ecology, provide the impetus to develop a perspective for parasite management". -- it probably sums up the purpose of this paper, and it is such a beautiful phrase! REFERENCES
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22 Andersen, F.L., Levine, N.D. and Boatman, P.A., 1970. Survival of third-stage Trichos t r o n g y l u s c o l u b r i f o r m i s larvae on pasture. J. Parasitol., 56: 209--232. Anderson, N., Dash, K.M., Donald, A.D., Southcott, W.H. and Waller, P.J., 1978. Epidemiology and control of gastro-intestinal parasites of sheep in Australia. A.D. Donald, W.H. Southcott and J.K. Dineen (Editors). C.S.I.R.O., Melbourne, Australia, pp. 24--52. Armour, J., 1970. Bovine ostertagiasis: a review. Vet. Rec., 86: 184--190. Armour, J., 1980. The epidemiology of helminth disease in farm animals. Vet. Parasitol., 6: 7--46. Armour, J. and Bruce, R.C., 1974. The inhibition of development of Ostertagia ostertagi - a diapause p h e n o m e n o n in a nematode. Parasitology, 69: 161--174. Armour, J., Saqir, I.M., Bairden, K., Duncan, J.L. and Urquhart, G.M., 1980. Parasitic bronchitis and ostertagiasis on aftermath grazing. Vet. Rec., 106: 184--185. Barger, I.A., Benyon, P.R. and Southcott, W.H., 1972. Simulation of pasture larval populations of H a e m o n c h u s c o n t o r t u s . Proc. Aust. Soc. Anim. Prod., 9: 38--42. Bawden, J.R., 1978. A perspective for parasite management. Agric., Environ., 4: 43--55. Bisset, S.A., 1980. Goats and sheep as hosts for some common cattle trichostrongylids. Vet. Parasitol., 7 : 363--368. Borgesteede, F.H.M., 1981. Experimental cross-infections with gastro-intestinal nematodes of sheep and cattle. Z. Parasitenkd., 65: 1--10. Bradley, D.J., 1972. Regulation of parasite populations. Trans. R. Soc. Trop. Med. Hyg., 66: 697--708. Brunsdon, R.V., 1964. The effect on the persistence and pattern of nematode infection of the transfer of naturally infected sheep from pasture to pens. N.Z. Vet. J., 12: 105-107. Brunsdon, R.V., 1980. Principles of helminth control. Vet. Parasitol., 6: 185--216. Burden, D.J. and Hammet, N.C., 1979. The development and survival of Trichuris suis ova on pasture plots in the south of England. Res. Vet. Sci., 26: 66--70. Callinan, A.P.L., 1977. The translation potential of sheep nematodes in Western Victoria. Proc. 8th Int. Conf. W.A.A.V.P., Sydney, Australia, Abstr. 83. Connan, R.M., 1968. Studies on the worm populations in the alimentary tract of breeding ewes. J. Helminthol., 42: 9--28. Crofton, H.D., 1958. Nematode parasite population in sheep on lowland farms. V. Further observations on the post-parturient rise and a discussion of its significance. Parasitology, 48: 251--260. Crofton, H.D., 1963. Nematode parasite populations in sheep and on pasture. Tech. Commun. 35. Commonwealth Agric. Bureau, Farnham Royal, England, 101 pp. Croll, N.A., 1972. Behaviour of larval nematodes. Behavioural aspects of parasite transmission. E.U. Canning and C.A. Wright (Editors). Academic Press, London. Dakkak, A., Fioramonti, J. and Bueno, L., 1981. H a e m o n c h u s c o n t o r t u s third stage larvae in sheep: kinetics of arrival into the abomasum and transformation during rumeno-omasal transit. Res. Vet. Sci., 31: 384. Dineen, J.K., Gregg, P. and Lascelles, A.K., 1978. The response of lambs to vaccination at weaning with irradiated T r i c h o s t r o n g y l u s c o l u b r i f o r m i s larvae: segregation into 'responders' and 'non-responders'. Int. J. Parasitol., 8: 59--64. Donald, A.D. and Waller, P.J., 1973. Gastrointestinal 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. Duncan, J.L., 1979. Studies on the epidemiology of bovine parasitic bronchitis. Vet. Rec., 104: 274--278. E1 Saqir, I., Armour, J., Bairden, K., Dunn, A.M., Jennings, F.W. and Murray, M., 1982. Observations on the infectivity and pathogenicity of three isolates of Ostertagia spp. sens. lat in calves. Res. Vet. Sci., 32: 106--112. Fincher, G.T. and Stewart, T.B., 1979. Vertical migration by nematode larvae of cattle parasites through soil. Proc. Helminthol., Soc. Wash., 46: 43--46.
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24 Shad, G.A., 1977. The role of arrested development in the regulation of nematode populations. In: G.W. Esch (Editor), Regulation of Parasite Populations. Academic Press, New York, 111 pp. Silverman, P.H. and Campbell, J.A., 1959. Studies on parasitic worms of sheep in Scotland. Embryonic and larval development of Haemonchus contortus at constant temperatures. Parasitology, 39: 23--37. 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., 1975. Decontamination of sheep and cattle pastures by varying periods of grazing with the alternate host. Int. J. Parasitol., 5: 45--48. Start, J.R. and Thomas, R.J., 1980. Parasitic gastro-enteritis in lambs -- a model for estimating the timing of the larval emergence peak. Int. J. Biometeor., 24: 223--229. Stevenson, P., 1979. The influence of environmental temperature on the rate of development of Ascaris suum eggs in Great Britain. Res. Vet. Sci., 27 : 193--196. Symons, L.E.A. and Steel, J.W., 1978. The epidemiology and control of gastro-intestinal parasites of sheep in Australia. In: A.D. Donald, W.H. Southcott and J.K. Dineen (Editors). C.S.I.R.O., Melbourne, Australia, pp. 9--22. Tallis, G.M. and Donald, A.D., 1964. Models for the distribution on pasture of infective larvae of the gastro-intestinal nematode parasites of sheep. Aust. J. Biol. Sci., 17: 504-513. Tallis, G.M. and Donald, A.D., 1970. Further models for the distribution on pasture of infective larvae of the strongyloid nematode parasites of sheep Math. Biosci., 7 : 179--190. Thomas, R.J., 1974. The role of climate in the epidemiology of nematode parasitism in ruminants. In: A.E.R. Taylor and R. Muller (Editors), The Effects of Meteorological Factors upon Parasites. Symposia of the Brit. Soc. Parasitol., 12: 13--32. Thomas, R.J. and Boag, B., 1972. Epidemiological studies on gastro-intestinal nematodes of sheep. Infection patterns on clean and summer-contaminated pastures. Res. Vet. Sci., 13: 61--69. Thomas, R.J. and Smith, W.C., 1968. Anthelmintic treatment of sows with thiabendazole. Vet. Rec., 83: 489--491. Thomas, R.J. and Starr, J.R., 1978. Forecasting the peak of gastro-intestinal nematode infection in lambs. Vet. Rec., 103: 465--468. Urquhart, G.M., Jarrett, W.F.M. and Mulligan, W., 1962. Helminth Immunity. Adv. Vet. Sci., 7: 87--129. Vlassof, A., 1975. The role of climate in the epidemiology of gastro-intestinal nematode parasites of sheep and cattle. Symposium on Meteorology and Food Production. N.Z. Meteorol. Service, Wellington, pp. 171--176. Waller, P.J. and Donald, A.D., 1970. The response to desiccation of eggs of Trichostrongylus colubriformis and Haemonchus contortus. Parasitology, 61 : 195--204. Waller, P.J. and Thomas, R.J., 1978. Nematode parasitism in sheep in North-East England: the epidemiology of Ostertagia species. Int. J. Parasitol., 8: 275--283. Waller, P.J., Dobson, R.J., Donald, A.D. and Thomas, R.J., 1981. Populations of strongyloid nematode infective stages in sheep pastures: comparison between direct pasture sampling and tracer lambs as estimators of larval abundance. Int. J. Parasitol., 11 : 359--368. Watt, K.E.F., 1971. Dynamics of populations: a synthesis. In: H. den Boer and H. Gradwell (Editors), Dynamics of Populations. Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands, pp. 568--580. Whitlock, J.H., 1949. The relationship of nutrition to the development of trichostrongylidoses. Cornell Vet., 39: 146--182. Young, R.R., Anderson, N., Overend, D. Tweedie, R.L., Malafant, K.W.J. and Preston, G.A.N., 1980a. The effect of temperature on times to hatching of eggs of the nematode Ostertagia circumcincta. Parasitology, 81: 477--491. Young, R.R., Nicholson, R.M., Tweedie, R.L. and Schuh, H.J., 1980b. Quantitative modelling and prediction of development times of the free-licing stages of Ostertagia ostertagi under controlled and field conditions. Parasitology, 81: 493--505.