lniernariond Journal/or Printed m Great Brirarn

Purrrsirology

Vol. 22, No. 6, pp. 789-799, 1992

002&7519/92 $5.00 + 0.00 Prrgamon Press Lrd SocieryJi~ Parasirology

Cj I992 Ausrrdian

A MODEL FOR NEMATODIASIS D. M. LEATHWICK,*

IN NEW ZEALAND

LAMBS

N. D. BARLOW? and A. VLASSOFF~

* Flock House Agricultural

Centre, Ministry of Agriculture and Fisheries, Private Bag 1900, Bulls 5452, New Zealand t Lincoln Agriculture and Science Centre, Ministry of Agriculture and Fisheries, P.O. Box 24, Lincoln, New Zealand $ Wallaceville Animal Research Centre, Ministry of Agriculture and Fisheries, P.O. Box 40063, Upper Hutt, New Zealand (Received 17 December 1991: accepted I5 March 1992)

Abstract-LEAntwIcK

D. M., BARLOWN. D. and VLASSOFF A. 1992. A model for nematodiasis in New Zealand lambs. Internariona/ Journalfor Parasitology 22: 789-799. A strategic model is described for the epidemiology of mixed nematode infections in New Zealand lambs. The model successfully reproduces known patterns of parasite epidemiology and production loss in lambs under currently implemented control strategies. The variation in model output during sensitivity analysis was within acceptable limits defined by field data. Model output was most sensitive to variation in parameters affecting survival and migration of the free-living stages and host resistance to infection, suggesting that these factors are most influential in regulating parasite populations. It is intended to use the model to focus research on key aspects of nematode epidemiology and control and, following the incorporation of appropriate genetic mechanisms, anthelmintic resistance. INDEX KEY WORDS: Nematodiasis; gastrointestinal nematodes; simulation: lambs; Ostertagia; Trichostrongylus; Haemonchus.

INTRODUCTION

epidemiology;

population

model;

The epidemiology of nematodiasis is complicated by interactions between the effects of weather on the development, migration and survival of the free-living stages, the variety of mechanisms of host resistance to the parasitic stages, the numerous grazing management practices used by farmers and the number of nematode species involved. As many as eight nematode genera may be present in lambs/sheep at one time (Brunsdon, 1970a; Douch, Harrison, Buchanan & Brunsdon, 1984). Disease dynamics are therefore highly variable and difficult to predict, and it may be unwise to generalize from the results of short-term field experiments (Callinan, 1987). In this situation, simulation modelling offers a useful avenue towards improved understanding of parasite dynamics, the development of new control strategies and the evaluation of control options for their likelihood to result in drench resistance. Previous models have focused on single species (Ractliffe, Taylor, Whitlock & Lynn, 1969; Paton, Thomas & Wailer, 1984; Grenfell, Smith & Anderson, 1987b; Barnes & Dobson, 1990), although Callinan, Morley, Arundel & White (1982) present parameter values for two species and Paton (I 987) assumes that an Ostertugiu spp. model could be applied to other species by varying egg output. However, processes other than egg output differ between species, and

THE control of nematodiasis in New Zealand is cyrrently based almost exclusively on the use of anthelmintic drenches (Kettle, Vlassoff, Lukies, Ayling & McMurtry, 198 I ; Kettle, Vlassoff, Ayling, McMurtry, Smith & Watson, 1982; Brunsdon, Kissling & Hosking, 1983). New Zealand sheep farms typically involve intensive, all year round grazing of pastures. Since climatic conditions are generally suitable for parasite development in the spring and autumn, and to a lesser extent during summer, there is considerable reliance by farmers on anthelmintic treatments to maintain animal growth throughout the year (Vlassoff & Brunsdon, 1981). Although grazing management has been promoted as a means of enhancing parasite control in lambs (Brunsdon & Adam, 1975), a 1979/1980 survey of farmer drenching practices (Brunsdon ef al., 1983) found that the annual number of drenches administered to lambs was 6.3 (range 0 to > l2), to I-2-year-old animals was 1.8 (range O-l 2) and to animals older than 2 years was I .2 (range O-10). However, the rapid rise, in recent years, in the reported incidence of anthelmintic resistance (McKenna, 1989a, b; Mason, 1989; West, Pomroy, Probert & Charleston, 1989) clearly indicates the need for a change from this strategy of regular drenching at short intervals. 789

D. M. LEATHWICK. N. D. BARLOW and A. VLASSOFF

790

rather than attempt to model each of these separately we use a different approach. Our primary objective is to increase understanding, in general terms, of the dynamics and control of nematodiasis in the field. This reflects the custom of regarding the disease as a single clinical entity (Brunsdon, 1966a). A model has therefore been developed for mixed nematode infections which reproduces the generalized epidemiological patterns observed in New Zealand (Brunsdon & Vlassoff, 1982; Vlassoff, 1982). This paper describes the model, the derivation of parameters, the results of a sensitivity analysis and an evaluation of the model’s performance. MATERIALS

L_________, 4 withinthe raeces -----------_----,

+

seasclna,Variation

AND METHODS

The model was run as an interactive

computer simulation with a discrete time step of 1 day. The basic model structure is presented in Fig. 1 and the derivation of parameter values is discussed below. Ene egg inpuls. Values for faecal egg production by lactating ewes were based on data from Brunsdon (1966b, 1970b, 1971) and Brunsdon & Vlassoff (1971). A pattern was assumed over time with 400 epg at lambing (late August), rising to a peak of 1000 epg midway through lactation (6 weeks post-lambing) then declining to 50 epg by weaning (late November/early December). After weaning no further ewe contribution to pasture contamination was allowed for, on the assumption that in New Zealand the ewe contribution to parasite epidemiology outside lactation is minimal (Brunsdon, 1982; Brunsdon & Vlassoff. 1982). Development of the non-i&five stages. The rate of development of the free-living stages is primarily dependent on temperature (Thomas, 1974; Young. Anderson, Overend, Tweedie, Malafant & Preston, 1980). As a result, seasonal differences in development times may be large. Under ideal conditions development from the egg to the infective third larval stage (L3) requires just a few days whereas at low temperatures the combination of slow development and high mortality results in few, if any, infective larvae developing. TABLE l-SEASONALLY

VARYING

Feb. Mar. Apr. May June July Aug. Sept. Oct. Nov. Dec.

FIG 1.Structure of the model for nematodiasis in lambs. The major driving variables are: seasonal variation affecting development rate of the egg and Ll:L2 stages (I and 2). survival from egg to L3 (3) and migration of L3s onto herbage (4); the vertical distribution of L3s on herbage and herbage height influences the number of L3 ingested (5) and developing host resistance reduces establishment of ingested larvae (6) and survival of adult worms (7). Monthly average values for the duration of the egg stage (I-7 days) and first two larval stages (7-21 days) were calculated using the observed seasonal pattern of development under New Zealand conditions (Vlassoff, 1982) and are presented in Table I. This gave a range in development times from egg to L3 of 8-28 days which, when combined with the seasonal survival values outlined below, mimicked the expected rapid transition under warm conditions and slow development with low survival during winter (e.g. Boag & Thomas, 1970). Survival of /hc non-irzfective stages. Survival of the egg and non-infective larval stages has been shown to vary enormously with temperature, humidity and aeration (Rose. 1963; Anderson & Levine. 1968; Young & Anderson. 198 I : Wharton, 1982). In laboratory cultures the proportion of

PARAMETER

VALUES

USED

IN

IHE

MODAL

Egg (days)

LI/L2

Survival egg to L3

Daily migration L3 onto herbage

(days)

(“A)

(%)

(kg ha ‘)

1.3 1.6 2.1 2.8 5.3 7.0 3.5 2.9 2.5 2.0 1.6 1.3

7.0 7.7 9.8 14.7 19.6 21.0 21.0 19.6 16.1 12.6 9.8 7.7

0.9 2.0 8.0 9.8 2.5 0.7 0.2 0.3 0.7 2.8 5.0 3.0

0.14 0.32 1.30 1.60 0.40 0.11 0.03 0.05 0.11 0.45 0.80 0.48

1900 1850 1400 1250 1050 950 750 850 950 I600 1900 2050

Duration Month

rime

Herbage dry matter

A model for nematodiasis eggs producing third-stage larvae ranges from 18 to 67 (Salih & Grainger. 1982). 54 to 70 (Young et ul., 1980) and 0 to 100% (Berberian & Mizelle, 1957). In the field survival to the third larval stage in ovine parasites has been estimated as up to 21 (Dinaburg, 1944) l-7 (Rose, 1963), O-8.9 (Callinan, 1978b), O-16 (Callinan, 1978a) and O-5% (Callinan, 1979). We therefore followed the seasonal pattern of development success outlined in Vlassoff (1982) with maximum and minimum values set at IO and 0.2%. Migrafion of i&tive larvae. The migration of infective larvae onto herbage is influenced substantially by temperature and humidity (Rees, 1950; Silangwa & Todd, 1964; Callinan & Westcott, 1986). The climatic factors favourable for migration are also those likely to favour survival of eggs and non-infective larvae. We therefore used the curve for seasonal variation in survival of the non-infective stages (Vlassoff, 1982; see previous section) to estimate seasonal patterns of larval migration. To estimate actual migration rates we used a pasture phase submodel utilizing the relationship for survival and development of the free-living stages described in the following and previous two sections. Known faecal egg counts were entered into the submodel and the height of the migration curve adjusted to give the appropriate pasture larval counts from the data sets. The resulting estimates for average instantaneous migration rate ranged from 0.016 (in autumn) to 0.00016 (in winter) with an annual mean value of 0.00486. This range of values encompasses the maximum likelihood value of0.00884 estimated by Grenfell. Smith&Anderson (1986) for Ostertugiu osrertugi in cattle and is similar to the rates measured experimentally by Rees (1950). Silangwa & Todd (1964) and Callinan & Westcott (1986). Survival of i&/ire lurvue. Of the free-living stages the infective third-stage larva (L3) is the most resistant to temperature and desiccation, and the longest lived (Rose, 1961, 1963; Young & Anderson, 1981). The survival of L3 larvae may vary with temperature, moisture, sunlight and larval age (Rose, 1963; Grenfell et al., 1986) although Rose (1961) reports no effect of climate. Grenfell et al. (1986) suggest that although climatic factors affect L3 survival, field sampling procedures are not always rigorous enough to detect their influence. In their model of larval demography a constant survival rate gave equivalent output to a climatedriven variable survival (Grenfell et al., 1986). The limited data available on the survival of infective larvae under New Zealand climatic conditions indicate that some larvae may survive on pasture for over 6 months (Vlassoff, unpublished data). We therefore used a constant daily survival of 0.977. While this value is less than the maximumlikelihood value (0.9911) for 0. ostertugi and Cooperiu oncophoru in calves estimated by Grenfell et al. (1986) it is close to the 0.97 for Osrertugiu circumcincfu in lambs used by Paton et al. (1984). When applied to a single cohort of larvae this value yields a steady decline in numbers with I .5% surviving longer than 6 months. This is not dissimilar to the observations of Gibson & Everett (1967, 1972) and Boag & Thomas (1970). Larvae ingested. Equations from White, Bowman, Morles, McManus & Filan (1983) were used to develop a relationship between intake of dry herbage and age of the lambs. After the

in New Zealand

lambs

791

first 14 days of life during which herbage intake is assumed be zero, dry-matter intake is estimated by: I = 1.45 x (7’ -

to

14)‘i (3600 + (T ~ 14)‘);

where I is kg dry herbage ingested per lamb per day and Tis time in days since birth. In order to calculate the number of larvae being ingested, and to compare pasture larval populations with observed data (larvae per kg wet herbage), dry herbage values were converted to wet weight. This was done using weekly means for herbage percentage dry matter calculated from data collected over 2 years from six sites throughout New Zealand (Vlassoff, unpublished data). The vertical distribution of larvae on the sward is not uniform (Callinan & Westcott, 1986) and the height of grazing is variable. This is likely to result in more larvae being ingested as available herbage, and hence grazing height, is reduced (Martin, Beveridge, Pullman & Brown, 1990). In the model we assume an exponential relationship for the vertical distribution of larvae on herbage (Vlassoff, 1982). By arbitrarily setting grazing height at half that of the herbage we calculate the number of infective larvae ingested daily by multiplying the herbage intake (kg per lamb per day), larval density on the herbage (larvae kg ‘) and the proportion of those larvae available to the lambs. Thus:

Li = I x Lt x Pa

where Li is the number of the intake of wet herbage number ofinfective larvae proportion of total larvae as;

infective larvae ingested daily, I is per lamb per day, Lt is the total per kg of wet herbage and Pa is the available to the lambs, calculated

pa = e 05H.” where H is herbage dry matter ha ’ (for simplicity herbage biomass is used as an indicator of herbage height) and a is a constant (463 kg ha ‘) estimated by equating the data of Silangwa and Todd (1964) with conversion estimates for pasture height to kg ha- ’ dry matter. The establishment of ingested larvae. The proportion of ingested L3 larvae which establish in the host has been shown to decline with the host’s experience of infection (Gibson & Parfitt, 1973, 1976; Callinan & Arundel, 1982; Gibson & Whitehead, 1981; Barger & Le Jambre, 1988). Some data suggest that this decline in establishment is dependent entirely on the duration of infection and that the magnitude of the parasite burden and the rate of infection have no influence (Barger, Le Jambre, Georgi & Davies, 1985; Smith, 1988). However, with some worm species at least it has been shown that animals exposed to high larval challenge develop immunity faster than those receiving fewer larvae. This implies that regulation is at least partially a function of the intensity of larval exposure (Chiejina & Sewell, 1974b; Waller & Thomas, 1981; Dobson, Wailer & Donald, 1990). The effect of host age on establishment of infective larvae was estimated directly from the data sets of Douch et al. (1984) and Douch (1988, 1989). Worm burdens of previously uninfected ‘tracer’ lambs were divided by estimates for

792

D. M. LEATHWICK, N. D. BARLOW and A. VLASSOPF

number of larvae ingested. These were calculated from pasture larval counts and estimates of daily herbage intake (see previous section). Data presented in Waller, Dobson, Donald & Thomas (1981) suggest that in tracer lambs significant mortality of established worms does not occur within the first 4-6 weeks. This supports the assumption. implicit in these calculations, of near zero death rate for worms established in the tracers. What is not accounted for. however, is the possibility of density-dependent regulation of worm burdens through a direct effect of infection rate (Waller et al., 1981). Under New Zealand field conditions the probability of lambs being free from larval challenge is almost zero and so host age and the duration of Infection are effectively the same. The proportional establishment of infective larvae as a function of host age, or the duration of infection, is therefore described by: p=rr-hT where p is the proportion of ingested larvae which establish, u = 0.466, b = 8.02 x 10 ’ (estimated from the data of Douch et al. (1984), Douch (1988, 1989); r’ = 0.60) and T is the age of the lambs in days. By assuming minimal mortality of fourth-stage (L4) larvae (Grenfell, Smith & Anderson, 1987a; Smith, 1988) it was also possible to calculate approximate establishment rates for permanently grazed lambs from the data set of Douch el al. (1984). The difference in larval establishment between permanently grazed and tracer lambs reflects the host’s experience of infection. Combining these two factors gives:

where ELI is the cumulative daily total of L3 larvae ingested. The data set was incomplete with regard to pasture larval counts so it was not possible to calculate directly the effect of experience of infection on establishment rate. We therefore set a lower limit on establishment based on the available data and estimated the coefficient c (= 7.23 x 10 ‘) by tuning the model to give the required output. Under a normal pattern of larval challenge (in the absence of drenches) the resulting decline in larval establishment is a declining sigmoidal shape similar to that used by Smith (1988). The death rate of established ~wrms. Once third-stage larvae become established in the host they develop through a fourth stage where mortality is negligible (Hong, Michel & Lancaster, 1986; Grenfell ef al.. 1987a; Smith, 1988). We therefore assume no mortality in these stages and applied mortality to the adult (LS) stage only. Some authors have related mortality of established worms to the current rate of larval intake (Anderson & Michel, 1977; Callinan & Arundel. 1982; Barger & Le Jambre, 1988). However, in our model a death rate equation of this type failed to explain the observed changes in the lamb’s worm burdens. In particular, when the number of larvae ingested declined following the autumn peak in pasture infestation, the adult worm death rate would also decline. This resulted in unrealistically high worm burdens over the winter when self-cure would normally have occurred (Brunsdon, 1970a). We therefore follow Grenfell PI al. (1987a,b) and Smith (1988) in relating survival of adult worms to cumulative experience of infection.

Thus: where .v is the daily survival rate for adult worms, ZLI is the cumulative daily total of L3 larvae ingested and c1and h are constants (a = 0.9993: h = 5.603 x 10 ‘: r’ = 0.36) estimated from the data of Douch e( ul. (1984). When used in the model, this equation produces estimates of daily survival for adult worms ranging from 0.999 to 0.904 which are similar to the estimates of Anderson & Michel (1977), 0.9@ 0.98; Barger & Le Jambre (1988).0.913-0.964 and Paton (21trl (1984), 0.96. Fecundif! o/ /emcde ~wrm.s. Numerous authors have reported the effect of increasing host resistance in reducing fecundity of adult female worms in single species Infections (Gibson & Parfitt, 1973; Chiejina & Sewell. 1974b: Coop. Sykes & Angus, 1977: Smith, Grenfell & Anderson. 1987). However, nematode species differ considerably in thclr fecundity (Dineen & Wagland, 1966; Callinan c’t (I/., 1982). and so the effect of host resistance may not be so obvious in I field situation. with multiple species infection and with species composition changing over time. Analysis of the detailed field data set of Douch (II al. (1984) failed to indicate a decline in mean eggs per adult worm (all species pooled) over a 12 month period. It was also found, by running the model, that the ef?ect of a decline in fecundity w’as insignificant in terms of model output, compared to the efrcct of declining worm burdens. Fecundity was therefore held constant at 450 eggs per female per day and a constant 50:50 sex ratio assumed. The resulting predictions of daily pdecal egg counts were not dissimilar to those based on Paton c’t (I/. (1984)‘s conversion of 0.225 x the number of adult worms. Ho.c/ thrifi. The parasite host interaction is complex, and at present is not fully understood. Parasitism is manifcxt in the host as a reduction both in food intake and the eficiencq of utilization of metabolizable energy. This results in reduced skeletal development. weight gains and wool growth (Coop. Sykes. Spence & Aitchison. 1981: Sykes & Poppl. 1982). At least two components are known to be responsible for the parasites’ effect on the host. Histological and metabolic changes associated with the presence of parasites in the ho\t are well documented (Coop ef ul.. 1977. 1981; Steel. Symons & Jones. 1980) and the production advantages due to removal of established worms by the use of anthelmintic drenches are well recognized. There is also clear evidence for production losses in lambs (McAnulty. Clark & Sykes. 1982) and mature sheep (Barger & Southcott, 1975: Brunsdon. Vlassoff & West, 1986) associated with the intake of larvae per .se. apparently through the stimulation of a host tmmune response. In order to reproduce the parasite effect on host thrift it was therefore necessary to consider both n,orm burdens and larval challenge. Data from Brunsdon ( 1966a) m which drenched and undrenched lambs were exposed to equal larval challenge were used to derive a relationship between cumulative worm burdens and weight loss. The effect 01 different larval intakes at the same worm burden was deduced from VlassofT& Brunsdon’s (198 1) comparison of protective and preventivedrenching regimes. In their trials thecumulatlve faecal egg counts were approximately equal. Under the assumption that faecal egg counts generally reflect relative worm burdens in lambs (McKenna, 1981: Douch CI ul.. 1984). the

A model for nematodiasis

in New Zealand lambs

production differences between treatments are the result of differences in the number of larvae ingested. Losses due to the two components, larval intake and worm burden, appeared not to be additive as unrealistically high losses were predicted when both are high. The simplest interaction was therefore assumed, with the effect of cumulative larval intake declining with high cumulative worm burdens. The effect of parasitism on lamb liveweights was therefore estimated as:

where WL is loss of liveweight due to parasitism, ZWB is the cumulative daily worm burden, ZLLi is the cumulative daily intake of infective larvae, and a and h are constants (a = 2.54 x IO ‘; rz = 0.94 and b = 3.21 x IO ‘; ? = 0.95) derived as outlined above. Fis the discount coefficient for the interaction between ZWB and ZLLi, defined as;

where JWB,,,

is the maximum cumulative worm burden. Fuecal output. Faecal output is assumed to be directly proportional to dry matter ingested and an equivalent relationship to that used to predict intake (see above) was used to predict faecal production up to a maximum of 1400 g per day at the two-tooth stage (Gillingham A., unpublished PhD thesis, Massey University. 1978).

RESULTS Sensitivit? The model successfully reproduces the generalized scenarios of Brunsdon and Vlassoff (1982) (Fig. 2). These scenarios represent the average values taken from a large number of data sets collected over a number of years and sites and thus are a useful indication of patterns of parasite epidemiology under different management options. However, as these scenarios were used in estimating some of the coefficients used in the model they could not be used for validation. No attempt was made to reproduce specific data sets for three reasons. Firstly, the model was developed not as a tactical tool but rather as a strategic aid in the management of nematodiasis and anthelmintic resistance. Secondly, because of the highly variable nature of individual field data sets, comparing them with model output is of limited value (Grenfell et al., 1987b). Finally, the use of experimental single species, trickle infection data was avoided on the grounds that it may not fully represent the epidemiology of mixed infections in the field. For example, pure infection of Trichostrongylus colubriformis may result in worm burdens reaching 100,000 (Chiejina & &well, 1974a) whereas in the field, numbers of this species seldom exceed 20-30,000 and total worm burdens above 50,000 are uncommon (Brunsdon, 1970a; Douch et al., 1984; Vlassoff, unpublished data).

FIG. 2. Faecal egg counts and the corresponding larvae per kilogram of herbage for (a) undrenched lambs and (b) for lambs given four protective drenches (v) at 28 day intervals from weaning, from the generalized scenario of Brunsdon & Vlassoff (1982) (-) and estimated by the model (0 l 0). Simulation involved lambing in late August, weaning at 12 weeks and set-stocking lambs at 15 ha ‘. Sensitivity analysis was used to test the robustness of model output, in the undrenched situation, to variations in parameter values. For the free-living stages, parameters for survival of eggs to L3s and migration of L3s onto herbage were varied by & 50%. The survival of L3 larvae was also varied by adjusting the time to 50% death for a cohort by f 50%. These perturbations produced similar variations in model output. However, while the first two parameters varied within the range of values measured in the field, the third parameter did not. For example survival of eggs to L3s was varied such that maximum values were between 5 and 15% which is within the 5-20% range observed in the field (Dinaburg, 1944; Callinan, 1979). Values for daily survival of L3s were varied between 0.9847 and 0.9548 which yield cohort survivals outside the ranges observed in New Zealand (Vlassoff, unpublished data). It follows then that for field populations, climate affecting survival of eggs to the L3 stage and migration of L3s onto the herbage is likely to play a greater role in determining parasite dynamics than changing levels of L3 survival. Other parameters including worm fecundity, the number of eggs deposited by ewes prior to weaning and the rate at which the host becomes refractory to incoming larvae and influences worm death rate were also varied by f 50% in turn. These substantial changes in any one parameter value yielded patterns of faecal egg counts and pasture larvae (Fig. 3) within the ranges observed in the field (Brunsdon, 1970a; Vlassoff, 1982).

D. M. LEATHWICK, N. D. BARLOW and A. VLASSOFF

L3s outside the host, rate of development of host immunity and worm fecundity were all varied by i 10% to establish effect on model output. The resulting variation in faecal egg output and pasture larval populations (Fig. 4) was within acceptable limits set by field data (Brunsdon, 1970a; Vlassoff, 1982) particularly as all five parameters are unlikely to vary in the same direction at the same time. The sensitivity analysis also indicates, under the mechanisms of the model, the relative importance of different factors in determining the overall pattern of parasite dynamics. Large differences in pasture larval populations, brought about by changing parameter values for parasite survival and migration (Fig. 3a,b) were not translated into equivalent differences in faecal egg output, due to the density-dependent effect of host immunity. Similarly, large differences in faecal egg output induced by varying the rate of development of host resistance to infection (Fig. 3d) resulted in only minor changes in pasture larval infestation. This was due to the high faecal egg counts occurring in late autumn and early winter when survival of eggs is normally low. Varying worm fecundity, however, resulted in an equivalent response in pasture larva1 populations (Fig. 3c), reflecting the well established relationship between egg production by lambs in the summer and the size of the autumn peak in pasture larvae (Vlassoff, 1982). FIG. 3. Model estimates for faecal egg output and pasture larval counts when parameter values for (a) survival of eggs to the L3 stage, (b) migration of infective larvae onto pasture, (c) worm fecundity, (d) rate of development of host immunity were varied by f 50%. Simulation involved lambing in late August, weaning at 12 weeks and set-stocking lambs at 15 ha ’ with no drenching.

. . . L. -. u. L---fK

8 =

6

-i

rz K 0

6

E.

_.--: .-

ii

-

--.

-

-

_-_

0

6

b

.

-.

k

82 0

.

.

I

-4 8

-4

--.

.

. --.

.

‘f

ASONDJFMAMJJA

FIG. 4. Model estimates for faecal egg output and pasture larval counts when the parameters for survival of eggs to the L3 stage, migration of infective larvae onto pasture, survival of L3 larvae, worm fecundity and host immunity were concurrently varied by f 10%. Simulation as for Fig. 3.

in parameter values was also tested. Five parameters; survival of eggs to L3s, migration of L3s onto herbage, survival of The influence

of concurrent

variation

M0”tl-l

MO”Wl

FIG. 5. The effect of setting parameters for host immunity (a) and survival and migration of free-living stages (b) constant at their yearly average (-) compared with normal model output (* l l). Simulation as for Fig. 3.

The role of the two factors having the greatest effect on model output (i.e. variation in the survival and migration of the free-living stages and the rate of development of host immunity) in determining the

A model for nematodiasis in New Zealand lambs overall pattern of parasite epidemiology was examined further. The influence of each in turn was removed by setting parameter values constant at their yearly average value. A constant value for host immunity (Fig. 5a) resulted in lower pasture larval populations due to the slow build up of worms in the host, but the seasonal pattern of larvae on pasture was as expected. Faecal egg counts, however, failed to decline as expected indicating that density dependence, acting through acquired host immunity, is largely responsible for the decline in worm burdens and hence faecal egg output at the end of the season. Conversely, removing the effect of seasonality on the free-living stages had a significant effect on pasture larval populations (Fig. Sb), but the minor effect on faecal egg output could be accounted for as a delayed expression in the densitydependent effect of host immunity resulting from lower larval intake. The general pattern of parasite dynamics within the host can therefore be explained largely by the host’s ability to resist infection. This has also been demonstrated elsewhere (Roberts & Grenfell, 1991). Similarly the dynamics of pasture larval populations appears to be determined largely by the influence of climatic factors. Both effects are necessary to account for the overall within-year dynamics of the nematode populations.

A number of control strategies were compared using the model. These included preventive drenching (PD) consisting of five drenches at 28 day intervals starting in early December (Brunsdon & VlassofT, 1982), two integrated control (IC) strategies (Brunsdon & Adam, 1975) and the common farmer practice of drenching iambs monthly from December to June (seven drenches) (Brunsdon et al., 1983). The first integrated control strategy consisted of a drench and move to ‘safe’ pasture in early December followed by a second drench and move, again to safe pasture, in the first week in March. The second integratedcontrol strategy included an additional anthelmintic treatment given 21 days after each move (Brunsdon & Viassoff, 1982). Mean lambing date was taken as the last week in August, lambs were weaned at 12 weeks of age and set stocked at I5 ha-‘. Model output is in accordance with published data (Brunsdon and Vlassoff, 1982; Davis, 1986; Bell, 1987) in suggesting that under average climatic conditions all the strategies are approximately equal in their ability to control parasites (Table 2). However, the level of control decreased, and differences between the strategies increased, when parameters were varied to simulate autumn conditions of above average suitability for parasite development and migration. To

795

TABLE 2-ESTIMATEDPRODUCTION PARASITISMINLAMBSAT

Strategy

Farmer Preventive Integrated

Number of drenches

7 5 2 4

L~SSES(LIVE-WEIGHT)DUETO

12 MONTHSOFACE Weight loss Weight loss (kg) (kg) (average year) (good autumn*) 1.8 2.6 3.7 2.1

2.6 4.8 8.0 3.8

* Parameters modified to simulate above average conditions for parasites. simulate these conditions, survival of eggs to L3s was allowed to vary up to a maximum of 20%, which is the highest value recorded in the field (Dinaburg, 1944) and daily migration of L3s onto the herbage varied up to a maximum of 3.2%, which is less than the highest value (4.5%) recorded by Calhnan & Westcott (1986). Under these conditions, the period of protection offered by the basic PD programme was found to be insufficient, and only IC with four drenches appeared capable of maintaining a level of control close to that of protracted drenching (farmer practice). Again this is in keeping with current understanding of the dynamics and control of nematodiasis. Bell (1987) compared PD and preventive plus (PDi-) drenching (i.e. four additional drenches at 28 day intervals) with suppressive (fortnightly) drenching (SD) on nine farms. Average live-weight differences were 2.9 kg between PD and SD and I .8 between PD + and SD compared with model estimates of 2.2 kg for PD vs SD and 1.8 for PD vs PD + . The model therefore, appears capable, at least qualitatively, of reproducing observed parasite epidemiology under a range of management options and of estimating average production advantages due to parasite control for those strategies for which field measurements are available. DISCUSSION The model’s sensitivity to variation in the parameters for host resistance and survival and migration of the free-living stages suggests that these are the major determinants of the observed pattern of parasite epidemiology. As such they may offer the greatest potential for manipulation in order to influence parasite dynamics. The potential for manipulating the freeliving stages appears small, although there may be scope for using pasture species and management to manipulate microclimate, or predatory fungi to reduce larval survival (Hashmi & Connan, 1989). Model sensitivity (Fig. 3a,b) suggests, however, that large

D. M. LEATHWICK, N. D. BARLOW and

796

reductions in pasture contamination would be required to significantly reduce worm numbers in the host, due to the density-dependent effect of host immunity. There may be more potential to influence parasite dynamics through selecting for increased host resistance, or through the development of vaccines. The model has highlighted several points relating to this. Figure 3c shows that when egg output is reduced throughout the whole season the effect on autumn pasture contamination is large, but when egg output is only reduced in late summer and autumn (Fig. 3d) the resulting reduction in pasture contamination is relatively small. Therefore, to obtain maximum benefit from reduced pasture contamination. efforts to develop vaccines or select resistant lines of sheep need to concentrate on the earliest possible expression of host immunity. This work is in progress (Baker, Watson, Bisset & Vlassoff, 1990; Bisset, Vlassoff & West, 199 I ) and preliminary results have demonstrated the ability of young lambs to express some immunity (Douch, 1988). Also, it should be noted that if the development of host resistance is a function of cumulative larval exposure and/or worm burden, as assumed in this model, then any benefits attained from increasing host resistance are likely to be negated under frequent drenching. The dynamics of nematodiasis in the field is a highly variable process due to the changing complex of worm species, climate driven variables, differences in host resistance/tolerance to infection and the numerous management options possible. This high variability complicates the understanding of detailed parasite epidemiology and the evaluation of new management options, particularly those which do not rely heavily on the use of anthelmintics. The model outlined here represents our current understanding of the dynamics and driving variables of nematodiasis under New Zealand conditions. Its performance is consistent, in general terms, with current expectations and understanding of parasite dynamics under a range of control options. As such it forms a useful tool with which to focus discussion and research on key aspects of nematode epidemiology and management. The next step will be the incorporation of genetic mechanisms for anthelmintic resistance in order to address New Zealand’s escalating resistance problem. wish to thank Stewart Bisset and Mick Roberts for constructive comments on the manuscript and Phil Douch for access to his data. Acknowledgements-We

REFERENCES ANDERSON F. L. & Lrvt~r

N. D. 1968. Effect ofdesiccation on survival of the free-living stages of Trichosrrong>,luv co/uhriformis. Journal of Para.ritolqq 54: I I771 2X.

A.

VLASSOFF

ANDERSON R. M. & MICHEL J. F. 1977. Density-dependent survival in populations of Oslertagia ostertagi. International

Journalfor

Parasitology

I: 321-329.

BAKER

R. L., WATSOIYT. G., BESET S. A. & VLASSOFF A. 1990. Breeding Romney sheep which are resistant to gastrointestinal parasites. In: Proceedings ofthe 8th Corzference of’ the Au.vtralian

Palmerston

qfAnimal

Association

Breeding und Genetic.r.

North,

New Zealand, pp. 1733178. BARGER 1. A. & SOUTHCOTT W. H. 1975. Trichostrongylosis and wool growth 3. The wool growth response of resistant grazing sheep to larval challenge. Australian Journul of Experimental

Agriculture

und Animal

Husbandry

15: I67

172.

BARGER I. A., LE JAMBRL L. F., GEROGI J. R. & DA~IF_SH. I. 1985. Regulation of Haemonchus conmrtus populations in sheep exposed to continuous infection. Inrrrnurionul

Journalfor

Parasitology

15: 529-533.

BARCER I. A. & LF JAMBRE L. F. 1988. Regulation 01 Haemonchus conforrus populations in sheep: mortality 01 established worms. In.ternarional Journal fbr Purasi/ologr 18: 2699273. BARNES E. H. & Doeso~ R. J. 1990. Population dynamics of Trichmtrongylus coluhr(formis in sheep: computer model to simulate grazing systems and the evolution of anthelmintic resistance. International Journal for Prrrmi~olog,v 20: 823 831. BELL

K. 1987. Preventive drenching of lambs m Northland. 14: 13-14. BERBERIANJ. F. & MIZFLLF J. D. 1957. Developmental studies on Huemonc~hus c’on/or/u.t Rudolphi ( 1803). iimericcrn Surveillance

Midland

Naturcrlivt

51: 42

1 439.

Btssr,t S. A.. VLASSO~~A. & Wr-st C‘. J. 1991. Breeding for resistance/tolerance to internal parasites. In: Prwtic~trl Aspects of Internal Prrrusite Control (Edited by P~ILRS~U G. V.), pp. 8339 I. Proceeding.r of‘ lhr 2 lxt Seminar, Sheep and Beef CuttIe

.Soc,iety, Ne,t, Zealand

Veterinary

A.w-

July 1991. Publication No. 134. Massey University, Palmerston North. New Zealand. BOAG B. & THOMASR. J. 1970. The development and survival of free-living stages of Tric~ho.vtrong~lus c~o1uhrifbrmi.s and Osrerrcrgia circ~um&c,tu on pasture. Researc,h in Vetermcirj~ Scwnce 11: 380-38 I. BRLINS~~~ R. V. 1966a. Internal parasites of sheep and their effects on production. Proceedings of the New Zrcrland Socwly,fbr Animal Produclion 26: 165-l 8 I BRCJNSDON R. V. 1966b. Importance of the ewe as a source 01 trichostrongyle infection for lambs: control of the springrise phenomenon by a single post-lambing anthelmintic treatment. IV’CH. Zealand Vererinarr Journal 14: 118-125. BRUNSDON R. V. 1970a. Seasonal changes in the level and composition of nematode worm burdens in young sheep. Neir Zealand Journcrl of Agricultural Reseawh 13: 126-14X BKUNSLXINR. V. 1970b. The spring-rise phenomenon: seasonal changes in the worm burdens of breeding ewes and in the availability of pasture infection. NCH, Zcnlcrnd Veterincrry Journal 1X: 47. 54. BRUNSDON R. V. 1971. The post-parturient rise in the faecal ciation,

egg count of ewes: some host- parasite relationships. N~II, 19: 100&107. R. V. & VL\SSOI i A. 1971. The post-parturient rise: a comparison of the pattern and relative generic

Zealand

BRUMMX

C.e/erintrrF Journal

A model for nematodiasis composition of strongyle egg output from lactating and nonlactating ewes. Net%’Zealund Veterinary Journal 19: 19-25. BRUNSDONR. V. & ADAM J. L. 1975. Internal Parasites und Animal Production, New Zealand Society of Animal Production, Publication No. 4. BRUNSDON R. V. 1982. Host/parasite interrelationships in trichostrongylid infections. In: Control of Inter& Parusites in Sheep (Edited by Ross A. D.), pp. 21-24. Animal Industries Workshop, July 1982. Lincoln College, New Zealand. BRU~SDON R. V. & VLASSO~FA. 1982. Parasite control-a revised approach. In: Control qflntemal Parusites in Sheep (Edited by Ross A. D.), pp. 53-64. Animal Industries Workshop, July 1982, Lincoln College. New Zealand. BRUNSDONR. V., KISSLINGR. & HOSKINGB. C. 1983. A survey of anthelmintic usage for sheep: a time for change? Nen’ Zealand Veterinur) Journal 31: 24-29. BRUNSDONR. V., VLASSOFFA. &WEST C. J. 1986. Effect of natural trichostrongylid challenge on breeding ewes. Ne\r Zeuland Journal of E.uperimental Agriculture 14: 3741. CALLINANA. P. L. 1978a. The ecology of the free-living stages of Ostertugia circ’umcincta. Internutionul Joournal,for Parusitology 8: 233-237. CALLI~AN A. P. L. 1978b. The ecology of the free-living stages of Trichostrongylus uuei. Internationul Journul for Porasitology 8: 453456. CALLINANA. P. L. 1979. The ecology of the free-living stages of Trichostrongylus vitrinus. International Journal for Parasitology 9: 133-136. CALLIN~N A. P. L. & ARUNDEL J. H. 1982. Population dynamics of the parasitic stages of Ostertagia spp. in sheep. lnternotionol Journal for Parasitology 12: 531-535. CALLITYANA. P. L.. MORLEY F. H. W., ARUNDEL J. H. & WHITE D. H. 1982. A model of the life cycle of sheep nematodes and the epidemiology of nematodiasis in sheep. Agriculturcrl Systems 9: 199-225. CALLINA~ A. P. L. & WESTCOT~ J. M. 1986. Vertical distribution of trichostrongylid larvae on herbage and soil. International Journul.for Parasitology 16: 241-244. CALLINAN A. P. L. 1987. Nemat-a computer model for sheep nematodes. In: Computer Assisted Management qf Agricultural Production Systems (Edited by WHITE D. H. & WEBER K. M.), pp. 67-72. R.M.I.T.. Melbourne, 14-15 May. CHIEJINA S. N. & SEWELL M. M. H. 1974a. Experimental infections with Trichostrongylus colubrijormis (Giles, 1892) Looss, 1905 in lambs: worm burden, growth rate and host resistance resulting from prolonged escalating infections. Parasitology 69: 301-314. CHIEJINA S. N. & &WELL M. M. H. 1974b. Worm burdens, acquired resistance and live weight gains in lambs during prolonged daily infections with Trichostrongylus colubr~formis (Giles, 1892) Looss. 1905. Parasitology 69: 3 lS_ 327. COOP R. L., SYKES A. R. & ANGUS K. W. 1977. The effect of daily intake of Ostrrtagia circumcinctu larvae on body weight, food intake and concentration of serum constituents in sheep. Research in Veterinary Science 23: 7683. COOP R. L., SYKES A. R., SPENCE J. A. & AI~CHISON G. U. 1981. Ostertugia circumcincta infection of lambs, the effect

in New Zealand

lambs

797

ofdifferent intakes oflarvae on skeletal development. Journal of Comparative Pathology 91: 521-531. DAVIS G. B. 1986. An evaluation of a modified preventive drenching programme on commercial farms. Surveillance 13: 6-7. DIE~ABURG A. G. 1944. Development and survival under outdoor conditions of eggs and larvae of the common ruminant stomach worm, Haemonchus contortus. Journrrl q/Agriculturul Research 69: 421-433. DINEEN J. K. & WAGL~ND B. M. 1966. The dynamics of the host parasite relationship. IV The response of sheep to graded and repeated infection with Haemonchus contortus. Parasitology 56: 639-650. DOBSON R. J., WALLER P. J. & DONALD A. D. 1990. Population dynamics of Trichostrong_vlus colubr~formh in sheep: the effect of infection rate on the establishment of infective larvae and parasite fecundity. Internationul Journctl_for Parasitology 20: 347-352. DOUCH P. G. C., HARRISON G. B. L.. BLCHANA~ L. L. & BRUNSDONR. V. 1984. Relationship of histamine in tissues and antiparasitic substances in gastrointestinal mucus to the development of resistance to trichostrongyle infections in young sheep. Veterinary Parasitology 16: 273-288. DO~CH P. G. C. 1988. The response of young Romney lambs to immunization with Trichostrongylus colubr@rmis larvae. Internationul Journalfor Parasitology 18: 1035-1038. DO~CH P. G. C. 1989. The effects of immunization of sheep with Trichostrongylus colubr~~ormi.~ larvae on worm burdens acquired during grazing. Internutional Journal .for Purasitolcq~ 19: 177-I 8 I GIBSON T. E. & EVERETTG. 1967. The ecology of the freeliving stages _ of Trichostrongylus colubrjformis. Parositolog_v 57: 533-547. GIBSON T. E. & EVERETTG. 1972. The ecology of the freeliving stages of Ostertngia circumcinctu. Parasitology 64: 451460. GIBSON T. E. & PARPITT J. W. 1973. The development of resistance to Trichostrongylus colubr(fbrmis by lambs under conditions of continuous infection. Reseurch in Veterinq Science 15: 220-223. GIBSONT. E. & PARFITTJ. W. 1976. The effect ofanthelmintic treatment on the development of resistance to Ostertugia circumcincta in sheep. Journal of Compurative Puthology 86: 547-555. GIBSON T. E. & WHITEHEADJ. D. 1981. Changes in the worm burden of lambs under continuous infection with Ostertagia circumcincta. British Veterinary Journal 137: 192-195. GRENFELL B. T., SMITH G. & ANDERSON R. M. 1986. Maximum-likelihood estimates of the mortality and migration rates of the infective larvae of Ostertagia ostertagi and Cooperia oncophora. Parasitology 92: 643% 652. GRENFELL B. T., SMITH G. & ANDERSON R. M. 1987a. The regulation of Ostertagia ostertagi populations in calves: the effect of past and current experience of infection on proportional establishment and parasite survival. Parasitology 95: 363-372. GRENFELL B. T., SMITH G. & ANDERSON R. M. 1987b. A mathematical model of the population biology of

D. M. LEATHWICK. N. D. BARLOW and A. VLASSOFF

798

Ostertugia ostertugi in calves and yearlings. Puravitolog~ 95: 389406. HASHMI H. A. & CONNAN R. M. 1989. Biological control of ruminant trichostrongylids by Arthrohrys oligo.ypora, a predacious fungus. Parasitology Today 5: 28-30. HONG C., MICHEL J. F. & LANCASTERM. B. 1986. Populations of Ostertagia circumcincta in lambs following a single infection. International Journal,for Parasitology 16: 63-67. KETTLE P. R., VLASSOPF A., LUKIES J. M.. AYLIN~I J. M. & MCMURTRY L. W. 1981. A survey of nematode control measures used by sheep farmers and of anthelmintic resistance on their farms Part 1. North Island and the Nelson regions of South Island. Nrbc, Zealand Veterinur? Journal

29: 81-83.

KETTLE P. R., VLASSOI.FA., AYLING J. M.. MCMURTRY L. W.. SMITH S. J. & WATSOPIA. J. 1982. A survey of nematode control measures used by sheep farmers and of anthelmintic resistance on their farms Part 2. South Island excluding the Nelson region. New Z&and Vrte~inar~ Journal 30: 79-8 I, MARTIN R. R., BEVERIXE I., PVLLMAI\IA. L. & BROWNT. H. 1990. A modified technique for the estimation of infective nematode larvae present on pasture, and its application in the field under South Australian conditions. Vererinury Parasitology 37: 133-143. MASON P. 1989. Drench resistance in Otago and Southlandan update. Surveillance 16: 19-20. MCANULTY R. W.. CLARK V. R. & SYKES A. R. 1982. The effect of clean pasture and anthelmintic frequency on growth rates of lambs on irrigated pasture. Proceedings oj the New ZeulundSociet_v

ofAnimal

Production

42: 187-I 88.

MCK~NNA P. B. 1981. The diagnostic value and interpretation of faecal egg counts in sheep. N~M, Zealand Vererinury Journal 29: 129-l 32. MCKENNA P. B. 1989a. Anthelmintic resistance in the southern North Island. Surveilkmce 16: 15-17. MCKENNA P. B. 1989b. Multigeneric resistance to benzimidazole anthelmintics in sheep. Nero Zc&uzd Vererinury Journul37:

62-64.

PATON G., THOMAS R. J. & WALLER P. J. 1984. A prediction model for parasitic gastro-enteritis in lambs. Internutional Journal,for

Parasitology

14: 439445.

PATO~ G. 1987. Gastro-intestinal nematode infection in lambs-a model based on climatic indices for forecasting peak pasture larval contamination. International Journul of Biometeorology31:

175-181.

RACTLIPFF.L. H., TAYLORH. M., WHITLO(.KJ. H. & LYNNW. R. 1969. Systems analysis of a host-parasite interaction. Parasitology

59: 649-661.

REES G. 1950. Observations on the vertical migrations of the third-stage larva of Huemonchus contorfus (Rud.) on experimental plots of Lolium perenne S24. in relation to meteorological and micrometeorological factors. Prrrasitology

40: 127- 143.

ROBERTS M. G. & GRENPELL B. 7.

1991. The population dynamics of nematode infections of ruminants: periodic perturbations as a model for management. IMA Journalqf Mathematics

Applied in Medicine

& Biology 8: 83-93.

Rose J. H. 1961. Some observations on the free-living of Osrertagiu ostertagi, a stomach worm of Porrrsitology

51: 295-307.

stages cattle.

ROSE J. H. 1963. Observations on the free-living stages of the stomach worm Haemonchus c’ontortus. Parusitology 3: 46948 I. SALIH N. E. & GRAINGPR J. N. R. 1982. The effect of constant and changing temperatures on the development of the eggs and larvae of Osterfugia circumcinctu. Journal of Thermal Biology 7: 35-38.

SILANGWAS. M. & TODD A. C. 1964. Vertical migration of trichostrongylid larvae on grasses. Journul of Parusitolog~~ 50: 278-285. SMITH G., GREI\I~ELL B. T. & ANDERSON R. M. 1987. The

regulation of Osterfagiu osrerlugi populations in calves. density-dependent control of fecundity. Parasitology 95: 373-388. SMITH G. 1988. The population

biology of the parasitic stages of Haemonchus conlorfus. Parusitology 96: 185-195. STEELJ. W., SYMONSL. E. A. &JONES W. 0. 1980. Effects of level of larval intake on the productivity and physiological and metabolic responses of lambs infected with Trichostrongylus Agricuimral

colubriformis.

Austrulian

Journal

o/

Rrserrrch 31: 821-838.

SYKES A. R. & POPPI D. P. 1982. Effects of parasitism on metabolism in sheep. In: Control of Internal Pura.rite.c in Sheep (Edited by Ross A. D.), pp. 25-36. Animal Industries Workshop, July 1982. Lincoln College, New Zealand. THOMASR. J. 1974. The role of climate in the epidemiology of nematode parasitism in ruminants. In: The Eficts o/ Meteorological Fuctor.s upon Purasitrs (Edited by TAYLOR A. E. R. & MULL~R R.), pp. 13-32. Symposia ofthe British Society for Parasitology. Vol. 12. Blackwell Scientific Publications, London. VLASSO~~ A. & BRUNSDOX R. V. 1981. Control of gastrointestinal nematodes: advantages of a preventive over a protective anthelmintic drenching programme for lambs on pasture. Ne,c Zeulond Journul of E.~pcrimcnrtrl Agriculture

9: 221-225.

VLASSOP~A. 1982. Biology and population dynamics of the free-living stages of gastrointestinal nematodes of sheep. In: Control of Intrrnul Parasires in Sheep (Edited by Ross A. D.), pp. 1 l-20. Animal Industries Workshop. July 1982, Lincoln College, New Zealand. WALLER P. J., DOBSON R. J., DONALD A. D. & 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. Imernationul Journalfor Parasitology 11: 359-367. WALLER P. J. & THOMASR. J. 198 1. The natural regulation of Trichostrongylus spp. populations in young grazing sheep. Veterinary

Parasitology

9: 47-55.

WEST D. M., POMROY W. E., PROBER-~A. D. & CHARLESTON

W. A. G. 1989. Multigeneric resistance to benzimidazole anthelmintics in four sheep flocks. Net