Parasites, animal production and sustainable development.

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

Population dynamics of Trichostrongylus colubriformis in sheep: the effect of infection rate on the establishment of infective larvae and parasite fecundity.

The establishment of Trichostrongylus colubriformis was estimated in helminthologically naive 20-week-old Merino sheep given third stage infective larvae (L3) at rates of 2000, 632 or 200 L3 per day, 5 days per week. After varying periods of continuous L3 intake, a levamisole-susceptible strain of T. colubriformis was replaced with a highly resistant strain for 1 week. The animals were then treated with levamisole to remove the susceptible population, and establishment of the cohort of resistant worms was estimated. In previously uninfected sheep, approximately 65% of the L3 given in the first week became established as adults. This fell to low levels (less than 5%) after 7, 10 and 14 weeks of continuous L3 intake for the high, medium and low infection rates, respectively. At the low infection rate, establishment remained at maximum levels for the first 4 weeks, but then fell at a rate similar to that observed for the higher infection rates. This implied that a threshold of worm exposure was required before resistance to establishment developed. Parasite egg production, expressed as eggs per gram of faeces, was proportional to infection rate and is explained by higher worm burdens occurring at high infection rates. However, estimates of fecundity in eggs per female per day showed the opposite relationship with rate of infection. Fecundity stayed high (approximately 600) for 5 weeks at the low infection rate but only maintained this level for 3 weeks and 1 week at the medium and high rates, respectively. This suggests that fecundity, like establishment, was similarly affected at threshold levels of immunological recognition.

Population dynamics of Trichostrongylus colubriformis in sheep: the effect of host age on the establishment of infective larvae.

Sheep, reared worm-free in pens and aged 12-36 weeks, were infected each weekday with 2000 infective T. colubriformis larvae (L3). Establishment was measured at various times during the course of infection and the rate of development of resistance to new infection was found to be faster in older than in younger hosts. In addition arrested development at the exsheathed L3 stage was found to be less marked in older hosts. Sheep which had experienced natural infection on pasture up to 20 weeks of age before exposure, in pens, to the same experimental infections as their worm-free counterparts showed similar immune responses. However, at 36 weeks of age, pasture-reared sheep had acquired a high level of resistance to infection with T. colubriformis.

Population dynamics of Trichostrongylus colubriformis in sheep: the effect of infection rate on loss of adult parasites.

Rejection of adult T. colubriformis was examined in lambs given 2000, 1124, 632 or 200 L3 day-1, 5 days per week for up to 20 weeks. Rejection of adults began at approximately the same time for the first three infection rates, and took about 9 weeks to complete. Approximately 20% of adults were rejected by week 10 of infection at the higher infection rates and it was estimated that rejection commenced at about week 7. This coincided with a decline in establishment of larvae to about 1%. For the low infection rate, there was a delay of about 5 weeks before adult worm rejection commenced and reached equivalent levels to those observed at the higher rates. This delay also coincided with an estimated 5-week delay in larval establishment declining to 1% at the low rate.

Population dynamics of Trichostrongylus colubriformis in sheep: model to predict the worm population over time as a function of infection rate and host age.

The developing immunity of sheep to Trichostrongylus colubriformis infections was described by a mathematical function. The rate of adult establishment was assumed to be a measure of the host's acquired immunity to this parasite. Prediction of establishment from infection rate and host age was used to estimate worm burden, worm rejection and arrested development.

Changes in anthelmintic resistance status of Haemonchus contortus and Trichostrongylus colubriformis exposed to different anthelmintic selection pressures in grazing sheep.

This experiment was designed to study, over a 5-year-period, the effect of different frequencies of treatment with three different anthelmintic groups, namely, benzimidazoles, levamisole and ivermectin, and different frequencies of alternation between them, on existing levels of anthelmintic resistance in the nematode parasites Haemonchus contortus and Trichostrongylus colubriformis of grazing sheep. No evidence of ivermectin resistance emerged, even in suppressively treated groups. Likewise, H. contortus failed to develop resistance to levamisole under a similar selection regimen. Thiabendazole was shown to select positively against levamisole resistance in T. colubriformis resulting in significantly greater susceptibility to this drug than for the natural reversion which occurred in the untreated control. There was no evidence that an anthelmintic treatment combined with a movement of sheep to pastures of low infectivity selected more rapidly for resistance than where the same number of treatments were given to set-stocked sheep. Rotation between anthelmintic groups at yearly intervals appeared to be more beneficial in delaying resistance than rotation of drugs with each treatment.

Effects of helminth infection on the pre-weaning production of ewes and lambs: comparison between safe and contaminated pasture.

Comparison was made of the performances of cross-bred ewes and their lambs on pastures of low helminth infectivity ("safe" pastures) or contaminated pastures and at high or low stocking rates. Ewes grazing the safe, but not the contaminated, pastures were given a single pre-lambing drench. The largest difference in parasite infection between treatments was the level of exposure of sheep to Trichostrongylus spp, which was negligible on the safe pastures. The effects of parasite control on lamb growth were significant only in twins during the last 2 months before weaning. However, 22% of lambs on contaminated plots became soiled in the breech area and 38% were flystruck, compared with 8% and 10% respectively for lambs on the safe pastures. Ewe bodyweight gains were greater at low than at high stocking rate and were not affected by the parasite control treatments; differences in breech soiling and fly strike were similar to those in the lambs. Most importantly the parasite treatment produced a highly significant effect on ewe fleece weight at weaning. Ewes drenched and lambing on the safe pastures produced an extra 0.43 kg of wool, calculated to represent an increase of at least 40% during this period at the low-level of parasitic infection.

Effects of helminth infection on the pre-weaning production of ewes and lambs: evaluation of pre- and post-lambing drenching and provision of safe lambing pasture.

The pre-weaning production of ewes and lambs in spring on pastures grazed during the previous autumn and early winter by either weaner sheep, adult sheep, or cattle was investigated together with estimating the benefits of pre- and post-lambing drenches to ewes. These treatments were compared with one in which parasitism was uncontrolled in ewes lambing on pastures grazed previously by untreated weaner sheep, and another where parasitism was suppressed by 2-weekly drenching of the weaner sheep and also of the ewes and their lambs. Prior grazing by cattle effectively eliminated infection of pastures with intestinal Trichostrongylus and Nematodirus spp, but less so for Ostertagia spp. Worthwhile reductions in contamination were also achieved by grazing by adult sheep compared with grazing by undrenched weaners. Despite differences in the parasitological status of the pastures, there were no indications that pre-weaning growth rates of lambs were affected. However, wool growth in ewes was reduced by 10 to 20% by parasite infection. Wool growth of ewes on pastures grazed by cattle during the pre-experimental period exceeded that on any other treatment, and was significantly greater than that of ewes on pastures grazed by undrenched weaners. There was no production benefit in giving a pre-lambing drench to ewes on plots contaminated by weaners, or in giving the additional post-lambing drench to ewes grazing on plots contaminated by weaners, adult sheep or cattle.

A genetic model describing the evolution of levamisole resistance in Trichostrongylus colubriformis, a nematode parasite of sheep.

Data from 21 generations of selection on a levamisole-resistant strain of Trichostrongylus colubriformis, either exposed to selection with the anthelmintics levamisole (LEV) or thiabendazole (TBZ), or unexposed, were used to fit a genetic model describing the evolution of LEV resistance in this parasite species. A statistical model describing the dose-response relationship for a mixed population of susceptible and resistant parasite eggs exposed to anthelmintic was fitted to egg-hatch assay data for each generation and for each selection regimen. Estimated parameters from the statistical model provided the input for the genetic model from which were obtained estimates of the relative fitness of susceptible and resistant genotypes under each selection regimen. The experimental data and the genetic models both indicated that, in this parasite strain, LEV resistance was determined by a single dominant gene, and that TBZ selects for LEV susceptibility. A variety of drug alternation programmes was simulated for this genetic system. The programme that minimized the development of LEV resistance involved alternating the drugs (LEV and TBZ) between each worm generation.

An egg-hatch assay for resistance to levamisole in trichostrongyloid nematode parasites.

An in vitro technique is described for detecting resistance of nematodes to the anthelmintic levamisole hydrochloride. Samples of eggs are developed under controlled temperature conditions until just prior to the commencement of hatching. They are then exposed to different concentrations of the drug and, when hatching is almost complete, the test samples are killed and preserved. The proportion of unhatched eggs at each drug concentration can then be counted at leisure. Provided a suitable range of drug concentrations is chosen for each test isolate, this assay provides results which may be satisfactorily fitted to a log-concentration-probit regression model. Comparisons with in vivo anthelmintic assays have shown that the technique provides an accurate reflection of the resistance status of parasite populations.

New methods of drug application for control of helminths.

Several new ways have been developed of delivering anthelmintics to ruminants aimed particularly at reducing labour. For single doses, these include a semi-automatic rumen injector for giving insoluble drugs to cattle more conveniently and efficiently than by oral dosing, and the dermal application of levamisole which is, however, subject to seasonal variation in absorption. Sustained administration offers potentially a high level of preventive control but carries a greater risk of developing drug resistance. Even with the best available methods of group administration in feed supplements or drinking water, there remains some uncontrollable variation in individual intake. Intraruminal sustained release devices largely overcome this problem and constitute the most important new technology. They are represented at present by the commercially successful morantel sustained release bolus, and the more versatile Laby capsule which is under development for anthelmintic delivery. Other new applications include the possible development of synergists, potentiators and drug combinations, the special features of drugs which bind strongly to plasma proteins, and the new possibilities offered by a drug highly effective against all stages of Fasciola hepatica. In the general approach to anthelmintic application in helminth control, there have been advances in knowledge of helminth population biology which can lead to better timing of strategic dosing programs, which show that single treatments can have persistent benefits without a simultaneous reduction in infection rate, and which question the conventional view that control schemes require the treatment of all animals in the group.

Inhibited development of Ostertagia ostertagi in Australia related to survival over summer in the host or on pasture.

During autumn and winter, separate pasture plots were seeded with Ostertagia ostertagi eggs produced by worms which had persisted in the host over summer as inhibited larvae, or which had developed directly from larvae acquired from pasture in late summer. Successive groups of parasite-free calves grazed the plots in spring for 14 days at 4-week intervals and were killed for worm counts 14 days after removal from pasture. The proportion of inhibited early 4th-stage larvae was substantially greater in calves which grazed the plot carrying the progeny of previously inhibited worms. This finding is more easily reconciled with differential survival on pasture over spring and summer of inhibiting and non-inhibiting morphs, than with the concept of a physiological switch from inhibiting to non-inhibiting behaviour in individual larvae.

Inhibited development of Ostertagia ostertagi in relation to production systems for cattle.

On a coastal farm in New South Wales where beef and dairy cattle production was carried on side-by-side, separate pasture plots were contaminated with eggs of Ostertagia ostertagi by calves from each production system in autumn, winter or spring. Successive groups of parasite-free tracer calves grazed on the plots for 14 days at 4-week intervals and were then killed for worm counts 14 days after removal from pasture. On all plots, the proportion of inhibited early 4th-stage larvae in tracer calves reached a maximum in spring, and was consistently and very significantly higher in calves which grazed plots contaminated with O. ostertagi of beef cattle origin. Factors which may be responsible for this difference between beef and dairy cattle populations of O. ostertagi are discussed.

Inhibition of development of Ostertagia ostertagi--effect of temperature on the infective larval stage.

Populations of Ostertagia ostertagi established from fresh larvae and from larvae stored at 4 degrees C for up to 12 weeks contained about 10% inhibited early 4th-stage larvae. This value rose to 21% after 16 weeks, due to an increase in numbers of inhibited larvae while adult numbers remained unchanged. Storage at 15 degrees C had no effect. In the case of larvae stored at 4 degrees C for 8 weeks, increasing the larval dose to 90000 had no significant effect on the proportion of the dose which was inhibited. The response to low temperature storage was much weaker than in previously reported studies on British populations, which accords with our earlier conclusion that low temperature cannot be the effective stimulus for inhibition in Australia.