The control of gastrointestinal sheep nematodes with tanniferous forage plants

Abstract

Infections with gastrointestinal nematodes (GIN) represent a major constraint in sheep husbandry. For many years, the control of these parasites has solely relied on the repeated use of synthetic anthelmintics. However, the emergence of resistant GIN populations and the increasing concern of consumers for drug residues in animal products have provided a strong impetus towards the development of alternative strategies to control GIN. Amongst those, the administration of tanniferous fodder plants to infected animals received prime attention in the last decade, and although a considerable body of knowledge on this strategy has been accumulated, many questions remain to be answered. In sheep and goats, the anthelmintic effects observed in response to tanniferous fodder administration are believed to be associated to condensed tannins (CTs), contained in the plants. Chemically these molecules belong to the polyphenols and are expressed by a range of fodder plants together with other secondary metabolites. Across experiments, the most consistently observed anthelmintic effect is a reduction in parasite egg output (as measured by egg counts per gram faeces – FEC). Reductions in adult or juvenile GIN as well as decreases in female worm fecundity have also been reported but were less consistent, varying with the administered tanniferous plant species, the nematode species and also the host species (i.e. sheep or goat). The mechanism of CT-action on GIN is unknown, but it has been hypothesised that the high binding capacity of CT-molecules with protein might be involved in causing the effects. The investigation of the different sources of variability associated with the antiparasitic effects represents the major challenge in this area and some aspects of this research are covered in the present thesis. In a first feeding experiment, we investigated direct anthelmintic effects associated with the feeding of fresh herbaceous tanniferous forages and chicory against established populations of Haemonchus contortus and Cooperia curticei in lambs. Twenty-four parasite naive lambs were inoculated with a single dose of infective larvae of these parasites 27 days prior to the start of the feeding experiment. Lambs were individually fed with either chicory (Cichorium intybus), birdsfoot trefoil (Lotus corniculatus), sainfoin (Onobrychis viciifolia) or a ryegrass / lucerne mixture (control) for 17 days. Animals where then united to one flock and subjected to control feeding for another 11 days to test the sustainability of potentially lowered egg excretion generated by tanniferous forage feeding. When compared to the control feed, the administration of all tanniferous forages was associated with significant reductions of total daily faecal egg output specific to H. contortus (chicory: by 89 %; birdsfoot trefoil: by 63 %; sainfoin: by 63 %; all tests P < 0.05) and a tendency of reduced H. contortus worm burden (chicory: by 15 %; birdsfoot trefoil: by 49 % and sainfoin: by 35 %). Irrespective of the experimental fodder, no anthelmintic effects were found against C. curticei. Cessation of CT-feeding followed by non-CT control feeding did not result in a re-emergence of FEC based on faecal dry matter (FECDM) in any group, suggesting that egg output reductions are sustainable. The moderate to high concentrations of CT in birdsfoot trefoil (15.2 g CTs kg-1 DM) and sainfoin (26.1 g CTs kg-1 DM) were compatible with the hypothesis that the antiparasitic effect of these forages is caused by their content of condensed tannins. For chicory (3 g CTs kg-1 DM), however, other secondary metabolites need to be considered. Overall, birdsfoot trefoil and sainfoin seem promising candidates to contribute to the control of H. contortus, not only by mitigating parasite related health disturbances of the host but also by a sustained reduction of pasture contamination. Experiment two was carried out using a similar set-up as in experiment one (i.e., established populations of H. contortus and C. curticei, 16 days of experimental feeding). The objective of this second study was to examine the anthelmintic effect of dried and ensiled sainfoin (O. viciifolia). Twenty-four parasite naive lambs were inoculated with a single dose of infective larvae of the nematodes 28 days prior to the start of the feeding experiment. Groups A and B received sainfoin hay (61 g CTs kg-1 DM) or control hay (1 g CTs kg-1 DM) for 16 days. Groups C and D were fed on sainfoin silage (42 g CTs kg-1 DM) or control silage (1 g CTs kg-1 DM) for the same period. Feeds were offered ad libitum and, on the basis of daily refusals, were supplemented with concentrate in order to make them isonitrogenous and isoenergetic. The consumption of conserved sainfoin was associated with a reduction of adult H. contortus (by 47 % in the case of hay, P < 0.05; by 49 % in the case of silage, P = 0.075), but had little effect on adult C. curticei. Compared to the controls, H. contortus specific FECDM was reduced by 58 % (P < 0.01) in the sainfoin hay group and by 48 % (P = 0.075) in the sainfoin silage group. For both sainfoin feeds FECDM specific to C. curticei were significantly decreased when compared to the control feeds (hay by 81 % and silage by 74 %, both tests P < 0.001). The data of this study suggest that different mechanisms were responsible for the reduction in FECDM in response to feeding tanniferous fodder. For H. contortus the decrease seemed to be due to a nematocidal effect towards adult H. contortus. In contrast, for C. curticei the reduction in FECDM appeared to be a result of a reduced per capita fecundity. For both, hay and silage, an antiparasitic effect could be shown, offering promising perspectives for the use of conserved tanniferous fodder as a component of GIN-control. The aim of the third study was to investigate the anthelmintic effect of sainfoin silage fed as a sole diet on a mixed GIN-population in periparturient ewes in an on-farm setting. Thirty-three ewes with FEC > 300 were divided into two groups of 16 (sainfoin sialge) and 17 (ryegrass / clover silage; control) animals and fed on the respective feeds for twenty-five days. The GIN-population predominantly consisted of H. contortus (~ 50 %) and Trichostrongylus colubriformis (~ 35 %). After ten days of consecutive sainfoin silage feeding, FECDM was reduced by 60 % (P < 0.01) when compared to the control fed animals. FECDM of the sainfoin fed group consistently remained lower until the end of the study compared to the control. The area under the curve (AUC) based on FECDM, calculated for the entire experimental period was lowered by 32 % in the sainfoin group but this reduction was not significant (P = 0.17). When the AUC was calculated for the period following FECDM reduction in the sainfoin group (i.e. day 10-24) only, the reduction was 65 % (P = 0.09). The results from this study confirm some favourable antiparasitic effects associated with the consumption of sainfoin silage in naturally infected periparturient ewes. The potential impact of this effect on the epidemiology of trichostrongylidosis needs to be critically evaluated. In conclusion, our results suggest that the antiparasitic effects of tanniferous forages in general are achieved at lower CT-levels in the abomasum than in the small intestine and therefore would rather be organ dependent than GIN-species related. It has furthermore been shown that conservation of tanniferous fodder plants does not alleviate the anthelmintic effects and therefore offers exciting opportunities with respect to centralized production, sale, storage and an extended administration independent of the season. To date, however, the approach of tanniferous forage administration cannot be expected to provide satisfactory sustainable control of GIN. The combination with other alternative strategies in the sense of an integrated approach of GIN-control might be promising in terms of producing additive effects. Until rational integrative control approaches are available, the complete abandonment of synthetic anthelmintics is not sensible. However, in view of the widespread resistance of GIN against these drugs their economical and carefully targeted use is of vital importance until integrated alternative parasite control strategies are available.