Grazing behavior of horses on pasture: Predisposition to strongylid infection?

Refereed

GRAZING BEHAVIOR OF HORSES ON PASTURE: PREDISPOSITION TO STRONGYLID INFECTION? D. L. Medica, MS; M. J. Hanaway, BS; S. L. Ralston, VMD, PhD; M. V. K. Sukhdeo, PhD

SUMMARY

This study was designed to determine how the behaviors of horses on a fenced-in pasture in the northeastern United States may contribute to infection by Strongylus vulgaris. The infective stages of strongylid parasites of horses develop in the feces, and they must be ingested for infection to occur. Domestic horses are thought to be coprophobic, and to avoid grazing in areas contaminated with their feces, l'z In this study, nine Standardbred colts were observed on two pastures three times a week during two observation periods (January, 1995 and February through mid-March, 1995). Nine adult Standardbred mares and geldings were also observed on the same pastures during one observation period from April through midMay, 1995. On each pasture, the roughs (areas of group defecation associated with long grass), lawns (short-cropped grass) and bare areas (where hay was ted in racks), were mapped. Grazing occurred equally on roughs, lawns, and bare patches of the pasture in two of the three observation periods (January and April/May). In the February/midMarch observation period, most of the grazing activity occurred on the bare areas, where hay was provided, but there was still grazing in the roughs. Defecation and urination activities occurred at similar frequencies in all Authors' address: Department of Animal Sciences, Rutgers, The State University of New Jersey, New Brunswick, New Jersey, 08903. Acknowledgments:The authors wish to thank Melanie Chapman and Dr. Thomas Klei for providing the Strongylus vulgaris larvae used in this study. The authors also wish to thank two anonymous reviewers and Anne Bansemir for helpful comments on the manuscript. This study was supported by the Equine Special Initiative Fund (SES) of the State of New Jersey and is part of the Journal Series of the New Jersey State Agricultural Experiment Station (D-06188-3-96) supported by state and Hatch funds. Volume 16, Number 10, 1996

areas of the pastures during all observation periods. These data suggest that horses kept at high grazing intensities will graze near feces in the roughs, and will defecate in the "grazing" areas. It was also determined that the infective larvae of S. vulgaris are attracted to horse feces, but show no responses to grass, in laboratory chemical migration assays. These data suggest that the parasites may not migrate from the feces to the grass as part of their transmission strategy as previously reported. Thus, parasite infection may be occurring when horses graze in the roughs or near feces in the lawns and bare areas, and pasture management strategies for controlling these parasites may be most effective if focused on reducing the infective larvae present on the pasture.

INTRODUCTION

A characteristic pattern observed on fields grazed by horses includes areas of group defecation (roughs) where the grass is long and lush, but rarely consumed, and areas of short-cropped grass (grazing area or lawns). 1'2 The infective stages of most gastrointestinal parasites of the horse, including the large and small strongyles, are shed with the feces and must be ingested for infection to occur. The avoidance of grazing in the roughs is thought to have evolved as part of a behavioral strategy in the domestic horse to avoid grazing near feces, reducing the chance of ingesting parasites. 1 Thus, an increase in grazing intensity (number of horses/unit land) results in larger defecation areas and this reduces the nutritive value of the pasture. 3 Loss of nutritive pasture is extremely important in areas like the northeastern United States where available farm land is becoming scarce. For example, in New Jersey, farm 421

land has decreased by 7.5%, while horse numbers escalated by 26.8% in the last ten years. 4 Increased grazing intensity on horse pastures may force the animals to graze in the roughsfl and grazing near feces increases the potential for parasite infection, s Contemporary methods of controlling gastrointestinal parasites are aimed at the adult stages in the intestine of the horse, and involve routine medication, most often with ivermectins | or strongid9 However, the development of resistance to anthelmintics, including ivermectin | has been reported in several roundworm parasites of domestic animals. 8,7,8,9,1~ In addition, there is concern about the ecotoxicity ofendectocides such as the avermectins. These drugs and their residues are excreted in the feces of the horse, and can be lethal to organisms responsible for fecal breakdown on the pasturefl 1 Reduced fecal degradation rates will also increase the size of the roughs, and contribute to further reduction in grazing area. Thus, there is a need for the development of more natural, sustainable antiparasite strategies, which are focused on the control of the infective stages on the pasture, and preclude possible resistance or ecotoxicity, la Current methods to control the infective stages of parasites on the pasture include manual removal of feces 1a and rotational grazing of horses and sheep on the same pastures. 14,1s Infection levels of Strongylus spp. in the horse will decrease with both of these methods. However, a potential complication of rotational grazing of horses with sheep is the increase in infection levels of Trichostrongylus axei (a parasite of sheep and horses) in the horse? 5 Some exciting new strategies for parasite control include the use of biological agents such as nematophagous fungi, to control larvae on the pasture. 1a'17 However, understanding the biology of both parasite and host is essential in the development of effective pasture management strategies and in the implementation of novel parasite control strategies aimed at the infective stages on the pasture. This study investigates the behavior of both horse and parasite, to determine how horses might be infected with strongylid parasites on pasture in the northeastern United States.

MATERIALS AND METHODS Weather conditions All observations were made from December, 1994 through May, 1995 at Cook College, Rutgers University, located in central New Jersey. Mean daily temperatures and precipitation during all observation periods were obtained from the Rutgers Cooperative Extension weather service located at Cook College (New Brunswick, NJ).

Horse pastures Two pastures grazed by horses (field l: 96,000 sq. ft.; 422

field 2:83,000 sq. ft.) were surveyed every two months at the beginning of each observation period (December, 1994, February and April, 1995), and the location of the roughs, lawns, and bare areas of each field were mapped. Two or more fecal piles within 18 inches of each other associated with areas of long grass were considered roughs. Areas with no grass cover were considered bare, and the rest of the field (short-cropped grass) was considered to be lawn. Hay was provided to the horses free choice in feeders in the bare areas. There were also large three-sided shelters in the bare areas of each pasture.

Horse behaviors The grazing patterns of horses on the pastures were examined to determine if they actively avoid grazing near their feces. Nine yearling colts (December through midMarch) and nine ~idult geldings and mares 20 years of age and older (April through mid-May) were observed on the two pastures (field 1:5 horses, field 2:4 horses during all observation periods). The fields were empty for two weeks at the end of March before the adult horses were put on the pasture. The time of day of the behavioral observations were randomized, and all observations took place between 9 AM and 4 PM. All horses were kept in stalls overnight. The location of each horse, and its behavior, on the field were recorded at live-minute intervals for one half hour, three times a week for the duration of the study. The behaviors measured were: (a) grazing (head to ground, manipulating forage or ground with lips and chewing), (b) urination, (c) defecation, (d) playing (rearing, bucking, kicking at another horse), (e) standing still, not grazing, (1") running, and (g) roiling. /

Parasite behavior To determine whether the infective larvae of" S. vul/ garis migrate away from feces and towards grass (resulting in the parasites moving onto herbage), the response of infective larvae to various compounds were measured. Third stage infective larvae ofS. vuIgaris were provided by Dr. Tom Klei (Louisiana State University). The larvae had been obtained from the feces of a pony with a monospecific infection ofS. vulgaris and isolated by the method of Farrar and Klei] a Infective larvae were stored at 4~ until use. Extracts of horse feces, grass, and soil were prepared by mixing 10g of each substance in 10 ml water, storing each mixture at 4~ for 48 hr, and removing the liquid portions for use in the assay. Parasite responses to horse urine (100% solution) and extracts of horse feces, soil and grass were measured in a chemical gradient migration assay (Fig. 1), using 2% agar in a 60X 15 mm petri dish (modified from Sukhdeo et al. 19). Extracts of feces, grass, or soil were placed in a well on one side of the assay chamber, with water added to the other side. Water was placed in the wells on both sides of control chambers. The solutions were allowed to diffuse into the agar for 48 hrs, forming a lineal" JOURNAL OF EQUINE VETERINARY SCIENCE

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Data analysis All data were analyzed using Chi-square analysis:

)(2= (observed value - expected value) 2 expected value Expected values for the distribution of horse behaviors on the pasture were based on the percentage of the pasture that was comprised of lawn, rough, or bare area (e.g., if lawn comprised 20% of total pasture area, the expected value for any behavior in this region was 20%). Expected values for parasite behavior were based on the percentage of worms located in each 0.5 cm region of the control chambers, to account for random parasite movement. Significance was set at the 5% level.

RESULTS Weather conditions This study was conducted during an unseasonably mild winter for central New Jersey, with a single snowVolume 16, Number 10, 1996

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Horse pastures The fields surveyed in this study were composed primarily of lawns, with smaller areas of roughs and bare areas (Fig. 3). The percentage of lawn, rough, and bare areas on both pastures were comparable. The results shown ior horse behaviors on both fields in each observation Period are pooled. Horse behaviors Although seven behaviors were observed in this study, only the results for grazing, urination and defecation are shown here. There were no consistent patterns, relative to their occurrence in different regions of the field, in the playing, standing, running and rolling behaviors of the horses. There was no difference in the relative amount of time the horses spent in the lawns, roughs, and bare areas except during the Feb./Mar. observation period, where 423

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they spent more time in the bare areas (where shelter and hay were provided) than expected. The grazing behavior of both young (January) and old (April/mid-May) horses was random (P > 0.05), they grazed equally on the entire pasture (Fig. 4.). Grazing behavior of the yearling horses during the second observation period (Feb./Mar.) was not random, as there was more (P < 0.05) grazing in the bare areas than expected, though these horses grazed in the lawns and rough areas of the pasture as well (Fig. 4). Urination by the yearling and adult horses occurred rarely during the observation periods (2 to 9 times during each month-long observation period). Yearling horses urinated randomly on the entire pasture during both observation periods (January and Feb./Mar.), while the adults urinated only in the grazing areas (P<0.05) (Fig. 5). Defecation by both young and adult horses was also infrequent (4 to 7 incidences during each monthly observation period), but when observed, this behavior occurred randomly in all areas during all observation periods (Fig. 6). Parasite behavior The response ofS. vulgaris larvae to sUbstances present on horse pastures (soil, grass, and horse urine and feces) are shown in Figure 7. In control chambers, where water was 424

Figure 4. Grazing/behavior of yearling (January, Feb./ Mar.) and adult (April/May) horses (data from both pastures pooled). X2=RANDOM indicates that the behavior occurred randomly on the pasture (P>0.05) during the January and April/May observation periods. Grazing behavior during the Feb./Mar. observation period was nonrandom (P<0.05). placed in wells on both sides of the chamber, infective S. vulgaris larvae were found primarily in the first two regions surrounding the application zone. In chambers which contained soil or grass extracts as the experimental treatment, worm movement was random, and the distribution of the larvae was not different from that observed in the control chambers. In chambers which contained horse urine or feces extract as the treatment compound, most of the larvae were found at the treatment side of the chambers (P< 0.05).

DISCUSSION The transmission strategy ofS. vulgaris is thought toe. be similar to that of the other large and small (cyathostome) JOURNAL OF EQUINE VETERINARY SCIENCE

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Figure 6. Defecation b e h a v i o r of yearling (January, Feb./ Mar.) and adult (April/May) horses (data from both pastures pooled). Defecation b e h a v i o r w a s n o n - r a n d o m (P<0.05) during all o b s e r v a t i o n periods.

strongyles of horses, as well as to that of the roundworm parasites of other domestic herbivores. The infective stages of these parasites must migrate away from feces and onto grass as part of their transmission strategy because their hosts are thought to actively avoid grazing near their own feces. 2'2~ This "feces avoidance" behavior has been observed in sheep and cattle, which leave tufts of ungrazed grass around fecal pats, 1'2a and is thought to be especially well-developed in horses, which leave large areas of fecescontaminated pasture (roughs) essentially ungrazed. 1,2 Thus, to be ingested, the infective larvae of horse roundworms would have to move out of the roughs and onto the lawns (grazing areas) of the pasture. This was a distance of up to 20 ft. (from the center of the rough to the lawn) on the pastures used in this study; quite a considerable distance for a worm that is less than 1 mm in length. However, despite these obstacles, the parasites are very successful at transmission and, in the absence of intensive anthelmintic treatment, the prevalence of strongylid parasite infection in

domestic horses in the United States approaches 100%. zl Infective strongylid larvae can persist on pasture for months and thus can re-infect the horse even after the adult worms have been removed by anthelmintic treatment. 23 However, these infective stages are primarily found in the roughs, and grazing in the roughs may increase parasite infection levels. 5 Our data suggests that both yearling and adult horses at high grazing intensities ( 19,200 sq. It/horse in field 1; 20,750 sq. ft/horse in field 2) graze equally on the entire pasture, including in the roughs. If this is so, the formation of roughs may be due to increased forage growth due to the fertilizing effect of feces or to decreased total forage intake while grazing in these areas. The one exception to the random grazing pattern occurred in the yearlings during the February/March observation period. In this case, a large percentage of grazing was observed in the bare areas, possibly because the ground was snow covered, and hay and shelter were provided in these areas. Nevertheless, there was still some grazing observed in the roughs. In

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CONCLUSIONS

This study demonstrated that domestic horses, at high grazing intensities, may not be coprophobic, as previously thought. They will graze near feces, and defecate on the lawns where they graze. Strongylid parasites are not coprophobic either, and the infective stages may not migrate tar from horse feces on the pasture. Infective strongylid larvae are non feeding, and therefore have limited energy.2~ Migration out of the roughs could drain this limited energy and reduce the parasite's ability to infect the horse. Thus, it may be adaptive for these worms to employ a "sit and wait" strategy, staying in the roughs until a horse grazes near feces, and ingests them. At high grazing intensities, this could occur on all areas of the pasture. At lower stocking rates, transmission of strongylid parasites may occur primarily in the roughs. Thus, control strategies which are focused on reducing fecal contamination and the number of infective parasites in the roughs are appropriate. Such measures may include sustainable anti-parasite strategies such as pasture vacuuming and sweeping (to remove feces from the pasture), as well as appropriately timed single anthelmintic administration (to limit deleterious effects on feces-degrading organisms). 12,13

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Figure 7. Migration of Strongylus vulgaris larvae in response to chemical compounds. Larvae were placed in the center of the chamber (O). The treatment compound (trt) was present on one side of the chamber, water on the other. Positive numbers (+) denote attraction to compound, negative numbers (-) denote repulsion. The worms were aggregated (non-random, P<0.05) at the treatment end in urine and feces treatments, and were found in the center (near the application zone) of soil and grass treatments, and of the water control addition, yearling and adult horses defecated outside of the roughs, on both the lawns and bare areas. These data suggest that horses will graze in the roughs and defecate in the "grazing" areas. Thus, if horses graze and defecate in the same areas, the infective stron~ylid larvae on the pasture may not have to migrate out of the roughs to be ingested. This conclusion is supported by our data which suggests that infective S. vulgaris larvae may not migrate far away from feces before moving onto grass. In vitro behavioral assays demonstrate that they are not attracted to grass, and are not repelled by horse feces, contrary to the responses that would be expected if the larvae migrated out of the roughs to the lawns. Previous studies showing that strongylid larvae only move out of feces after rain, and then not further than 6 inches away from the feces, support our conclusions. 426

REFERENCES 1. Taylor EL: Grazing behavior and helmintic disease. Br J An Behav 1954;2:61-62. 2. Odberg FO, ,F'rancis-Smith K:Astudy on eliminative and grazing behaviour--the use of the field by captive horses. Equine Vet J 1976;8:147-149. 3. Odberg FO, Francis-Smith K: Studies on the formation of ungrazed eliminativeareas on fields used by horses. AppiAn Ethel 1977;3:27-34. / 4. NJ Census: Government iniormation home page. 19821992; http://govinfo,kerr.orst.edu/index.html. 5. Herd RP, Willardson KL: Seasonal distribution of infective strongyie larvae on horse pastures. Equine Vet J 1985;17:235237. 6. Drudge JH, Lyons ET, Tolliver SC: Benzimidazoleresistance of equine strongyles - - critical tests of six compounds against population B. Am J Vet Res 1979; 40:590-594. 7. French DD, Klei TR: Benzimidazole-resistant strongyle infections. A review of significance, occurrence, diagnosis, and control. Proc 29th Ann Conv AAEP 1983; 313-317. 8. van Wyk JA, Malan FS: Resistance of field strains of Haemonchus contortus to ivermectin, closantel, rafoxanide and the benzimidazoles in South Africa. Vet Rec 1988; 123:226-228. 9. Barger IA: Control of gastrointestinal nematodes in Australia in the 21st century. Vet Parasit 1993;46:23-31. 10. Shoop WL: Ivermectin resistance. Parasit Today 1993;9:154-159. 11. Herd RP, Stinner BR, Purrington FF: Dung dispersal and grazing area following treatment of horses with a single dose of !vermectin. Vet Parasit 1993; 48:229-240. 12. Herd RP: Endectocidal drugs: Ecological risks and counter-measures. Int J Parasit 1995;25:875-885. 13. Herd RP: Control strategies for ruminant and equine parasites to counter resistance, encystment, and ecotoxicity in the USA. Vet Parasit 1993;48:327-336. JOURNAL OF EQUINE VETERINARY SCIENCE

14. Eysker M, Jansen J, Wemmerhove R:AIternate grazing of horses and sheep as control for gastrointestinal helminthiasis in horses. Vet Parasit 1983; 13:273-280. 15. Eysker M, Jansen J, Mirck MH: Control of strongylosis in horses by alternate grazing of horses and sheep and some other aspects of the epidemiologyof Strongylidaeinfections. Vet Parasit 1986;19:103-115. 16. Grenvold J, Wolstrup J, Nansen P, Henriksen SA: Nematode-trapping fungi against parasitic cattle nematodes. Parasit Today 1993;9:137-140. 17. Bird J, Herd RP: Nematophagous fungi for the control of equine cyathostomes. Comp Cont Ed Pract Vet 1994;16:658665. 18. Farrar RG, Klei TR: In vitro development of Strongylus edentatus to the fourth larval stage with notes on Strongylus vulgaris and Strongylus equinus. J Parasit 1985;71 !489-499. 19. Sukhdeo MVK, Sukhdeo SC, Mettrick DF: Site-finding

behaviour of Fasciola hepatica (Trematoda), a parasitic flatworm. Behaviour 1987; 103:174-186. 20. Rogers WP, Sommerville RI: The infective stage of nematodes and its significance in parasitism. Adv Parasit 1963;1 : 109-177. 21. Austin SM: Large strongyles in horses. Comp Cont Ed Pract Vet 1994; 16:650-657. 22. Dohi H, Yamada A, Entsu S: Cattle feeding deterrents emitted from cattle feces. J Chem Ecol 1991 ;17:1197-1203. 23. Ogbourne CP: Survival on herbage plots of infective larvae of strongylid nematodes of the horse. J Helminthol 1973;47:9-16. 24. English AW: The epidemiology of equine strongylosis in southern Queensland. 2. The survival and migration of infective larvae on herbage. Aust Vet J 1979;55:306-309.

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