HELMINTHS OF THE WILD BOAR (SUS SCROFA L.) IN NATURAL AND BREEDING CONDITIONS

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1 Bull Vet Inst Pulawy 54, 6-66, 2 HELMINTHS OF THE WILD BOAR (SUS SCROFA L.) IN NATURAL AND BREEDING CONDITIONS MARCIN POPIOŁEK,2, DAMIAN KNECHT 3, JUSTYNA SZCZĘSNA-STAŚKIEWICZ, AND AGNIESZKA CZERWIŃSKA-ROŻAŁOW Institute of Biology, Deartment of Invertebrate Systematics and Ecology, Wroclaw University of Environmental and Life Sciences, 5 63 Wroclaw, Poland 2 Institute of Natural Sciences, Wroclaw University of Environmental and Life Sciences, Wroclaw, Poland 3 Institute of Animal Breeding, Wroclaw University of Environmental and Life Sciences, 5-63 Wroclaw, Poland marcin.oiolek@u.wroc.l Received for ublication January 2, 2 Abstract Comarative coroscoic studies on the occurrence of helminths in the wild boar included two grous of animals living under different conditions: one (A) - wild boar inhabiting a woodland area, another (B) wild boar from a free-range farm. Analysis of 42 samles of faeces revealed the occurrence of six nematode secies: Oesohagostomum s./globocehalus s., Metastrongylus s., Trichuris suis, Ascaris suum, Ascaros strongylina, and Physocehalus sexalatus. The revalence of infection was very high 97.2%, while the mean number of eggs was 34.3 ±88.6. The revalence was similar in the two grous: A=98.4% vs. B=96.3%. The mean number of eggs was higher in grou B (46.6 ±5.3; range -92) comared to A (8.3 ±7.2; -83). All the arasite taxa were found in each grou. The frequency of individual helminth taxa differed between the grous, but the differences were statistically significant only for Oesohagostomum s./globocehalus s. (χ 2 =4.34; df=; P=.37), Metastrongylus s. (χ 2 =8.3; df=2; P=.4), and A. suum (χ 2 =5.67; df=2; P=.). Key words: wild boar, Sus scrofa, helminths, breeding conditions, Poland. The wild boar (Sus scrofa L.) is now among the most abundant and economically imortant secies of the so called large wild animals in Poland. Its oulation abundance has shown a constant increasing tendency since 96 and the increase being faster than in other Euroean countries (2). Desite this, information on the arasite fauna of the native wild boar is still scanty and fragmentary. Tarczyński s aer was the first and still the most comrehensive ublication dealing with the helminth fauna of wild and domesticated suids (28). Gadomska (4) resented a quantitative and qualitative helminthological analysis of the wild boar oulation from the Kaminos National Park and the ark freerange farm. Only the latest aers by Pilarczyk et al. (23) and Winnicki et al. (3) deal with North-Western Poland. More data are to be found in Euroean literature. Publications by Pav et al. (22) and Antolova et al. () deal with the area of Czech Reublic and Slovakia, and by De-la-Muela et al. (5) and Fernandez-de-Mera et al. (8) Sain. In the Mediterranean region, the research on wild boar helminths were conducted in Italy (8), Croatia (24, 25), and Corsica (9, ). In France, the occurrence of wild boar arasites was studied by Humbert and Henry (6), in Germany by Barudzki et al. (2, 3) and Mennerich-Bunge et al. (9), in Hungary by Tacaks (27), in Iran by Eslami and Farsad Hamdi (7), and in Estonia - by Jarvis et al. (7). The Euroean research on wild boar helminths resulted in the list of 3 secies, encomassing flukes, taeworms, nematodes, and acanthocehalans as well as their larvae. The hitherto records from Poland, embracing 2 secies, oint to the necessity of further investigation of this articular host. The wild boar is an increasingly oular animal to breed in cativity. Profitability of both breeding and fattening deends mainly on the condition of the animals. Parasite-induced invasive diseases result in a decreased feed utilisation, feed losses, and rolonged fattening eriod. In farmed igs and wild boars such diseases are often resonsible for the absence of oestrus, small litters, and small viability of the rogeny. Hence studies on the arasite secies comosition characteristic for the animal environment are essential. Similarly, an attention should be aid to the athogenicity of the arasite assemblage, and adequate measures, which can limit the sread and invasiveness of the arasites, should be taken. Besides, cative-bred wild boar may resent a

2 62 otential zoonotic danger for humans and animals (, 8, 26, 32). This study aims at udating the secies comosition of wild boar s endoarasites and determining the level of infection in a cative-bred versus wild oulation. Material and Methods Study area. The study area is a art of Lubin Forest Division (Lower Silesia, SW Poland), with the area of ca. 64, ha, with 9,258 ha of arable land, and 8, ha of forest. The area is a lain with local deressions and numerous moraine hills. It has a mild climate and small amlitudes of monthly and annual temeratures. The mean vegetation eriod with daytime temerature above 5 o C is 22 d starts in the third decade of March and lasts till the end of October. Two grous of wild boars were selected for the studies: boars inhabiting a forest (grou A) and cativebred boars (grou B). Grou A occuied an area of ca. 4 ha. The number and structure of wild boar oulation during the whole study varied. Initially, it included two sows and eight juveniles, and a boar joined the grou during oestrus. The number ranged from 6 to 2 individuals. The grou referred to eat acorns, berries, and other forest fruits, and then roots, rhizomes, grasses, and herbs. The wild boars eat also earthworms, beetle larvae, and insects. Small rodents, as well as eggs and chicks of birds nesting on the ground and in short grass constitute minor comonents of the diet. Occasionally, the animals fed also on carrion ut out as bait by hunters. In the winter, additional feed in the form of cereals, maize cobs, raw otatoes, beetroots, and ales is rovided by forestry staff. In the wild, the animals were not dewormed. Grou B occuied an area of about 3.5 ha. It was a enned area (addock), with a small forest fragment and an oen, artly hardened yard. Initially, the grou included two boars, eight sows, and 7 juveniles. During the studies, the number varied from 8 to 32 animals. The feed was mostly rovided by man, in the form of boiled otatoes, maize, dry bread, and cereals. To a small extent, the diet was sulemented by items found in the field: acorns, beetle larvae, insects, berries, and other forest fruit, roots, and occasionally small mammals and birds (chicks and eggs). The grou was subjected to deworming twice a year, using Ivermectin (Biowet, Gorzów Wlk., Poland). Samling and laboratory analysis. Studies on the endoarasites were conducted from the sring of 25 till the winter of 25/26. In that eriod, during regular field tris considering henology, a total of 42 faecal samles were collected: 6 from the wild oulation (forest) and 8 from the cative animals (addock). Because of reatent eriod of the most of wild boar helminths, faecal samles from grou B were always collected at least nine weeks after deworming. Faeces were found and collected directly from the litter in the same laces in the morning. The samles of about 5 g were laced in lastic containers. Coroscoic analysis was erformed only with fresh material within 2-3 h after collecting the samle. Qualitative (modified by Willis) flotation method, with saturated NaCl solution as flotation fluid, was used to detect and isolate eggs and larvae of the arasites (33). From each samle, 2.5 g of faeces were weighed and mixed with 5 ml of NaCl solution. Eggs were isolated with the cover glass suerosed on convex meniscus for 5 min. The eggs were identified based on their morhology (shae, structure enveloe, number and size of blastomeres or resence of larva) and biometrics. The identification followed the ublications by Thienont et al. (3) and Foreyt (). To estimate the degree of invasion, standard arasitological indices were alied: revalence of infection and mean number of eggs er samle. Statistics. χ 2 test and non-arametric Mann- Whitney U test were used to comare the numbers of recorded secies and degree of infection between the wild and farmed wild boar. Secies accumulation curve was used to calculate the secies richness of the entire arasite assemblage and each wild boar grou searately; the results were estimated with the Chao 2 nonarametric secies richness estimator based on the formula rovided by Colwell (4). Calculations were done with EstimateS 7. ackage and Statistica 8. PL. Results Out of the 42 samles collected in Lubin Forest Division, 38 were found to contain arasite eggs. The revalence of helminth infection was very high 97.2%, while the mean number of eggs er samle was 34.3 ±88.6. Eggs of six nematode taxa were isolated and identified (Oesohagostomum s./globocehalus s., Metastrongylus s., Trichuris suis, Ascaris suum, Ascaros strongylina, Physocehalus sexalatus). Unidentified eggs were also found, assigned only to tye, but because of considerable biometrical differences called Nematoda s. and Nematoda s. 2. The first tye (7-85 x 4-48 µm), dislaying characters of tyical strongylid eggs, was imossible to identify to the generic level. Nematoda s. 2 eggs, exceeding µm (-6 x µm), contained seven to eight large blastomeres. The list of arasites and values of arasitological indices are shown in Table. The revalence of infection was very similar in the two grous: A-98.4% vs. B-96.3% (χ 2 =.54; df=2; P=.76). The mean number of eggs er samle was higher in grou B (46.6 ±5.3; range -92) than in grou A (8.3 ±7.2; -83). All the arasite taxa were resent in each grou. Their revalence and mean number of eggs er samle are resented in Table 2. The frequency of occurrence of articular helminth taxa in the two grous, exressed as revalence of infection, differed but the differences were statistically significant only for Oesohagostomum s./globocehalus s. (χ 2 =4.34; df=; P=.37), Metastrongylus s. (χ 2 =8.3; df=2; P=.4), and A. suum (χ 2 =5.67; df=2; P=.).

3 63 Table Prevalence of infection and mean number of helminth eggs er samle (n=42) Secies Prevalence (%) Number of eggs er samle mean ±SD range Oesohagostomum s./ Globocehalus s ±8. 92 Ascaros strongylina ±.4 9 Metastrogylus s ± Trichuris suis ±2.5 5 Ascaris suum ± Physocehalus sexalatus ±.3 3 Nematoda s ± Nematoda s ±.7 8 ±SD standard deviation Table 2 Prevalence and mean number of eggs of articular helminth secies in two comared wild boars acks Pack A (n=6) Pack B (n=8) Taxa of arasites eggs er samle eggs er samle (%) (%) mean ±SD range mean ±SD range Oesohagostomum s./ Globocehalus s ± ±5 92 Ascaros strongylina ± ±.2 6 Metastrogylus s ± ± Trichuris suis ± ±2.4 3 Ascaris suum.6 3. ± ± Physocehalus sexalatus.6 2. ± ±.4 3 Nematoda s ± ± Nematoda s ± ±. (%) revalence of infection; ±SD standard deviation For the first two taxa and for A. strongylina and Nematoda s., the values were higher in grou A, while for A. suum, T. suis, and P. sexalatus they were distinctly higher in grou B. The arasite taxa in the two grous differed also in the distribution of the number of eggs among the samles (Table 2). Significant differences were noted for Metastrongylus s. (Mann- Whitney U Test; Z=2.68; P=.72) and A. suum (Mann-Whitney U Test Z=-2.5; P=.8). Table 2 shows that the values of the mean number of eggs er samle in grou B were higher also for Oesohagostomum s./globocehalus s. and Nematoda s.. The values for the remaining taxa were similar. Secies accumulation curves and estimates of secies richness indicate a maximal samled helminths community of aroximately nine secies, based on faecal flotations (Fig..) The number of observed secies (8) and the mean Chao2 estimate for all 42 samles (8) suggest that this survey has identified all faecal arasites, and that the analysis of additional samles would not increase estimates of secies richness. A similar situation was observed in the farmed wild boar (8 vs. 8 ±.46). However, the richness of the helminths of the forest wild boar remains inexact. The Chao2 estimator indicates a secies richness of 8.98 ±2.22. The shae of the curve and slight difference in relation to the value of richness observed (8) indicate that an exact estimate would necessitate additional samling (Fig. ). Out of the 42 examined samles, 2.8% contained one arasite taxon, 42.3% two taxa, 25.4% three taxa, 7% four taxa and only.7% showed a co-invasion of five different taxa (Fig. 2). In the two grous the mean number of secies er samle was similar: grou A 2.26±.92, grou B 2.5 ±.97). In each case samles with three taxa were the most numerous, followed by samles with two and then with one taxon. Contrary to the addock grou, among the forest grou there was no case of co-occurrence of five taxa in one samle. Discussion The helminth fauna of the wild boar from Lubin Forest Division is abundant. Literature data suggest that almost a comlete set of nematodes recorded in this host is resent. Some of the arasites are termed Oesohagostomum s./globocehalus s. According to Gundłach and Sadzikowski (5), correct identification of Oesohagostomum dentatum, O. quadrisinulatum, and Globocehalus urosubulatus with coroscoic methods and without rearing larvae can be burdened with too great error. For this reason, the grou contains eggs, whose morhology and biometrics allowed for classifying them with one of the two mentioned genera.

4 64 C 9 8 s 7 e n 6 h 5 ric s 4 ie c e 3 S 2 A 9 8 s 7 e n 6 h 5 ric s 4 ie c e 3 S 2 B 9 8 s 7 e n 6 h ric 5 s 4 ie c e 3 S 2 Observed Chao Number of samle Observed Chao Number of samle Observed Chao Number of samle Fig.. Secies accumulation curves for wild boar s helminths communities: A ack from forest; B ack from breeding; C all sites combined. Lower curve is based on observed data. Uer curve is the results of the Chao2 non-arametric estimator of secies richness based on successively greater numbers of samles from the data set s5 le m4 s a % 3 A 2 s5 le m4 s a % 3 B C 2 s5 le m4 a s % 3 2,6 6,4 47,5 23,, Number of secies 3,7 25,9 38,3 27,2 3,7, Number of secies 2,8 2,8 42,3 25,4 7, Number of secies Fig. 2. Distributions of number of helminth taxa identified er samle: A ack from forest (n=6); B ack from breeding (n=8), C combined two sites (n=42). Members of both genera have been recorded from the wild boar, but G. urosubulatus is tyical and more frequent in this host. The secies has been noted only twice in the wild boar in Poland (Tarczyński (28) revalence 54.%, Gadomska (4) %). So far only one secies of the genus Oesohagostomum has been recorded from the wild boar in Poland O. dentatum (4, 23, 28). Nosal et al. (2) have described another secies from domestic igs O. quadrisinulatum, and it can be conjectured that it may occur also in the native wild boar. This seems to be more likely since Barutski et al. (2, 3), and Mennerich-Bunge et al. (9) have found the arasite in the wild boar from the environs of Berlin and from southern Germany. The results of Pav et al. (22) from the former Czechoslovakia, and Gadomska (4) from the Kaminos National Park (KPN) make it ossible to comare infection indices in the wild boar living under different conditions. Data of Pav et al. (22) show that the level of infection with G. urosubulatus and O. dentatum is distinctly higher in farmed animals comared to wild oulation (G. urosubulatus % vs. 8.3%; O. dentatum. 26.3% vs. %, resectively). Gadomska (4) reorts on the much higher revalence of G. urosubulatus in wild oulation (% vs. 67% in farmed animals). The values for O. dentatum are the reverse, i.e. higher in farmed wild boar (9% vs. 56%).

5 65 Though the results resented here (grou A - 9.8% vs. grou B - 79%) artly corresond with Gadomska s (4) data, they are not comarable because of the joint treatment of eggs of the two genera in coroscoic studies. Outside Poland, reresentatives of both genera have been found in the wild boar from e.g. the former Czechoslovakia, Bulgaria, France, Sain, the Netherlands, Germany, and Iran. Nematodes of the genus Metastrongylus are the second most revalent (48.6%). Because five secies of the genus have been recorded from the wild boar in Poland: Metastrongylus elongatus, M. salmi, M. udendotectus, M. confuses, and recently M. asymetricus (6, 4, 2, 28), detailed egg-based identification is not ossible. The differences in the revalence between the two grous (62% vs. 38%) result from its heteroxenic develoment, which requires soil oligochaetes as intermediate hosts. It seems obvious that the oulation using an unlimited and not hardened exanse of fields and forests is more rone to invasion of this ulmonary arasite. The differences observed in this study do not find the confirmation in Gadomska s (4) results; she has observed similar levels of infection with this arasite (92% vs. 89%) in the wild boar from the Kaminos Forest and farmed wild boar. Comletely different data have been resented by Pav et al. (22), with the revalence in farmed wild boar greatly exceeding the value for the wild oulation. The total revalence of infection with Metastrongylus s., of slightly less than 5%, observed in this study, is similar to Tarczyński s (28) result 52.5% and much higher than the values from Western Pomerania 2.9% (23). Slightly higher indices of infection with this arasite have been noted, among others, by Jarvis et al. (7) from Estonia - 82%, Barutzki et al. (2, 3) from Germany %, and Humbert and Henry (6) from France 9%. The differences in the level of invasion between the two grous are the greatest in the case of Ascaris suum. In grou A it is very low - only.6%, comared to 26% in grou B. Likewise, the mean number of eggs er samle differs significantly. It is likely that the recorded number of eggs, almost 3-times higher in grou B, results from cumulation of invasive forms of this secies within the limited area occuied by the herd as well from common feeding of animals on low variety of man sulied food. The results are wholly comatible with data of Pav et al. (22) and Gadomska (4). Though A. suum is common in igs and wild boars worldwide, the level of wild boar infection is not very high. The trend is also confirmed by the small (5.5%) total revalence of infection observed in this study. Additionally, Trichiuris suis shows a rather small revalence of infection (3.4%), with higher values for the farmed wild boar. Different results are reorted by Gadomska (4), who has found the revalence to be twice higher in the wild boar from the KPN (65% vs. 33%). Similar values for two comared grous have been observed in the former Czechoslovakia (22): 26.3% vs. 23%). T. suis is a tyical suid arasite. Its simle life cycle and resistance of eggs to environmental conditions make it widesread and often recorded from wild boar. Other secies with similar biology, recorded in this study are Ascaros strongylina and Physocehalus sexalatus. They are secific and frequent wild boar arasites. Their revalence in the studied oulations is small (A. strongylina 9% P. sexalatus 2.8%), while e.g. Tarczyński (28) reorts 44.3% and 9.7% infection, and Gadomska (4) - 82% and 6%, resectively. Of the two studied grous, the infection with A. strongylina is higher in the wild oulation (23% vs. 6%). Gadomska s (4) data show a similar level of infection in two oulations (43% vs. 44%), and Pav et al. (22) have found a distinctly higher infection level in farmed wild boar (68.4% vs. 6%). In the case of P. sexalatus the higher infection level in the farmed animals is comatible with the data from the former Czechoslovakia (22). Rather low indices of the infection with the two nematodes are rather surrising. Parasitological literature shows that the two secies are rather common. At the same time the arasite has a life cycle involving a common intermediate host, easily accessible to wild boar dung-eating insects. A considerable role in sreading of the secies is layed by beetles, retiles, birds, and small mammals, which assively transort larvae as reservoir hosts (3, 5). All these organisms constitute a considerable roortion of the wild boar diet in the studied area. The unidentified eggs, classified to the level of tye, show biometrical differences: Nematoda s. eggs of average (8 x 45 µm) size, dislay characteristics of tyical strongylid eggs and are imossible to identify to the generic level; Nematoda s. 2 exceeding µm in length, contain seven to eight large blastomeres. The number of blastomeres, according to Gundłach and Sadzikowski (5), oints to Hyostrongylus rubidus, but the size does not corresond with the values given in the descritions of the secies. Such large, strongylomorh eggs are characteristic for Stehanurus dentatus a ig and wild boar kidney arasite. The nematode, however, occurs mainly in the troics and is very rare in Euroe (29). In conclusion, it can be assumed that the small differences involve only values of some arasitological indices while the arasite secies comosition does not differ between the studied grous. The data do not suggest any strong effect of the environment, and esecially the availability and diversity of the feed basis, on the level of infection of the wild boar. The results confirm the diversity of wild boar helminth fauna and the high level of infection with intestinal and ulmonary arasites and justify further monitoring of the condition of wild boar. The ossible vector role of wild boar towards domestic animals is also imortant, as well as the economic consequences leading to a decrease in wild boar abundance and rofitability of the increasingly oular wild boar farming. Acknowledgments: We would like to exress our thanks to Professor Beata M. Pokryszko for revising the English of our aer. We also thank anonymous reviewer for useful comments.

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