Download as pdf or txt
Download as pdf or txt
You are on page 1of 7

Veterinary Parasitology 115 (2003) 335–341

Short communication
Wild boar helminths: risks in animal translocations
Isabel G. Fernandez-de-Mera a , Christian Gortazar a,∗ ,
Joaquin Vicente a , Ursula Höfle a , Yolanda Fierro b
a National Research Institute on Game Biology (IREC, CSIC-UCLM), Ciudad Real, Spain
b Yolfi Properties S.L. Abenojar, Ciudad Real, Spain

Received 3 January 2003; received in revised form 28 April 2003; accepted 17 May 2003

Abstract
The helminth populations found in a group of wild boars collected in central Spain were compared
to those in a group of animals imported from a French game farm that produces boars for restocking.
Eleven helminth species, including ten nematodes and one acanthocephalan, were found. Gongy-
lonema pulchrum and Macracanthorhynchus hirundinaceus were only detected in autochthonous
wild boars, while Oesophagostomum dentatum, Ascaris suum, and Trichuris suis were detected
in imported animals only. Autochthonous wild boars were more frequently and more intensely
parasitised by Ascarops strongylina than the imported ones. No differences in prevalence nor in-
tensity were found for the species Capillaria garfiai, Globocephalus urosubulatus, Metastrongylus
sp., Physocephalus sexalatus and Simondsia paradoxa. To our knowledge, G. urosubulatus, G.
pulchrum and S. paradoxa have not previously been described in wild boars in Spain. Our results
highlight the risks of translocating wild animals, with regard to their helminth parasites. Until
improved control measures are established, it would be wise to avoid long-distance translocations
in order to prevent the potential introduction of foreign parasites.
© 2003 Elsevier B.V. All rights reserved.
Keywords: European wild boar; Helminths; Sus scrofa; Risk factors; Spain

1. Introduction

The intestinal helminths of the domestic pig (Sus domesticus) have been described at
length in many European areas (Nansen and Roepstorff, 1999). However, less information
exists on the helminths of the European wild boar, Sus scrofa (for example Gadomska,
1981; Cotteleer and Fameree, 1982; Kutzer, 1986; Eslami and Farsadhamdis, 1992; Takacs,
1997).
∗ Corresponding author. Tel.: +34-926-295450; fax: +34-926-295451.
E-mail address: christian.gortazar@uclm.es (C. Gortazar).

0304-4017/$ – see front matter © 2003 Elsevier B.V. All rights reserved.
doi:10.1016/S0304-4017(03)00211-5
336 I.G. Fernandez-de-Mera et al. / Veterinary Parasitology 115 (2003) 335–341

Previous reports on helminths of the wild boar in the Iberian Peninsula are scarce and
either refer to different geographical regions (Cordero del Campillo and Rojo Vázquez,
1999; Pereira et al., 1994; De-la-Muela et al., 2001) or focus on a particular helminth
species (Gállego and Mas-Coma, 1975; Gállego et al., 1977).
The wild boar is the most important large game species in the Iberian Peninsula. Only
in the province of Ciudad Real, central Spain, over 5000 wild boars are shot annually dur-
ing the hunting season. Due to the high demand for boar-hunting, an unknown number of
wild-caught or captive-bred wild boars are imported yearly for restocking purposes, mainly
from France. The geographical distance between the localities of origin of imported boars
and their release sites in Spain, as well as the differences in production systems, may be pos-
sible reasons for differences between the helminth communities of autochthonous Spanish
wild boars and the imported, eventually farm-bred, wild boars. In fact, it is well recognised
that management practices determine the transmission rate and the risk of economic losses
due to parasitism in domestic pigs (Nansen and Roepstorff, 1999).
Since little is known on the parasites and diseases of wild boars imported to Spain for
hunting purposes, our objective was to compare their helminth community with those of a
sample of autochthonous wild boars. This was done in order to assess the risks of importing
new parasites into naı̈ve populations or of coming into contact with new parasites after
release. Also, this study attempts to evaluate if extensively held domestic pigs could be at
risk of infections by parasites introduced with imported wild boar.

2. Materials and methods

2.1. Sources of the carcasses

Autochthonous wild boars (n = 16), were collected from hunters from January to March
2002 in two private hunting estates in south central Spain (38◦ 55′ N, 0◦ 36′ E and 39◦ 25′
N, 0◦ 22′ E; both 600–850 m above sea level). In terms of climate, these areas belong to
the Mediterranean region and the habitat is characterized by scrubland and evergreen oak
(Quercus ilex) woodlands with scattered pastures and small crops. The ranges are fenced
in order to enclose the wild ruminants, but boars are able to cross under these fences.
In February 2002, 21 captive-bred wild boars were imported from a French breeding
facility into the quarantine facility of a private hunting estate. The breeding facility in
France consists in a 1 ha large enclosure with supplementary feeding and watering. This
importation had been carried out without the mandatory permit from the regional Fish and
Game Service. When informed about the importation, the Spanish Authorities ordered the
slaughter of the imported boars in order to prevent genetic or sanitary risks. Prior to slaughter
12 out of the 21 imported wild boars were treated with anthelminthics on an experimental
basis. Thus, only the untreated control group (n = 9) is included in the results of this paper.

2.2. Processing of the material

Both the farmed and the hunted wild boars were necropsied immediately after death. Each
animal was measured, weighed and its sex determined. Based on tooth eruption patterns,
I.G. Fernandez-de-Mera et al. / Veterinary Parasitology 115 (2003) 335–341 337

boars less than 12 months of age were classified as juveniles, and those over 1 year of
age were classified as adults. We estimated fat condition using the kidney fat index (Riney,
1955).
Each animal was thoroughly analysed for the presence of helminths, that were re-
moved using the common proceedings described in parasitology (Ministry of Agriculture
Fisheries and Food, 1986). Tongue, lung, digestive tract, liver, gall-bladder, and renal pelvis
were examined with routine techniques for the detection of helminth parasites (Soulsby,
1982). Parasites were fixed in 70% ethanol and cleared with lactophenol blue solution for
identification according to Soulsby (1982).
A coprological analysis was carried out with faecal material extracted from the rectum of
each animal after necropsy by zinc sulfate flotation (specific gravity 1.18) using McMaster
chambers (Ministry of Agriculture Fisheries and Food, 1986).
Helminths were identified based on figures and descriptions given in Boch and Supperer
(1983), Soulsby (1982), Mehlhorn et al. (1992), and Cordero del Campillo et al. (1994). We
used quantitative parasitology for evaluating the statistical significance of all prevalence
differences and to calculate the confidence intervals for prevalence and intensity (Rózsa
et al., 2000).

3. Results

All imported wild boars were less than 1-year old, and only 2 of the 16 autochthonous
boars were adults (Fisher’s test, P > 0.05). The head and body length ranged from 62
to 142 cm in the autochthonous boars and from 78 to 115 in the imported ones (U-test,
Z = − 1.78, P > 0.05). No significant difference in the gender ratio was detected between
the study groups (χ2 = 5.4, 1 d.f., P > 0.05). The condition of the imported animals was
poor, with an average KFI of 32.9 ± 22. This KFI was lower than the one found in the
sample of autochthonous wild boars (63.3 ± 44; U-test, Z = 2.17, P < 0.05). None of the
autochthonous animals, but three of nine imported wild boars, showed severe diarrhoea.
The helminthological findings are summarized in Table 1. None of the 25 examined
carcasses was free of helminth parasites. Eleven helminth species were identified, includ-
ing ten nematodes and one acanthocephalan. The nematodes Globocephalus urosubulatus,
Metastrongylus sp., Ascarops strongylina, Physocephalus sexalatus, Simondsia paradoxa
and Capillaria garfiai were the predominant helminths in both groups of wild boar. The
prevalence of Metastrongylus sp. was similar in the two groups. Oesophagostomum denta-
tum, Ascaris suum and Trichuris suis were only detected in the sample of imported boars,
while Gongylonema pulchrum and Macracanthorhynchus hirundinaceus, two heteroxenous
species, were found only in the autochthonous animals. To our knowledge, G. urosubula-
tus, G. pulchrum and S. paradoxa have not been described previously in the wild boar
in Spain. The prevalence and intensity of parasitism by A. strongylina was higher in the
autochthonous wild boars.
The results of the coprological analysis are shown in Table 2. Prevalence of parasite eggs
in the faeces was higher in the imported boars than in the autochthonous individuals for
all parasite species except for Capillaria sp. In one case, shedding of Capillaria-eggs was
detected in an autochthonous boar in which no adult capillarid had been found.
338

Table 1
Sample size (n), prevalence (% and 95% CI), intensity of parasitation (average and 90% CI), parasite distribution (variance/mean ratio and k statistic), and statistical level
of significance of differences in prevalence (Fishers test) and intensity (U-test)a
Imported Autochthonous Fisher U-test

n Prevalence Intensity Variance/ k n Prevalence Intensity Variance/ k


% CI (95%) Mean CI (90%) mean % CI (95%) Mean CI (90%) mean

G. urosubulatus 9 11.1 0–48 3.00 0.00–0.00 3.00 0 15 26.7 8–55 80.75 16.0–137.5 165.72 0.05 0.3597 n.s.
O. dentatum 9 22.2 3–60 23.50 3.00–23.50 40.68 0.06 15 0.0 0–22 NA 0 NA 0 0.1304 n.s.
Metastrongylus sp. 9 66.7 30–92 633.0 21.17–1245 1692 0.14 15 46.7 21–73 6.29 2.71–9.71 9.08 0.27 0.3001 n.s.
A. suum 9 44.4 14–79 3.00 1.00–4.75 5.063 0.37 15 0.0 0–22 NA 0 NA 0 0.0119 n.s.
G. pulchrum 9 0.0 0–34 NA 0 NA 0 14 21.4 5–51 3 1.00–3.00 5.41 0.13 0.2055 n.s.
A. strongylina 9 11.1 0–48 1.00 0.00–0.00 1.00 0 15 60.0 32–84 16.89 7.78–26.22 26.09 0.23 0.0245 P < 0.05
P. sexalatus 9 22.2 3–60 1.50 1.00–1.50 1.50 0.57 14 35.7 13–65 4.80 2.60–6.80 4.97 0.22 0.4182 n.s.
S. paradoxa 9 22.2 3–60 1.50 1.00–1.50 1.50 0.57 14 28.6 8–58 7.00 5.25–8.25 5.92 0.13 0.5652 n.s.
T. suis 9 33.3 7–70 117.67 6.00–214 240.41 0.07 15 0.0 0–22 NA 0 NA 0 0.0415 n.s.
C. garfiai 9 11.1 0–48 1.00 0.00–0.00 1.00 0 14 0.0 0–23 NA 0 NA 0 0.3913 n.s.
M. hirundinaceus 9 0.0 0–34 NA 0 NA 0 15 53.3 26–79 6.63 2.13–11.25 19.73 0.28 8.75E− 03 n.s.
a
n.s., not significant; NA, not applicable.
I.G. Fernandez-de-Mera et al. / Veterinary Parasitology 115 (2003) 335–341
I.G. Fernandez-de-Mera et al. / Veterinary Parasitology 115 (2003) 335–341 339

Table 2
Types of parasite propagules detected in fecal samples from autochthonous and imported European wild boars
Type of parasite propagule Autochthonous (n = 15) Imported (n = 9)

n % n %
Metastrongylus sp. 1 6.7 6 66.7
A. suum 0 0 1 11.1
T. suis 0 0 1 11.1
Capillaria sp. 2 14.3 1 11.1
Other nematodes 1 6.7 2 22.2
M. hirundinaceus 5 33.3 0 0

4. Discussion

Farm-reared animals do usually have higher prevalences of direct-cycle parasites than of


heteroxenous ones. Moreover, overcrowding favours parasite transmission, and the farming
of wild boars for the restocking of hunting areas is frequently carried out without the
care applied to domestic pig production. In our sample of farm-bred boars, a poor body
condition was evident, and it is well known that malnourishment compromises the pig’s
ability to resist parasitic infections (Pedersen et al., 2002). Thus, it was not surprising to
detect high prevalences and intensities of parasites such as O. dentatum, A. suum or T. suis.
In contrast, some heteroxenous parasites such as G. pulchrum and M. hirundinaceus were
only detected in the free-living autochthonous animals, probably because of their higher
probability of coming into contact with the intermediate hosts.
The translocation of animals may create different types of disease problems. The first is
that a new disease agent may be introduced into an area where it did not previously occur.
The second problem is that animals may be released into an area where a disease agent,
to which they are susceptible, already exists (Wobeser, 1994). A third problem is that the
disease agents carried by the translocated animals may benefit from the stress-mediated
immunosuppression, causing more severe disease and negatively affecting their survival
probabilities.
In the present study, three nematodes found in imported wild boars, O. dentatum, A.
suum and T. suis, were not detected in the autochthonous ones. Since all three species
have been reported previously in wild boars from other Spanish regions (Pereira et al.,
1994, De-la-Muela et al., 2001), their apparent absence from the study area may be due to
the small sample of autochthonous wild boars investigated, or to a real absence of these
nematodes from this boar population. In that case, their introduction into the hunting estates
may have had consequences on the wild populations, since all of them have been related
with clinical disease in the European wild boar (Boch and Schneidawind, 1988). Moreover,
in most individuals, the presence of different helminth species would have gone undetected
if only a single coprological analysis had been carried out, instead of a complete necropsy.
On the other hand, G. pulchrum and M. hirundinaceus were present in the sample of
autochthonous wild boars, but not in the imported ones. The absence of these helminths may
reflect a real absence of these parasites from the breeding facility due to their heteroxenous
life-cycle (see above), or may alternatively be explained by the small sample size of imported
340 I.G. Fernandez-de-Mera et al. / Veterinary Parasitology 115 (2003) 335–341

boars that were investigated, or even by age-related differences in their prevalence, since all
imported individuals were less than 1-year old (e.g. De-la-Muela et al., 2001). If released,
the imported wild boars may be coming into contact with new parasites that could affect
their condition (Boch and Schneidawind, 1988).
Finally, two of the imported boars had more than 1000 Metastrongylus sp. in their lungs,
and high intensities of T. suis and O. dentatum were found in two and one animals, respec-
tively. Considering the stress caused by the transport and release of an animal into a new
range, these or other parasites could have had a negative influence on their survival after
release.
Our results highlight the risks of translocating wild animals, with regard to their helminth
parasites. The current veterinary inspection of wildlife translocations in Europe urgently
needs to be improved. Concerning the helminths of the European wild boar, diagnostic
procedures need to be tested and, eventually, treatment trials should be done in order to
prevent any negative effect of the translocations on game production, conservation and
animal welfare. Meanwhile, it would probably be wise to avoid long-distance translocations
in order to prevent the contact between extremely different helminth communities.

Acknowledgements

The authors thank Diego Villanua and Pelayo Acevedo for their help in the laboratory, and
Bernardo Herrera, Alfredo Peña and the gamekeepers of the study site for their assistance
in the field. The study was supported by project AGL2001-3947, Ministerio de Ciencia y
Tecnologı́a and FEDER. This is a contribution to the agreement between Yolanda Fierro
and Universidad de Castilla, La Mancha, and to the Plan Andaluz de Investigación (PAI,
Grupo RNM 118).

References

Boch, J., Schneidawind, H., 1988. Krankheiten des jagdbaren Wildes. Parey, Berlin, 398 pp.
Boch, J., Supperer, R., 1983. Veterinärmedizinische Parasitologie. Parey, Berlin, 532 pp.
Cordero del Campillo, M., Rojo Vázquez, F.A., 1999. Parasitologı́a Veterinaria. McGraw-Hill, Interamericana,
968 pp.
Cordero del Campillo, M., Castañón, L., Reguera, A., 1994. Index-Catalogue of Iberian Zooparasites. Universidad
de León, Secretariado de publicaciones, 650 pp.
Cotteleer, C., Fameree, L., 1982. Eimeriidae and helminths of pig and wild boar in Belgium. Incidence of anti
toxoplasmic antibodies. Schweizer Archiv fur Tierheilkunde. 124 (1), 37–47.
De-la-Muela, N., Hernández de Luján, S., Ferre, I., 2001. Helminths of wild boar in Spain. J. Wildlife Dis. 37 (4),
840–843.
Eslami, A., Farsadhamdis, 1992. Helminth-Parasites of Wild Boar, Sus scrofa, in Iran. J. Wildlife Dis. 28 (2)
316–318.
Gadomska, K., 1981. 1981. The qualitative and quantitative structure of the helminthocoenosis of wild boar (Sus
scrofa L.) living in natural (Kampinos National Park) and breeding conditions. Acta Parasitol. Polonica. 28,
151–170.
Gállego, J., Mas-Coma, S., 1975. Capillaria garfiai n. sp. (Nematoda: Trichuridae). Parásito de la mucosa lingual
del jabalı́, Sus scrofa Linnaeus, 1758 (Mammalia: Artiodactyla). Vie Milien. XXV, 2, C, pp. 237–248.
I.G. Fernandez-de-Mera et al. / Veterinary Parasitology 115 (2003) 335–341 341

Gállego, J., Rocamora, J.M., Mas-Coma, S., 1977. Nuevos datos sobre Capillaria garfiai Gállego et Mas-Coma,
1975 (Nematoda: Trichuridae), parásito común del jabalı́ en la Penı́nsula Ibérica. Revista Ibérica de Parasitologı́a
37, 3–4.
Kutzer, E., 1986. Zur Behandlung der Sarcoptesräude bei Wildund Hausschweinen. Deutsche Tierärztl
Wochenschrift. 93, 426–429.
Mehlhorn, H., Düwel, D., Raether, W., 1992. Atlas de parasitologı́a veterinaria. Grass, Barcelona, 436 pp.
Ministry of Agriculture Fisheries and Food, 1986. Manual of veterinary parasitological laboratory techniques, 3rd
ed. HMSO Books, London, 196 pp.
Nansen, P., Roepstorff, A., 1999. Parasite helminths of the pig: factors influencing transmission and infection
levels. Int. J. Parasitol. 29, 877–891.
Pedersen, S., Saeed, I., Michaelsen, K.F., Friis, H., Murrell, K.D., 2002. Impact of protein energy malnutrition on
Trichuris suis infection in pigs concomitantly infected with Ascaris suum. Parasitology 124, 561–568.
Pereira, J.M., Ortega, L.M., González, R., Reguera de Castro, E., Reyero, F., 1994. Parasites of wild boar in
Riaño Mountain (León, Spain). Ponencias y comunicaciones del I Congreso de Veterinarios de Castilla y León.
Excma. Diputación Provincial de León, Gráficas Alse, León, Spain, pp. 289–290.
Riney, T., 1955. Evaluating condition of free ranging red deer (Cervus elaphus), with special reference to New
Zealand. NZ J. Sci. Technol. Sect. B 36, 429–463.
Rózsa, L., Reiczigel, J., Majoros, G., 2000. Quantifying parasites in samples of hosts. J. Parasitol. 86, 228–232.
Soulsby, E.J.L., 1982. Parasitologı́a y enfermedades parasitarias de los animales domésticos. 7th ed.
Interamericana, Mexico, 809 pp.
Takacs, A., 1997. Contribution to the helminth infestation in wild boar (Sus scrofa L.) in Hungary. Wien Tierarztl
Monat. 84 (11), 314–316.
Wobeser, G.A., 1994. Investigation and Management of Disease in Wild Animals. Plenum Press, New York,
265 pp.

You might also like