|A survey of intestinal helminths in wild carnivores from the Tatra National Park, southern Poland
Anna Boreckaa, *, Jakub Gawora, Filip Ziębab
a Laboratory of Parasitoses of Domestic Animals, W. Stefański Institute of Parasitology of the Polish Academy of Sciences, Twarda 51/55, 00-818 Warsaw, Poland
b Tatra National Park, Chałubińskiego 42a, Zakopane, Poland
From January 2011 to July 2012 we examined 144 faecal samples of wild carnivores - 72 of wolves (Canis lupus), 45 of red foxes (Vulpes vulpes), 15 of pine martens (Martes martes) and 12 of brown bears (Ursus arctos) from the Tatra National Park to evaluate the prevalence of intestinal helminths. In wolves monospecific infection with Trichuris vulpis (13.9%), Toxocara canis (6.9%), Ancylostoma/Uncinaria (5.6%) and taeniids (1.4%) was revealed. In red foxes the most prevalent was T. vulpis (64.4%), along with T. canis (11.1%), Ancylostoma/Uncinaria (8.9%) and taeniids (2.2%). Monospecific infection with T. vulpis was more frequent (44.4%), than infection with two species, i.e. T. vulpis vs. Ancylostoma/Uncinaria, T. vulpis vs. T. canis or T. vulpis vs. taeniids (17.8%). In pine martens Trichuris spp. was the most prevalent (40.0%), T. cati and Ancylostoma/Uncinaria were found in 13.3% and 6.7% samples, respectively. In faeces from brown bears no parasite eggs were found.
The present survey in wild carnivores revealed significant prevalence of hazardous to human and animal health parasites, such as Toxocara spp. and Trichuris spp. (8.3% and 31.0% in all examined samples, respectively).
Keywords parasites, eggs, infection, faeces, wild carnivores
The Tatra National Park is located in the Tatra Mountains in southern Poland, bordering Slovakia. The National Park was created in 1954 on an area of 215 km2. It is the most visited national park in Poland, with more than 3 million tourists every year. Within this area live many species of predatory mammals, namely wolves (Canis lupus), red foxes (Vulpes vulpes), pine martens (Martes martes), beech martens (Martes foina), brown bears (Ursus arctos), Eurasian lynxes (Lynx lynx), marmots (Marmota marmota latirostris), wildcats (Felis silvestris), European polecats (Mustela putorius), stoats (Mustela erminea), least weasels (Mustela nivalis), European otters (Lutra lutra) and European badgers (Meles meles).
Population of wolves and brown bears in TPN is more than ten of each species, red foxes and martens about a hundred. To date no examinations of internal parasites of predatory animals in the Tatra National Park have been done.
The aim of the present study was to provide data on the intestinal helminths fauna of wolves (Canis lupus), red foxes (Vulpes vulpes), pine martens (Martes martes) and brown bears (Ursus arctos) from the Tatra National Park, Poland.
Materials and Methods
From January 2011 to July 2012 we examined 144 faecal samples of wolves (72), red foxes (45), pine martens (15) and brown bears (12) from the Tatra National Park. The scats were identified by the staff of the National Park by their appearance, size and shape. Collected samples were frozen at -180C to eliminate hatching Ancylostoma/Unicinaria larvae from eggs. To recover parasite eggs we used flotation with saturated NaCl solution (specific gravity 1.2) according to Fülleborn’s method with Willis’ modification. In the procedure 1 gram of faeces was mixed with 10 ml of saline solution, wiped through a sieve, and then transferred to 10 ml centrifuge tube. The tubes were centrifuged at 1200 rpm for 10 min. The solution was added to each tube to form a meniscus and a coverslip was overlaid. After 15 min the coverslip was transferred to a glass slide which was examined at x 100 magnification and parasites eggs were counted. The eggs were identified according to their morphological features as described by Mehlhorn et al. (1986) and the percentage of positive samples was calculated and number of worm eggs per gram of feces samples (epg) also.
The results are shown in Table 1. Among 144 faecal samples examined in 60 (41.7%) helminth eggs were found; in samples from bears no eggs were revealed. Among 72 faecal samples from wolves in 20 (27.8%) monospecific infection with Toxocara canis (6.9%), Trichuris vulpis (13.9%), Ancylostoma/Uncinaria (5.6%) or taeniids (1.4%) were found, in one sample (1.4%) T. canis and T. vulpis were revealed. Out of examined 45 faecal samples of red foxes, 31 contained parasites eggs (68.9%). The most prevalent was T. vulpis (64.4%), along with T. canis (11.1%), Ancylostoma/Uncinaria (8.9%) and taeniids (2.2%). Monospecific infection with T. vulpis was more frequent (44.4%), than two species (T. vulpis vs Ancylostoma/Uncinaria, T. vulpis vs T. canis, and T. vulpis vs taeniids) or three species infection (T. canis, T. vulpis and Ancylostoma/Uncinaria) (17.8% and 2.2%, respectively). Among 15 faecal samples from pine martens Trichuris spp. was the most prevalent (40.0%), while T. cati and Ancylostoma/Uncinaria were found at 13.3% and 6.7%, respectively. The considerable number of Trichuris and Toxocara eggs per gram (epg) was found in samples from red foxes, pine martens and wolves, with a mean epg 132.2 (1-592), 84.7 (1-284), 22.2 (1-120) and 27.2 (3-65), 156.0 (40-272), 69.2 (4-262), respectively. For Ancylostoma/Uncinaria a mean epg was 25.5 (2-40) in foxes and 3.0 (1-5) in wolves. In case of taeniids, 22 and 1 egg were found in each of one wolf and fox sample.
In 41.4% of examined faecal samples from five species of wild carnivores eggs of parasite were present, with 27.8% samples positive in wolves, 68.9% in foxes and 53.4% in martens. In this study we examined a small number of samples from brown bears (12) due to difficulty to obtain material in the large mountainous area from their small population. In the case of 72 samples collected from wolves, accordingly to the small population of these predators in the Tatra National Park (about ten animals) it must be assumed that some samples came from the same individual.
Infection with Toxocara spp. and Trichuris spp. was found in wolves, red foxes and pine martens, with the highest prevalence of Trichuris vulpis in red foxes (64.4%). Ascarids and hookworms are the most common parasites in wild carnivores all over the world.
In Poland and other European countries Toxocara canis has been recorded in wolves. In mountainous areas of the southern Poland, in wooded areas in the north-eastern Poland, in Latvia and in the southern Kazakhstan T. canis was found with prevalence of 5.6%, 13.5%, 5.8% and 39%, respectively (Popiołek et al. 2008; Kloch et al. 2005; Bagrade et al. 2009; Abdybekova and Torgerson 2012). In this study we found eggs of Trichuris vulpis in 13.9% samples from wolves, the higher level of infection was noted in the north-eastern Poland - 38.5% (Kloch et al. 2005), and in the southern Kazakhstan – 22.0% (Abdybekova and Torgerson 2012).
Ancylostoma/Uncinaria were found at a low prevalence in the wolf from the Tatra National Park (5.6%), however Kloch et al. (2005) found the parasites in 31% of faecal samples from 57 wolves. In one sample from wolf we found taeniid eggs (1.4%), which can not be determined to the species level based on their morphology. Segovia et al. (2003) in wolves from various localities in Spain found four species from Taenidae family - T. hydatigena, T. multiceps, T. serialis and T. pisiformis.
Red foxes are the most frequently studied wild carnivore species. Analysis of available data shows a strong resemblance of intestinal helminth fauna of red foxes from the Tatra National Park and other regions in Poland. The most common nematodes in foxes in the previous studies include T. canis (13.6%-28.3%), T. vulpis (28%) and Uncinaria stenocephala (11.1%-35.8%) (Górski et al. 2006; Pacoń et. al. 2006; Borecka et al. 2009). Previously in foxes were also found flukes Alaria alata (2.2%-56.7%) and tapeworms - Mesocestoides spp. (63.8%-76.8%) and Echinococcus multilocularis (1%-62.9%) (Ramisz and Balicka-Ramisz 2001; Balicka-Ramisz et al. 2003; Pacoń et al. 2006; Malczewski et al. 2008; Borecka et. al. 2009).
In this study in pine martens we found two nematode species, T. cati and Trichuris spp. Górski et. al (2006) in the same host species from Bialowieża Primeval Forest (eastern Poland) recorded T. cati and Uncinaria criniformis. Segovia et al. (2007) in pine martens from the Iberian Peninsula and Balearic Archipelago found seventeen helminth species, with three dominant trichurids species, namely Pearsonema plica, Eucoleus aerophilus and Aonchotheca putorii (72.2% of total helminth individuals detected).
In bears faeces collected in the Tatra National Park no parasites were present. Other authors showed the most frequent parasite of bear Baylisascaris transfuga, followed in order of prevalence by fish tapeworm Diphyllobothrium spp., taeniid tapeworms, hookworms Uncinaria spp., fluke Echinostoma revolutum and filarial worm Dirofilaria ursi (Choquette et al. 1969).
The present survey in wild carnivores revealed considerable prevalence of hazardous to human and animal health parasites, such as Toxocara spp. and Trichuris spp. (8.3% and 31.0% in all examined samples, respectively). Trichurids were highly prevalent in foxes (64.4%) and martens (40.0%), and the faecal samples contained a considerable number of eggs (a mean 132.2 epg in foxes, 84.7 in martens). Ascarids were found 6.9%-13.3% prevalent in wolves, foxes and martens, with the highest epg of T. cati in martens (a mean 156.0). So, there is a high potential of spreading of trichurid and ascarid eggs by wild carnivores. Red foxes act as a main parasite reservoirs for the pet dogs, and in association with their invasion of urban areas play an important role in the transmission of helminthic zoonoses.
The present survey revealed that there is a serious risk of such zoonoses in the Tatra National Park for tourists, especially children. Regional county authorities should implement educational programs for prevention of zoonotic parasites infections with focusing on people visiting the Tatra National Park. The outdoor interpretation panels should provide such information for residents and guests.
We would like to thank the staff of the Tatra National Park for collecting faecal samples in the Tatra Mountains.
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Table 1. Prevalence of intestinal helminths based of faecal samples examination in wolves (Canis lupus), red foxes (Vulpes vulpes) and pine martens (Martes martes) from the Tatra National Park, Poland.
Family Species of samples
Toxocara Toxocara Trichuris Trichuris Ancylostoma/Uncinaria Taenidae
canis cati vulpis spp. family
Canidae Canis lupus 72
Canidae Vulpes vulpes 45
Mustelidae Martes martes 15
6.9 13.9 6.9 1.4
11.1 64.4 8.9 2.2
13.3 40.0 6.7 -