Parasitological survey of Polish primitive horses (Equus caballus gmelini Ant.): influence of age, sex and management strategies on the parasite community

Polish primitive horses or the Polish Konik horse (Equus caballus gmelini Antonius form silvatica Vetulani) is the primitive horse breed originating directly from the tarpans (Pruski, 1959; Pruski & Jaworowska, 1963; Kownacki, 1984; Pasicka, 2013). This semiwild breed of horse is a natural relic and a precious part of Poland’s and Europe’s heritage. Due to their small numbers these horses are classified as an endangered breed and have been included into the program for protection of threatened local breeds (Jaworski, 2007). Analysis of data collected in 2010 documented the national population of Polish primitive horses to be 150 mares and 40 stallions in state breeding centers; and 550 mares and 130 stallions under nature conditions (Jezierski et al., 2012).

Polish primitive horses are maintained under three different strategies: stabled (ST), free-ranging (FR) and semi-free (SF) management systems (Jezierski & Jaworski, 2008). The stabled system is traditional – the horses are kept and fed in stables or on small paddocks. In the free-ranging system, horses are kept in natural reserves as free ranging animals under nearly natural conditions without human care (Jaworski, 2007). The semi-free conditions are characterized by keeping the horses in large reserve areas, similarly to free-ranging conditions, but the horses are periodically in contact with people, moved onto small paddocks, and can be used for various types of work (Jezierski & Jaworski, 2006, 2008). Grazing is very important in all three management strategies and horses must spend most of their time on pastures or paddocks (Jaworski & Jaszczycska, 2004).

Worldwide, wild and domestic horses kept under different management strategies are infected with gastrointestinal parasites that cause significant problems to their health (Lichtenfels, 1975; Dvojnos & Kharchenko, 1994; Hodgkinson, 2006). Previous studies monitoring the gastrointestinal parasite community of Polish primitive horses from different reserves indicated high levels of infections with intestinal parasites, especially with strongylids, which without anthelmintic treatments reached infection levels estimated as thousands of eggs per gram of feces (Romaniuk et al., 2001, 2002, 2003). Even though anthelmintic treatments significantly reduces the burden levels of intestinal parasites, regular treatments before moving them to new places are not routinely practiced in Poland; therefore, their parasites may spread into new territories (Romaniuk et al., 2007; Slivinska et al., 2010).

Several studies on the gastrointestinal parasites in the Polish primitive horses from different reserves in Poland were performed recently (Slivinska et al., 2009; 2012; 2013; 2016). However, our knowledge on the influence of various internal and external factors such as age, sex and types of management strategies on the gastrointestinal parasite community is still limited. The aim of the present study was to perform an extensive analysis of relations between age, sex and management strategies and the gastrointestinal parasite communities of Polish primitive horses maintained on nine horse farms in north-eastern and central Poland. Special analysis of the strongylid community structure in the horses of different sexes, ages and from different farms also was carried out.

This work represents the first extensive analysis of a dependence of infections of gastrointestinal parasites in Polish primitive horses in regard to their age, sex and management strategies. Our parasitological survey was carried out during a five year period at nine breeding farms located in four regions of north-eastern and central Poland. Previous studies of the gastrointestinal parasite community in Polish primitive horses and species composition of these parasites were carried out only at separate farms and involved smaller number of animals (Gawor, 2000; Romaniuk et al., 2001, 2002, 2003; Slivinska et al., 2009, 2010, 2013). The present study included 124 horses, which composed more than a half of the Polish primitive horse population existing in Poland. Thus, the results obtained in our survey can adequately characterize the current state of infection of these horses with gastrointestinal parasites. The level of infections with gastrointestinal helminthes in Polish primitive horses, using the McMaster method (EPG values) in our study were rather low. The prevalence of strongylid infections close to 100 %, an average EPG value of 870.9, and did not exceed 2 – 3 thousand EPG in the most “contaminated” farms. At the same time, studies of Polish primitive horses carried out in previous years indicated the levels of infections with strongylids of more than 3 – 4,000 EPG, and even up to 15,700 EPG (Romaniuk et al., 2001, 2002, 2003). The level of infection with P. equorum also has decreased in recent years from more than 500 EPG to about 200 EPG (Romaniuk et al., 2001; Slivinska et al., 2013). We believe that such a decrease in infections with the gastrointestinal parasites is primarily due to regular, or even periodic, deworming with highly effective macrocyclic lactone anthelmintic drugs.

The most abundant and pathogenic parasites of the Polish primitive horses documented in this study were strongylids (with a prevalence from 95.2 % with coprological examinations to 100 % in the diagnostic deworming studies) and parascarids (with a prevalence up to 30 %) (Table 2). Oxyuris equi, S. westeri and H. muscae were detected less frequently and do not have such pathogenic effects on horses as do strongylids and parascarids (Renemey & Nielsen, 2013). Habronema muscae has been previously reported in domestic horses in Poland with prevalence of 8 % (Gawor, 1995). Data on prevalence or intensity of infection with H. muscae in Polish primitive horses was not found in the literature before our studies (Slivinska et al., 2013). In our opinion, lack of information about Habronema in this indigenous horse breed is connected with methods which were used to collect parasites previously. Traditional quantitative and qualitative coprological methods of examination are not sensitive enough to detect Habronema eggs, but traditional methods of post mortem examination previously were not used to study parasites of the Polish primitive horses. Application of the diagnostic deworming method allowed us to collect H. muscae adults and obtain the first data on prevalence of these nematodes in Polish primitive horses. The situation with S. westeri is similar to that with Habronema – even strongyliodosis was detected in domestic foals in Poland (Gawor, 1995; Sokół et al., 2015), information about prevalence of these nematodes in the Polish primitive horses was not available before our studies. Cestodes (A. perfoliata) were found only in horses from five farms in the north-eastern regions of Poland. The botfly G. intestinalis larvae were observed at seven farms, but their number was low (less than 4 specimens per horse on average). Our data on prevalence of G. intestinalis were similar to previous findings in domestic horses in Poland (from 33 – 40 % to 47 %) (Gawor, 1995; Romaniuk & Niedzwiedz et al., 2013), but lower than in southern regions of Europe – more than 80 % in Italy or south of Russia (Egri et al., 1995; Otranto et al., 2005). Minimal data in regard to the presence of G. intestinalis in Polish primitive horses are available in the literature (Romaniuk & Snarska, 2002); however their results are not comparable with our present data.

The gastrointestinal parasites we found in the Polish primitive horses are typical parasites of wild and indigenous breeds of horses in Poland and elsewhere in Europe (Romaniuk et al., 1983, 2001, 2002, 2003; Gawor, 2000; Francisco et al., 2009; Kuzmina et al., 2009, 2011). We documented more species of intestinal strongylids reported in previous studies in Polish primitive horses (Gawor, 2000; Slivinska et al., 2009). Perhaps this was due to a larger geographic study area utilized in this present study, which included horses from nine farms in four regions of Poland.

In our studies, significant differences in gastrointestinal parasite communities associated with sex were observed only for the intestinal strongylids: females (mares and fillies) had significantly higher numbers of strongylids as compared to stallions and colts, using both the coprological examination data and the diagnostic deworming data (Table 3). Similar differences related to sex of horses were reported by other authors (Bucknell et al., 1995; Romaniuk et al., 2004; Fikru et al., 2005; Francisco et al., 2009; Kornas et al., 2010). In our opinion, such differences were primarily due to inequality of management strategies – traditionally on brood horse farms mares and foals are kept and graze in groups, while stallions, even young ones, are separated from the main herd. This reduces the possibility of parasite exchange between stallions and mares and, consequently, decreases the infection of the former with strongylids transmitted through pasture grazing (Reinemeyer & Nielsen, 2013). However, analysis of combined influences of sex and management strategies (which were performed on our data) documented that such correlations were found to be insignificant in the Polish primitive horses. We believe that for indigenous horses, the external factors such as management strategies affect the infection levels much more than internal factors. For the other parasites, significant differences in their infection associated with sex were not observed.

Significant differences with infection of intestinal parasites associated with age were observed only for Strongylidae, P. equorum and O. equi (Table 3). Our data are consistent with similar observations on brood domestic horses (Hoglund et al., 1997; Lind et al., 1999; Larsen et al., 2002; Kornas et al., 2010; Kuzmina, 2012), and support the concept on the development of anti-parasite immunity in horses with age (Klei & Chapman, 1999). Concerning H. muscae, A. perfoliata and G. intestinalis, significant differences in the levels of infection of horses of different ages were not detected.

The more obvious differences in parasite infections in Polish primitive horses in our study were associated with the management strategies. The FR horses at all farms examined had higher levels of strongylid infection. In our opinion this finding was primarily associated with infrequent or absent anthelmintic treatments. On the contrary, more frequent deworming in ST horses resulted in a lower EPG values and poorer species biodiversity of the intestinal parasites. In the analysis of species composition of the strongylid communities we found that ST horses harbored the lowest number of species of these nematodes (15), while the highest species biodiversity (30 or 31) was documented in FR horses. Our findings correspond to the results of other authors who conducted similar studies in Poland (Kornas et al., 2006; Pilarczyk et al., 2010), as well as in other countries (Hoglund et al., 1997; Lind et al., 1999; Larsen et al., 2002; Kuzmina et al., 2007, 2009, 2011; Kuzmina, 2012).

The results of our survey of gastrointestinal parasite infections in Polish primitive horses depending on their age, sex and, especially, management strategies should be taken into account in elaboration of parasite control programs on farms and, in particular, during transportation of horses between farms to prevent spreading of parasites. Taking into account a high resilience of the Polish primitive horses to infection with different groups of gastrointestinal parasites (Romaniuk et al., 2007; Romaniuk & Jaworski, 2007), as well as the specificity of their management strategies, especially on FR farms, the methods of parasite control (mostly deworming) must not be done too often and, best done, after monitoring studies of the parasite infections. This will prevent the development and spreading of anthelmintic resist intestinal parasites.