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.
Materials and Methods
Study areas and horses
Our study was carried out on nine farms with different types of management strategies from four regions of Poland (Fig. 1): the Warminsko-Mazurskie region – Popielno forest reserve (Popiel-no; 53°45′16.4″N; 21°37′42.1″E), Seven Island Lake Nature Reserve (Seven Island; 54°18’N 21°34’E), and a private ecological farm “Majdan” near Ruczane-Nida town (Majdan; 53°39′16″N 21°29′1″E); the Podlaskie region – the Bialowieza National Park (Bialowieza; 52°45′7.66″N 23°52′44.86″E), Biebrza National Park (Biebrza; 53°40′0”N, 22°46′0”E), Narew National Park (Narew; 53°03′00″N 22°24′15″E) and a private farm near Monki town (Monki; 53°24’N 22°48’E); Lubelskie region – Roztocze National Park (Roztocze; 50°21′55″N 22°34′48″E), and Lodzkie region – a breeding farm “Siriusz” near Lodz city (Siriusz; 51°47’N 19°28’E). Totally, 124 Polish primitive horses (96 females and 28 males) were included in this study during spring seasons in 2008 – 2012. According to the different types of management strategies, all horses were divided into three groups: 1) stabled horses (ST) (n=46); 2) semi-free horses (SF) (n=30), and 3) free-ranging horses (FR) (n=48). All horses examined were divided into three age groups: foals and horses less than 3 years old (n=53), horses from 3 to 10 years old (n=51) and old horses of more than 10 years old (n=20) (Table 1). All horses had natural levels of parasite infections and had not been treated with any anthelmintics at least for 3 month before the study began.
Number of Polish primitive horses (n=124) examined of different age groups from nine horse farms in Poland
|Farm||Location/Region||Types of horse management||Number of samples per age group|
|< 3 years||3 – 10 years||>10 years||Total|
Regions: W-M – Warminsko-Mazurskie region, PR – Podlaskie region, LBR – Lubelskie region, LR – Lodzkie region;
Types of horse management: ST – stabled horses, FR – free-ranging horses, SF – semi-free horses.
The level of horse infections with gastro-intestinal parasites was determined by the coprological McMaster technique with sensitivity of 25 eggs per gram of feces (EPG value) (Herd, 1992). Fresh fecal samples were collected per rectum from every individual horse, or from the ground.
Gastrointestinal parasites (nematodes and cestodes) were collected from every individual horse in vivo by the diagnostic deworming method after anthelmintic treatment (Kuzmina et al., 2005). All horses examined (except the horses from Popielno) were treated with Equimax paste (ivermectin, 18.7 mg + praziquantel, 140.3 mg, Virbac de Portugal Laboratorios LDA, Portugal) at a dose of 1.07 g of paste per 100 kg of body weight. Horses from the Popielno were treated with Abamitel-Plus (abamectin, 4 mg + praziquantel, 50 mg; Krka, Slovenia) at a dose of 1 ml paste per 20 kg of body weight. Fecal samples (200 g) containing expelled gastrointestinal parasites were collected from each horse 24, 36, and 48 hours after treatment. Samples were washed with tap water, pre-fixed in 40 % ethanol and kept in refrigerator (t°=+4 °C) until parasites were collected manually and fixed in 70 % ethanol. All helminthes collected were identified under a light microscope by morphological criteria (Ivashkin, Dvojnos, 1984; Dvojnos, Kharchenko, 1994; Lichtenfels et al., 2008). Before identification, the nematodes were clarified in phenol-glycerin solution (80 % phenol, 20 % glycerin). Totally, 66,192 parasite specimens were collected and identified.
Primer 6 software (Clarke, Gorley, 2006) was used for statistical analysis. Taking into account that expulsion of parasites (eggs and adults) into feces is not normally distributed, statistical analysis was performed using the nonparametric Kruskal-Wallis test with significant differences at p < 0.05.
Coprological examination of the Polish primitive horses showed that strongylid nematodes were the most prevalent parasites at all farms – 95.2 % of horses were infected with strongylids; eggs of Parascaris equorum were detected in 26.6 % and Strongyliodes westeri in 12.9 % (Table 2). Eggs of cestodes were not observed in the fecal samples examined. Analysis of the results revealed a dependence of levels of horse infections with intestinal nematodes (EPG value) with their sex, age and management strategies (Table 3). The level of infection with strongylids was significantly higher in females (average EPG = 923.9 ± 891.2 SD), than in males (average EPG = 591.3 ± 641.7 SD) (Kruskal-Wallis test; p <0 .05). However, if we include the management strategies (FR, SF ant ST) as a second factor, this dependence of strongylids infection with sex became insignificant (p > 0.05). Significant differences in the level of horse infections by P. equorum and S. westeri between sexes were not found (p > 0.05).
Prevalence (%) of infection with gastrointestinal parasites in Polish primitive horses (n=124) from nine farms in Poland: results of the fecal egg counts (EPG) and diagnostic deworming
|Farm/ Number of horses||Fecal egg count data, prevalence/EPG (average)||Diagnostic deworming data, prevalence in %|
|Strongylidae||P. equorum||S. westeri||Strongylidae||P. equorum||O. equi||H. muscae||A. perfoliata||G. intestinalis|
|Prev., %||EPG||Prev., %||EPG||Prev., %||EPG||Prev., %||No. of species|
|Popielno, ST (22)||100||1030.1||18.2||25.0||22.7||285||100||24||4.5||45.5||—||63.6||45.5|
|Popielno, FR (11)||100||684.1||63.6||28.6||27.3||250||100||25||63.6||100||18.2||72.7||90.9|
|Seven Isl., FR (11)||100||247.7||—||—||100||30||—||100||—||—||72.7|
|Majdan, SF (14)||100||1544.6||35.7||40.0||—||100||19||35.7||14.3||—||64.3||35.7|
|Bialowieza, SF (6)||100||387.5||—||—||100||18||—||—||—||100||—|
|Biebrza, FR (10)||100||1802.5||40.0||437.5||30.0||150||100||28||20||70||30||90||80|
|Narew, SF (2)||100||137.5||—||—||100||18||—||50||—||—||100|
|Monki, SF (8)||100||637.5||50.0||183.8||12.5||400||100||22||37.5||62.5||—||—||37.5|
|Roztocze, FR (16)||100||320.3||43.8||225||25.0||175||100||31||56.3||—||43.8||37.5||56.3|
|Roztocze, ST (13)||100||1021.2||15.4||350||—||100||24||38.5||—||69.2||7.7||23.1|
|Siriusz, ST (11)||40.0||131.3||—||—||100||15||10||—||—||—|
Types of horse management strategies: ST – stabled, SF – seml-free horses, FR – free-ranging horses
The dependence of gastrointestinal parasites infections in Polish primitive horses in regard to sex, age and management strategies: results of the Kruskal-Wallis test (H)
|EPG value data|
|Diagnostic deworming data|
Significant differences in strongyle egg counts (EPG) were not observed between horses from the three age groups (Kruskal-Wallis test; p > 0.05). For P. equorum, young horses (up to 3 years old) had significantly higher levels of infection as compared to older horses (p < 0.05). Eggs of S. westeri were detected only in fecal samples from young horses (<3 years old).
In regard to the management strategies, the significant differences in the EPG values were observed only for Strongylidae. For example, on the Popielno and Roztocze farms where horses were stabled and free-ranging, all FR horses had much higher levels of strongylid infection (aver. EPG = 1324.3 ± 973.8 SD) than ST horses (aver. EPG = 290.7 ± 225.1 SD). The level of strongylid infection in semi-free horses was intermediate. Significant relationships in infections with P. equorum and S. westeri and type of management strategies were not observed (Kruskal-Wallis test; p > 0.05) (Table 3).
Diagnostic deworming data
Results of the diagnostic deworming examination revealed presence of P. equorum (27.4 %), Oxyuris equi (38.7 %), Habronema muscae (16.9 %), Anoplocephala perfoliata (42.7 %) and Gasterophilus intestinalis (46.8 %) in the Polish primitive horses examined (Table 2). S. westeri was not found using this diagnostic deworming technique.
A similar analysis of the data on the number of parasites obtained by the diagnostic deworming technique compared to the sex, age groups and different management strategies of the horses also was carried out (Table 3). Similar to the EPG-value data, the Polish primitive horse females had a significantly higher infection with intestinal strongylids than males (Kruskal-Wallis test; p < 0.001). For others parasites (P. equorum, O. equi, H. muscae; A. perfoliata and G. intestinalis), statistically significant differences between infected males and females were not observed (p > 0.05). Significant correlations between the age of the horse and the level of infections were observed only for Strongylidae, P. equorum and O. equi. Polish primitive horses older than 10 years had significantly lower numbers of strongylids than younger horses. In contrast, P. equorum and O. equi were mostly found in young horses up to 3 years old (Kruskal-Wallis test; p < 0.05). Significant influence of the age of the horse with infections of H. muscae, A. perfoliata and G. intestinalis was not observed (p > 0.05) (Table 3).
The management strategies affected the level of parasite burdens only for strongylids, O. equi and the larvae of the gastric botfly G. intestinalis (Kruskal-Wallis test; p < 0.05). Free ranging horses had much higher number of strongylid nematodes collected in the fecal samples after the diagnostic deworming as compared to the ST and SF horses. The highest numbers of O. equi and larvae of G. intestinalis also were found in FR horses.
Prevalence of gastrointestinal parasite infections in Polish primitive horses (n=124) from nine farms: results of diagnostic deworming
|Farm/ Number of horses||Strongylidae||P. equorum||O. equi||H. muscae||A. perfoliata||G. intestinalis|
|Popielno, ST (22)||100||4.5||45.5||—||63.6||45.5|
|Popielno, FR (11)||100||63.6||100||18.2||72.7||90.9|
|Seven Isl., FR (11)||100||—||100||—||—||72.7|
|Majdan, SF (14)||100||35.7||14.3||—||64.3||35.7|
|Bialowieza, SF (6)||100||—||—||—||100||—|
|Biebrza, FR (10)||100||20||70||30||90||80|
|Narew, SF (2)||100||—||50||—||—||100|
|Monki, SF (8)||100||37.5||62.5||—||—||37.5|
|Roztocze, FR (16)||100||56.3||—||43.8||37.5||56.3|
|Roztocze, ST (13)||100||38.5||—||69.2||7.7||23.1|
|Siriusz, ST (11)||100||10||—||—||—||—|
Types of horse management strategies: ST – stabled, SF – semi-free, FR – free-ranging horses
Analysis of the strongylid community structure
Since intestinal strongylids were the most abundant group of parasites found in the Polish primitive horses in this study, the analysis of strongylid communities in horses of different sex, age groups and management strategies was performed. Totally, 31 species from 13 genera were identified: 6 species of large strongyles (subfamily Strongylinae) and 25 species of small strongyles (subfamily Cyathostominae). From 4 to 28 species were observed per horse (average 15.1 ± 5.1 SD).
Ten cyathostome species with the prevalence 80 – 100 % dominated the strongylid community of the Polish primitive horses; together they composed more than 93.5 % of the total number of strongylids collected. Large strongyles (Strongylinae) were found in 54.0 % of the horses examined: from 44.4 % for S. vulgaris to 8.8 % for C. acuticaudatum (Fig. 2). Prevalence of separate species of large strongyles varied in horses from different types of management strategies. Free ranging horses had the highest prevalence of large strongyles (75 % for S. vulgaris, 60.4 % for S. edentatus, 56.3 % for T. serratus); SR horses had the lowest prevalence of large strongyles (26.7 % for S. vulgaris, 6.6 % for S. edentatus, 0 % for T. serratus); prevalence of large strongyles in ST horses was intermediate (23.9 % for S. vulgaris, 26.1 % for S. edentatus, and 15.2 % for T. serratus).
Analysis of the influence of sex and age of horses to the strongylid community structure revealed that statistically significant differences in prevalence of the separate strongylid species or their proportion in communities were not observed between females and males, or between the three age groups (Kruskal-Wallis test; p > 0.05).
Species diversity in strongylid communities of the Polish primitive horses significantly differed between horse farms (Table 2). The lowest number of species (15) was found on the farm “Syriusz”, where the horses are kept in stables, and the maximum numbers of strongylid species (30 and 31) were found on farms Seven Island and Roztocze in FR horses.
The types of management strategies of the horses had substantial influence on the strongylid community structure. The FR horses had significantly higher prevalence of large strongyles (Strongylinae) and their proportion in the community was higher compared to horses from others types of management strategies (Kruskal-Wallis test; p < 0.05). Division of the strongylid species into 10 prevalence classes also showed apparent differences in the strongylid community structures between horses from FR, SF and ST conditions (Fig. 3).
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.
The authors thank colleagues from the I. I. Schmalhausen Institute of Zoology of the NAS of Ukraine, Dr. Igor I. Dzeverin for his valuable consultations on statistical analysis of the results, and Dr. Yuriy Kuzmin for his comments to the manuscript, and Prof. Terry R. Spraker from the Colorado State University, Fort Collins Colorado, USA, for his corrections to the manuscript. The authors thank all the staff of the Polish primitive horse farms and reserves for their assistance in field work.
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statistically significant results are marked in bold