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The incidence and species composition of Gasterophilus (Diptera, Gasterophilidae) causing equine myiasis in northern Xinjiang, China
Veterinary Parasitology 217 (2016) 36–38
Contents lists available at ScienceDirect
Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar
Short communication
The incidence and species composition of Gasterophilus (Diptera, Gasterophilidae) causing equine myiasis in northern Xinjiang, China Shan-Hui Liu, Kai Li ∗,1 , De-Fu Hu ∗ Key Laboratory of Non-invasive Research Technology for Endangered Species, College of Nature Conservation, Beijing Forestry University, Beijing 100083, PR China
a r t i c l e
i n f o
Article history: Received 3 October 2015 Received in revised form 26 December 2015 Accepted 28 December 2015 Keywords: Przewalski’s horse Mongolian wild ass Sympatry Gasterophilus Myiasis
a b s t r a c t A survey was conducted on the detection of the larval Gasterophilus species in 90 equines via necropsy or after administering oral ivermectin in Xinjian, China, from 2008 to 2013. All 90 (100%) equines were infested by larval Gasterophilus, and 3723 second instar larvae (L2) and 63,778 third instar larvae (L3) were collected from faecal samples and the digestive tract, a ratio of L2:L3 = 1:17. Over 84.45% of the animals contained ≤1500 larvae and 7.78% had >2000 larvae. The highest totals of L2 and L 3 larvae in any one animal were 1208 in Mongolian wild ass (Equus hemionus hemionus), 2491 in Przewalski’s horse (Equus ferus przewalskii), and 1785 in the domestic horse (Equus ferus caballus). Six species of Gasterophilus were identified, with the following proportions of overall parasite abundance: Gasterophilus pecorum 88.94%, Gasterophilus nigricornis 4.94%, Gasterophilus nasalis 3.93%, Gasterophilus haemorrhoidalis 1.91%, Gasterophilus intestinalis 0.19%, and Gasterophilus inermis 0.087%. A majority of equines (n = 32, 35.57%) was infested with five Gasterophilus species, while 29 animals (32.22%) harboured four species, 13 animals (14.44%) had six, 12 animals (13.33%) had three, three (3.33%) had two, and one (1.11%) had only one species. The percentage of Przewalski’s horses infested was higher than local domestic horse or Mongolian wild ass. © 2015 Elsevier B.V. All rights reserved.
1. Introduction The Kalamaili Nature Reserve (KNR) in Xinxiang, China is one of the few places in the world where the habitats of different wild equids overlap, and is an important area where Przewalski’s horse, Mongolian wild ass, and domestic horse live sympatrically, and share pastures seasonally. The larvae of flies of the genus Gasterophilus are common obligate parasites of the equids gastrointestinal tract (Zumpt, 1965). The genus Gasterophilus includes nine species of flies whose larvae cause gastrointestinal myiasis in equids. Six of the nine known Gasterophilus species occur in China: Gasterophilus pecorum, Gasterophilus nasalis, Gasterophilus nigricornis, Gasterophilus haemorrhoidalis, Gasterophilus intestinalis, and Gasterophilus inermis (Li et al., 2007; Liu, 2012). Gasterophilosis epidemics in the desert steppe of Xinjiang, China, have been reported to be quite severe and to have caused health problems
in Przewalski’s horse, a single individual was even infested by all six Gasterophilus species (Li et al., 2007; Liu, 2012). Although these parasites are considered to be well tolerated by the host, they have been incriminated in inducing gastric erosions, ulcers, ruptures, and debilitation with heavy infestation, which sometimes prove fatal (Hall and Wall, 1995). Gasterophiliidae species can severely affect wild ruminant welfare and animal production in the tropics and subtropics, especially in rural and less developed areas (Korna´s et al., 2006), where they may cause significant economic losses to the livestock industry. This present study exploited updated information on Gasterophilus spp. larvae infecting equines in China, with the aims of elucidating the mechanism behind the differences in infection levels of Gasterophilus among three host species, and providing additional insight into the dynamics of infection with the different Gasterophilus spp. 2. Materials and methods
∗ Corresponding authors at: At College of Nature Conservation, Beijing Forestry University, Beijing 100083, P. R. China. E-mail addresses: likai [email protected] (K. Li), [email protected], [email protected] (D.-F. Hu). 1 Contributed equally to this work. http://dx.doi.org/10.1016/j.vetpar.2015.12.028 0304-4017/© 2015 Elsevier B.V. All rights reserved.
The KNR (latitude 44◦ 40 to 46◦ 0 N, longitude 88◦ 33 to 90◦ 0 E) consists mainly of the Gobi Desert and semi-desert and located between the Altai Range and Junggar Basin. The climate is characterised by a typical continental climate. Comparative data were collected from equines over an approximate 5 year period from
S.-H. Liu et al. / Veterinary Parasitology 217 (2016) 36–38
37
Fig. 1. The intensity, abundance, and prevalence of Gasterophilus from on sympatric. Equids. Abbreviations: Przewalski’s horses (Ph); Domestic horses (Dh); Mongolian wild ass (Mw); G. haemorrhoidalis (Gh); G. intestinalis (Gi); G. nasalis (Gn); G. pecorum (Gp); G. inermis (Gin) and G. nigricornis (Gni); second instar larval (L2); third instar larval (L3). (a) Different groups of equines infested by the percentage of Gasterophilus species; (b) The percentage of different equid were infested by different categories Gasterophilus species; (c) The percentage equines who was infested; (d) Range in intensity of the Gasterophilus infestations per individual equine;
September 2008 to February 2013 to identify the species composition, intensity, abundance, and prevalence of Gasterophilus infesting equines Gasterophilus. Anti-parasitic drug treatment was performed on 77 equids (49 Przewalski’s horses and 28 domestic horses), where Gasterophilus larvae were collected and counted for 4 days in all fecal samples of each horse after from ivermectin administration. The necropsy was carried out in entire digestive tract (from the oesophagus to the rectum, at.) from 9 accidentally died equids (7 Mongolian wild asses and 2 Przewalski’s horses) and 4 equids slaughtered (domestic horses) that live sympatrically, where larvae were observed. All collected larvae were identified morphologically based on the peritreme structures on the surface of the segments using the description of Zumpt (1965). Details of the age, sex, type, and recent origin of each horse were recorded. Table 1 shows the number and percentage of positive and negative equids, grouped according to age and sex. 3. Results All 90 (100%) equines studied were infested by Gasterophilus larvae. a total of 3723 second instar larvae (L2) and 63,778 third instar larvae (L3) were found, at a ratio of L2:L3 = 1:17. G. pecorum was the most common species (88.94%), comprising 93.65% of the para-
Table 1 Number and percentage of infested equids grouped according to age and sex. Variable
Ph
Total
n 51
% 100%
n 32
% 100%
n 7
% 100.%
24 27 1 20 18 12
46.30% 53.70% 2.50% 43.90% 34.10% 19.50%
28 4 0 5 7 20
85.20% 14.80% 0% 18.50% 18.50% 63.00%
4 3 0 2 5 0
57.14% 42.86% 0.00% 28.57% 71.43% 0.00%
Sex Ages
Male Female <2 years 2–4 years 4–6 years >6 years
Dh
Mw
Abbreviations: n, number of infested equines; Przewalski’s horses (Ph); domestic horses (Dh); Mongolian wild ass (Mw).
sites found in Mongolian wild asses, 89.90% of those in Przewalski’s horses, and 74.78% of those in local domestic horses (Fig. 1(a)). The average proportion of the overall parasite diversity in all equines represented by each species was 88.94% for G. pecorum, 4.94% for G. nigricornis, 3.93% for G. nasalis, 1.91% for G. haemorrhoidalis, 0.19% for G. intestinalis, and 0.087% for G. inermis. Parasites varied in both species identity and abundance among the equines, as summarised in Fig. 1(b). Most animals were infested by five (35.57%) or four (32.22%) Gasterophilus species, although 13 (14.44%) animals were
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S.-H. Liu et al. / Veterinary Parasitology 217 (2016) 36–38
infested by six species, 12 (13.33%) by three species, 3 (3.33%) by two species, and one (1.11%) by only one species. G. pecorum and G. inermis had the highest and lowest infestation rate in the three equines, respectively. These results are detailed in Fig. 1(c). The ranked infestation severity in the 90 equids examined is given in Fig. 1(d). When the larval burdens of all species were combined, over 66.67% animals had up to 1500 larvae, while 7.78% equines had over 2000 larvae. The infestations were greater in Przewalski’s horses than in domestic horses and wild asses. 4. Discussion Six of the nine known Gasterophilus species occur in equine from KNR, China. Most equines were infested by five (35.57%) or four (32.22%) Gasterophilus species (Fig. 1b). This species richness is greater than in other regions with infestations by two species (G. intestinalis and G. nasalis) reported in Jordan (Mukbel et al., 2001), Saudi Arabia (Anazi and Alyousif, 2011), Brazil (Felix et al., 2007); by three species (G. intestinalis, G. nasalis, and G. pecorum) in South Africa (Krecek et al., 1989) and Sanliurfa (Gökc¸en et al., 2008); by four species (G. nasalis, G. haemorrhoidalis, G. intestinalis, and G. inermis) in the Stavropol region of Russia (Egri et al., 1995); and by five species (G. nasalis, G. haemorrhoidalis, G. intestinalis, G. pecorum, and G. inermis) in Italy (Principato, 1989). The dominant species in the study area was G. pecorum, while G. intestinalis and G. nasalis are common elsewhere in the world (Zumpt, 1965). The oviposition site selection behaviour of G. pecorum provides better opportunities for success in infesting a suitable host after hatching, and it reduces the chance of offspring dying due to lack of a host, explaining why it is the dominant species in the KNR (Liu et al., 2015). The diversity of the species composition of Gasterophilus in the region are the result of multiple factors. First, there are seven kinds of equine in worldwide, including four African and three Asian species and three kinds of them are sympatric in KNR. Owing to food and water shortages, their ranges have a high degree of overlap, increasing the probability of cross-infection. Second, the region is located in the Junggar Basin and the arid desert steppe of the Mongolia border region, and is both the ancestral home of Przewalski’s horse and a major ancient Eurasian continental trade route, so this area became an important species evolution platform for equine. Furthermore, the 100% occurrence rate of Gasterophilus spp. larvae in this study exceeds the 94% reported from horses in Italy (Principato, 1989), 43% in Ireland (Sweeney, 1990), and 9.9% in Sweden (Hoglund et al., 1997); similarly, it matches the 100% for donkeys in Burkina Faso (Kaboret et al., 1986), and exceeds the 97.5% for donkeys in Morocco (Pandey and Cabaret, 1993), 98.3% in Egypt (Hilali et al., 1987), and 88.6% in Jordan (Mukbel et al., 2001). Gp was the predominant species and its high prevalence was very different from all other countries. The mean intensity of infestation in Przewalski’s horses (1109 ± 157.6 parasites per individual) and wild donkeys (756.4 ± 169.1) in the region was much higher than in equines in the Republic of Turkey (409; Gökc¸en et al., 2008), the Stavropol region of Russia (35; Egri et al., 1995). This study evaluated the parasitic burden and parasite diversity from on sympatric equids in KNR of Xinxiang, China. The species composition of Gasterophilus and differences in the prevalence and larval burdens of Gasterophilus between horses and donkeys may be due to inherent differences in the susceptibility of the three host species, breed and age of the animals, parasite strains, geographic location, and the environment. Despite the sometimes high larval output, domestic horses and Mongolian wild asses appear to cope well with their respective parasitic loads. In comparison, Przewalski’s horses have obvious problems with parasitic infestation, as manifested
by diarrhoea, loss of weight, and coughing (Liu, 2012). However, Przewalski’s horses seem to cope very well with the sometimes high parasite burden in the Great Gobi “B” Strictly Protected Area, Mongolia (Painer et al., 2011). The reason of manifestation in different equids is these domestic equids in mongolia and Przewalski’s horses in china are handled occasionally by herders and monitor, and may suffer more from stress (Elias et al., 2002; Liu, 2012). The infestation status of parasites were investigated in wild equids, and the results may help with the management of both wild and captive populations. More details on the interactions among the three species, and the possible effects of these interactions on parasite burden are interesting topics for future research. Acknowledgements We would like to thank the KNR for providing all the samples used in this study. This work was mainly funded by the Project for New Century Excellent Talents in University (No. NCET-12-0783). References Anazi, Alyousif, 2011. Prevalence of non-strongyle gastrointestinal parasites of horses in Riyadh region of Saudi Arabia. Saudi J. Biol. Sci. 18, 299–303. Egri, B., Sárközy, P., Bánhidy, G., 1995. Prevance of botflies larval and lice in studs of north Caucasus acta (Stawropol County, Russia). Acta Vet. Hung. 43 (2-3), 287–289. Elias, F., Sterregaard, F., Baumgartner, R., et al., 2002. Parasitologic examinations in reintroduced Przewalski horses (Equus c. przewalskii) compared to mongolian domestic horses (E. caballus) and Dschiggetais (E. h. hemionus) in the Dzungarian Gobi. Mong. Pro. Eazwv Ewda., 233–240. Felix, S.R., Silva, C.E., Schmidtt, E., Nizoli, L.Q., Gotze, M.M., 2007. Presence of Gasterophilus (Leach, 1817) (Diptera, Oestridae) in horses in Rio Grande do Sul State. Brazil. Parasitol. Latinoam. 62 (3–4), 122–126. Gökc¸en, A., Sevgili, M., Altas¸, M., Camkerten, I., 2008. Presence of Gasterophilus species in Arabian horses in Sanliurfa region. Turkiye Parazitol. Derg. 32, 337–339. Hall, M.J.R., Wall, R., 1995. Myiasis of humans and domestic animals. Adv. Parasitol. 35, 257–334. Hilali, M., Derhalli, F.S., Baraka, A., 1987. Incidence and monthly prevalence of Gasterophilus spp. Larvae (Diptera: Gasterophilidae) in the stomach of donkeys (Equus asinus) in Egypt. Vet Parasitol. 23, 297–305. Hoglund, J., Ljungstrom, B.L., Nilsson, O., 1997. Occurrence of Gasterophilus intestinalis and some parasitic nematodes of horses in Sweden. Acta. Vet. Scand. 38, 157–165. Kaboret, Y., Pangui, L.J., Vercruysse, J., 1986. Note surla gasterophilose des anes au Burkina Faso. Rev. Elev. Med. Vet. Pays. Trop. 39, 211–212. Korna´s, S., Gawor, J., Skalska, M., Nowosad, B., 2006. Occurrence of botfly in horses from small farms. Med. Weter. 62, 452–454. Krecek, R.C., Reinecke, R.K., Horak, L.G., 1989. Internal parasites of horses on mixed grassveld and bushveld in Transvaal, Republic of South Africa. Vet. Parasitol. 34, 135–143. Li, K., Wu, Z., Hu, D.F., 2007. The new pathogens (Gasterophilus spp.) reports of Przewalski horses (Equus przewalskii) gastric myiasis in China. Anim. Husb. Vet. Sci. 38 (8), 837–840. Liu, S.H., 2012. Morphology and epidemiological investigation and the mitochondrial Cytochrome Oxidase I (COI) and 16 S rRNA gene phylogenetic of Gasterophilus. Beijing forestry university. PP 54-56. This is an postgraduate dissertation. Liu, S.H., Hu, D.F., Li, K., 2015. Oviposition site selection by Gasterophilus pecorum (Diptera: Gasterophilidae) in its habitat in Kalamaili Nature Reserve, Xinjiang, China. Parasite 22, 34, http://dx.doi.org/10.1051/parasite/2015034. Mukbel, R., Torgorson, P.R., Abo-Shehada, M., 2001. Seasonal variations in the abundance of Gasterophilus spp: larvae in donkey in northern Jordan. Trop. Anim. Health Prod. 33, 501–509. Painer, J., Kaczensky, P., Ganbaatar, O., et al., 2011. Comparative parasitological examination on sympatric equids in the great Gobi “B” strictly protected area, Mongolia. Eur. J. Wildlife Res. 57, 225–232. Pandey, V.S., Cabaret, J., 1993. Stomach parasites of donkeys in Morocco: habitat and interspecific interactions. Vet. Parasitol. 49, 331–337. Principato, M., 1989. Observations on the occurrence of five species of Gasterophilus larvae in free-ranging horses in Umbria, central Italy. Vet. Parasitol. 31, 173–177. Sweeney, H.J., 1990. The prevalence and pathogenicity of Gasterophilus intestinalis larvae in horses in Ireland. Irish Vet. J. 43, 67–73. Zumpt, F., 1965. Myiasis in Man and Animals of the Old World. Butterworths, London.
Contents lists available at ScienceDirect
Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar
Short communication
The incidence and species composition of Gasterophilus (Diptera, Gasterophilidae) causing equine myiasis in northern Xinjiang, China Shan-Hui Liu, Kai Li ∗,1 , De-Fu Hu ∗ Key Laboratory of Non-invasive Research Technology for Endangered Species, College of Nature Conservation, Beijing Forestry University, Beijing 100083, PR China
a r t i c l e
i n f o
Article history: Received 3 October 2015 Received in revised form 26 December 2015 Accepted 28 December 2015 Keywords: Przewalski’s horse Mongolian wild ass Sympatry Gasterophilus Myiasis
a b s t r a c t A survey was conducted on the detection of the larval Gasterophilus species in 90 equines via necropsy or after administering oral ivermectin in Xinjian, China, from 2008 to 2013. All 90 (100%) equines were infested by larval Gasterophilus, and 3723 second instar larvae (L2) and 63,778 third instar larvae (L3) were collected from faecal samples and the digestive tract, a ratio of L2:L3 = 1:17. Over 84.45% of the animals contained ≤1500 larvae and 7.78% had >2000 larvae. The highest totals of L2 and L 3 larvae in any one animal were 1208 in Mongolian wild ass (Equus hemionus hemionus), 2491 in Przewalski’s horse (Equus ferus przewalskii), and 1785 in the domestic horse (Equus ferus caballus). Six species of Gasterophilus were identified, with the following proportions of overall parasite abundance: Gasterophilus pecorum 88.94%, Gasterophilus nigricornis 4.94%, Gasterophilus nasalis 3.93%, Gasterophilus haemorrhoidalis 1.91%, Gasterophilus intestinalis 0.19%, and Gasterophilus inermis 0.087%. A majority of equines (n = 32, 35.57%) was infested with five Gasterophilus species, while 29 animals (32.22%) harboured four species, 13 animals (14.44%) had six, 12 animals (13.33%) had three, three (3.33%) had two, and one (1.11%) had only one species. The percentage of Przewalski’s horses infested was higher than local domestic horse or Mongolian wild ass. © 2015 Elsevier B.V. All rights reserved.
1. Introduction The Kalamaili Nature Reserve (KNR) in Xinxiang, China is one of the few places in the world where the habitats of different wild equids overlap, and is an important area where Przewalski’s horse, Mongolian wild ass, and domestic horse live sympatrically, and share pastures seasonally. The larvae of flies of the genus Gasterophilus are common obligate parasites of the equids gastrointestinal tract (Zumpt, 1965). The genus Gasterophilus includes nine species of flies whose larvae cause gastrointestinal myiasis in equids. Six of the nine known Gasterophilus species occur in China: Gasterophilus pecorum, Gasterophilus nasalis, Gasterophilus nigricornis, Gasterophilus haemorrhoidalis, Gasterophilus intestinalis, and Gasterophilus inermis (Li et al., 2007; Liu, 2012). Gasterophilosis epidemics in the desert steppe of Xinjiang, China, have been reported to be quite severe and to have caused health problems
in Przewalski’s horse, a single individual was even infested by all six Gasterophilus species (Li et al., 2007; Liu, 2012). Although these parasites are considered to be well tolerated by the host, they have been incriminated in inducing gastric erosions, ulcers, ruptures, and debilitation with heavy infestation, which sometimes prove fatal (Hall and Wall, 1995). Gasterophiliidae species can severely affect wild ruminant welfare and animal production in the tropics and subtropics, especially in rural and less developed areas (Korna´s et al., 2006), where they may cause significant economic losses to the livestock industry. This present study exploited updated information on Gasterophilus spp. larvae infecting equines in China, with the aims of elucidating the mechanism behind the differences in infection levels of Gasterophilus among three host species, and providing additional insight into the dynamics of infection with the different Gasterophilus spp. 2. Materials and methods
∗ Corresponding authors at: At College of Nature Conservation, Beijing Forestry University, Beijing 100083, P. R. China. E-mail addresses: likai [email protected] (K. Li), [email protected], [email protected] (D.-F. Hu). 1 Contributed equally to this work. http://dx.doi.org/10.1016/j.vetpar.2015.12.028 0304-4017/© 2015 Elsevier B.V. All rights reserved.
The KNR (latitude 44◦ 40 to 46◦ 0 N, longitude 88◦ 33 to 90◦ 0 E) consists mainly of the Gobi Desert and semi-desert and located between the Altai Range and Junggar Basin. The climate is characterised by a typical continental climate. Comparative data were collected from equines over an approximate 5 year period from
S.-H. Liu et al. / Veterinary Parasitology 217 (2016) 36–38
37
Fig. 1. The intensity, abundance, and prevalence of Gasterophilus from on sympatric. Equids. Abbreviations: Przewalski’s horses (Ph); Domestic horses (Dh); Mongolian wild ass (Mw); G. haemorrhoidalis (Gh); G. intestinalis (Gi); G. nasalis (Gn); G. pecorum (Gp); G. inermis (Gin) and G. nigricornis (Gni); second instar larval (L2); third instar larval (L3). (a) Different groups of equines infested by the percentage of Gasterophilus species; (b) The percentage of different equid were infested by different categories Gasterophilus species; (c) The percentage equines who was infested; (d) Range in intensity of the Gasterophilus infestations per individual equine;
September 2008 to February 2013 to identify the species composition, intensity, abundance, and prevalence of Gasterophilus infesting equines Gasterophilus. Anti-parasitic drug treatment was performed on 77 equids (49 Przewalski’s horses and 28 domestic horses), where Gasterophilus larvae were collected and counted for 4 days in all fecal samples of each horse after from ivermectin administration. The necropsy was carried out in entire digestive tract (from the oesophagus to the rectum, at.) from 9 accidentally died equids (7 Mongolian wild asses and 2 Przewalski’s horses) and 4 equids slaughtered (domestic horses) that live sympatrically, where larvae were observed. All collected larvae were identified morphologically based on the peritreme structures on the surface of the segments using the description of Zumpt (1965). Details of the age, sex, type, and recent origin of each horse were recorded. Table 1 shows the number and percentage of positive and negative equids, grouped according to age and sex. 3. Results All 90 (100%) equines studied were infested by Gasterophilus larvae. a total of 3723 second instar larvae (L2) and 63,778 third instar larvae (L3) were found, at a ratio of L2:L3 = 1:17. G. pecorum was the most common species (88.94%), comprising 93.65% of the para-
Table 1 Number and percentage of infested equids grouped according to age and sex. Variable
Ph
Total
n 51
% 100%
n 32
% 100%
n 7
% 100.%
24 27 1 20 18 12
46.30% 53.70% 2.50% 43.90% 34.10% 19.50%
28 4 0 5 7 20
85.20% 14.80% 0% 18.50% 18.50% 63.00%
4 3 0 2 5 0
57.14% 42.86% 0.00% 28.57% 71.43% 0.00%
Sex Ages
Male Female <2 years 2–4 years 4–6 years >6 years
Dh
Mw
Abbreviations: n, number of infested equines; Przewalski’s horses (Ph); domestic horses (Dh); Mongolian wild ass (Mw).
sites found in Mongolian wild asses, 89.90% of those in Przewalski’s horses, and 74.78% of those in local domestic horses (Fig. 1(a)). The average proportion of the overall parasite diversity in all equines represented by each species was 88.94% for G. pecorum, 4.94% for G. nigricornis, 3.93% for G. nasalis, 1.91% for G. haemorrhoidalis, 0.19% for G. intestinalis, and 0.087% for G. inermis. Parasites varied in both species identity and abundance among the equines, as summarised in Fig. 1(b). Most animals were infested by five (35.57%) or four (32.22%) Gasterophilus species, although 13 (14.44%) animals were
38
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infested by six species, 12 (13.33%) by three species, 3 (3.33%) by two species, and one (1.11%) by only one species. G. pecorum and G. inermis had the highest and lowest infestation rate in the three equines, respectively. These results are detailed in Fig. 1(c). The ranked infestation severity in the 90 equids examined is given in Fig. 1(d). When the larval burdens of all species were combined, over 66.67% animals had up to 1500 larvae, while 7.78% equines had over 2000 larvae. The infestations were greater in Przewalski’s horses than in domestic horses and wild asses. 4. Discussion Six of the nine known Gasterophilus species occur in equine from KNR, China. Most equines were infested by five (35.57%) or four (32.22%) Gasterophilus species (Fig. 1b). This species richness is greater than in other regions with infestations by two species (G. intestinalis and G. nasalis) reported in Jordan (Mukbel et al., 2001), Saudi Arabia (Anazi and Alyousif, 2011), Brazil (Felix et al., 2007); by three species (G. intestinalis, G. nasalis, and G. pecorum) in South Africa (Krecek et al., 1989) and Sanliurfa (Gökc¸en et al., 2008); by four species (G. nasalis, G. haemorrhoidalis, G. intestinalis, and G. inermis) in the Stavropol region of Russia (Egri et al., 1995); and by five species (G. nasalis, G. haemorrhoidalis, G. intestinalis, G. pecorum, and G. inermis) in Italy (Principato, 1989). The dominant species in the study area was G. pecorum, while G. intestinalis and G. nasalis are common elsewhere in the world (Zumpt, 1965). The oviposition site selection behaviour of G. pecorum provides better opportunities for success in infesting a suitable host after hatching, and it reduces the chance of offspring dying due to lack of a host, explaining why it is the dominant species in the KNR (Liu et al., 2015). The diversity of the species composition of Gasterophilus in the region are the result of multiple factors. First, there are seven kinds of equine in worldwide, including four African and three Asian species and three kinds of them are sympatric in KNR. Owing to food and water shortages, their ranges have a high degree of overlap, increasing the probability of cross-infection. Second, the region is located in the Junggar Basin and the arid desert steppe of the Mongolia border region, and is both the ancestral home of Przewalski’s horse and a major ancient Eurasian continental trade route, so this area became an important species evolution platform for equine. Furthermore, the 100% occurrence rate of Gasterophilus spp. larvae in this study exceeds the 94% reported from horses in Italy (Principato, 1989), 43% in Ireland (Sweeney, 1990), and 9.9% in Sweden (Hoglund et al., 1997); similarly, it matches the 100% for donkeys in Burkina Faso (Kaboret et al., 1986), and exceeds the 97.5% for donkeys in Morocco (Pandey and Cabaret, 1993), 98.3% in Egypt (Hilali et al., 1987), and 88.6% in Jordan (Mukbel et al., 2001). Gp was the predominant species and its high prevalence was very different from all other countries. The mean intensity of infestation in Przewalski’s horses (1109 ± 157.6 parasites per individual) and wild donkeys (756.4 ± 169.1) in the region was much higher than in equines in the Republic of Turkey (409; Gökc¸en et al., 2008), the Stavropol region of Russia (35; Egri et al., 1995). This study evaluated the parasitic burden and parasite diversity from on sympatric equids in KNR of Xinxiang, China. The species composition of Gasterophilus and differences in the prevalence and larval burdens of Gasterophilus between horses and donkeys may be due to inherent differences in the susceptibility of the three host species, breed and age of the animals, parasite strains, geographic location, and the environment. Despite the sometimes high larval output, domestic horses and Mongolian wild asses appear to cope well with their respective parasitic loads. In comparison, Przewalski’s horses have obvious problems with parasitic infestation, as manifested
by diarrhoea, loss of weight, and coughing (Liu, 2012). However, Przewalski’s horses seem to cope very well with the sometimes high parasite burden in the Great Gobi “B” Strictly Protected Area, Mongolia (Painer et al., 2011). The reason of manifestation in different equids is these domestic equids in mongolia and Przewalski’s horses in china are handled occasionally by herders and monitor, and may suffer more from stress (Elias et al., 2002; Liu, 2012). The infestation status of parasites were investigated in wild equids, and the results may help with the management of both wild and captive populations. More details on the interactions among the three species, and the possible effects of these interactions on parasite burden are interesting topics for future research. Acknowledgements We would like to thank the KNR for providing all the samples used in this study. This work was mainly funded by the Project for New Century Excellent Talents in University (No. NCET-12-0783). References Anazi, Alyousif, 2011. Prevalence of non-strongyle gastrointestinal parasites of horses in Riyadh region of Saudi Arabia. Saudi J. Biol. Sci. 18, 299–303. Egri, B., Sárközy, P., Bánhidy, G., 1995. Prevance of botflies larval and lice in studs of north Caucasus acta (Stawropol County, Russia). Acta Vet. Hung. 43 (2-3), 287–289. Elias, F., Sterregaard, F., Baumgartner, R., et al., 2002. Parasitologic examinations in reintroduced Przewalski horses (Equus c. przewalskii) compared to mongolian domestic horses (E. caballus) and Dschiggetais (E. h. hemionus) in the Dzungarian Gobi. Mong. Pro. Eazwv Ewda., 233–240. Felix, S.R., Silva, C.E., Schmidtt, E., Nizoli, L.Q., Gotze, M.M., 2007. Presence of Gasterophilus (Leach, 1817) (Diptera, Oestridae) in horses in Rio Grande do Sul State. Brazil. Parasitol. Latinoam. 62 (3–4), 122–126. Gökc¸en, A., Sevgili, M., Altas¸, M., Camkerten, I., 2008. Presence of Gasterophilus species in Arabian horses in Sanliurfa region. Turkiye Parazitol. Derg. 32, 337–339. Hall, M.J.R., Wall, R., 1995. Myiasis of humans and domestic animals. Adv. Parasitol. 35, 257–334. Hilali, M., Derhalli, F.S., Baraka, A., 1987. Incidence and monthly prevalence of Gasterophilus spp. Larvae (Diptera: Gasterophilidae) in the stomach of donkeys (Equus asinus) in Egypt. Vet Parasitol. 23, 297–305. Hoglund, J., Ljungstrom, B.L., Nilsson, O., 1997. Occurrence of Gasterophilus intestinalis and some parasitic nematodes of horses in Sweden. Acta. Vet. Scand. 38, 157–165. Kaboret, Y., Pangui, L.J., Vercruysse, J., 1986. Note surla gasterophilose des anes au Burkina Faso. Rev. Elev. Med. Vet. Pays. Trop. 39, 211–212. Korna´s, S., Gawor, J., Skalska, M., Nowosad, B., 2006. Occurrence of botfly in horses from small farms. Med. Weter. 62, 452–454. Krecek, R.C., Reinecke, R.K., Horak, L.G., 1989. Internal parasites of horses on mixed grassveld and bushveld in Transvaal, Republic of South Africa. Vet. Parasitol. 34, 135–143. Li, K., Wu, Z., Hu, D.F., 2007. The new pathogens (Gasterophilus spp.) reports of Przewalski horses (Equus przewalskii) gastric myiasis in China. Anim. Husb. Vet. Sci. 38 (8), 837–840. Liu, S.H., 2012. Morphology and epidemiological investigation and the mitochondrial Cytochrome Oxidase I (COI) and 16 S rRNA gene phylogenetic of Gasterophilus. Beijing forestry university. PP 54-56. This is an postgraduate dissertation. Liu, S.H., Hu, D.F., Li, K., 2015. Oviposition site selection by Gasterophilus pecorum (Diptera: Gasterophilidae) in its habitat in Kalamaili Nature Reserve, Xinjiang, China. Parasite 22, 34, http://dx.doi.org/10.1051/parasite/2015034. Mukbel, R., Torgorson, P.R., Abo-Shehada, M., 2001. Seasonal variations in the abundance of Gasterophilus spp: larvae in donkey in northern Jordan. Trop. Anim. Health Prod. 33, 501–509. Painer, J., Kaczensky, P., Ganbaatar, O., et al., 2011. Comparative parasitological examination on sympatric equids in the great Gobi “B” strictly protected area, Mongolia. Eur. J. Wildlife Res. 57, 225–232. Pandey, V.S., Cabaret, J., 1993. Stomach parasites of donkeys in Morocco: habitat and interspecific interactions. Vet. Parasitol. 49, 331–337. Principato, M., 1989. Observations on the occurrence of five species of Gasterophilus larvae in free-ranging horses in Umbria, central Italy. Vet. Parasitol. 31, 173–177. Sweeney, H.J., 1990. The prevalence and pathogenicity of Gasterophilus intestinalis larvae in horses in Ireland. Irish Vet. J. 43, 67–73. Zumpt, F., 1965. Myiasis in Man and Animals of the Old World. Butterworths, London.