Aus dem Forschungsinstitut für Wildtierkunde und Ökologie
der Veterinärmedizinischen Universität Wien
(Leitung: O.Univ.Prof. Dr.rer.nat. Walter ARNOLD)
Fach: Wildtiermedizin
COMPARATIVE PARASITOLOGICAL EXAMINATION ON SYMPATRIC
EQUIDS IN THE GREATER GOBI “B” STRICTLY PROTECTED AREA,
MONGOLIA
DIPLOMARBEIT
Zur Erlangung der Würde einer
MAGISTRA MEDICINAE VETERINARIAE
Der Veterinärmedizinischen Universität Wien
Vorgelegt von
Johanna Painer
Wien, im November 2009
Betreuer: Univ. Prof. Dr. med. vet. habil., Christian Walzer Arbeitsgruppe: Wildtiermedizin Forschungsinstitut für Wildtierkunde und Ökologie
Gutachterin: Univ. Prof. Dr. med. vet. habil., DipEVPC Anja Joachim Institut für Parasitologie und Zoologie Department für Pathobiologie
Inhaltsverzeichnis
Seite
1) Einleitung 01
2) Publikation (entsprechend dem Format von “Vet. Parasitol.“) 03 - 30 Abstract 03 Introduction 04 Material and Methods 06 Results 09 Discussion 11 Conclusion 17 Acknowledgements 18 References 18 Tables 22 Figures 23
3) Deutsche Zusammenfassung 31
4) English Summary 32
1
1) EINLEITUNG
Der Naturschutzpark der Großen Gobi „B“ im Südwesten der Mongolei gehört zu einem der wenigen Orte auf der Welt, wo Streifgebiete verschiedener Wild-Equiden überlappen und er ist das einzige Gebiet wo der Asiatische Wildesel und das Przewalskipferd sympatrisch leben und saisonbedingt ihre Weiden mit mongolischen Hauspferden teilen.
Das Przewalskipferd (Equus caballus przewalskii, in der Mongolei bekannt als „Takhi“, POLIAKOV 1881) lebte früher weit verbreitet in den Steppen des Zentralasiatischen Raumes. Im späten 19. Jahrhundert wurde es von der westlichen Welt entdeckt. Bis in das Jahr 1947 fanden Fang- und Transportaktionen für zoologischen Gärten statt. Zuletzt wurden wildlebende Individuen in der Dzungarischen Wüste, im südwestlichen Teil der Mongolei, gesichtet. In den späten 1960’er Jahren wurde das Przewalskipferd, als in der freien Wildbahn, für ausgestorben erklärt (Boyd and Houpt, 1994). Die Spezies wurde jedoch, basierend auf einer Gründerpopulation von nur 13 Individuen, sehr erfolgreich in ex-situ Projekten weltweit gezüchtet (Mohr and Volf, 1971). Erste Bemühungen für den Start des Wiedereinführungsprogramms fanden bereits 1979 statt, jedoch wurden erst 1992 die ersten Individuen zum Wiedereinführungsgebiet nach Takhin Tal (45.53.80 N, 93.65.22 E), im Südwesten der Mongolei, transportiert. Nachdem im Jahre 1999 die Internationale Takhi Gruppe (ITG) gegründet wurde, wurde das Projekt entsprechend den Wiedereinführungsrichtlinien der Weltnaturschutzunion (IUCN/SSC, 1998) erweitert (Walzer et al., 2004). Seit der Entstehung des Projekts wurden 89 Individuen aus 24 Zoologischen Gärten weltweit in das Gebiet transportiert (Kaczensky et al., 2005). Zu Beginn wurden die Przewalskipferde in Adaptionsgehegen gehalten, die erste Haremsgruppe wurde im Jahr 1997 in die freie Wildbahn entlassen (Walzer et al., 2004). Heute leben 145 freie Przewalskipferde in der Naturschutzregion, aufgeteilt in 10 Haremsgruppen und einer variierenden Anzahl an Junggesellengruppen (ITG, 2009, http://www.takhi.org).
Die Asiatische Wildeselpopulation (E. hemionus hemionus, örtlich bekannt als „Khulan“, PALLAS 1775) wird auf 19.000 bis 20.000 Individuen in der Mongolei und weniger als 5.000 Individuen außerhalb der Mongolei geschätzt (Kaczensky et al., 2008). Ungefähr 2.000 Asiatische Wildesel leben in dem Naturschutzpark der Großen Gobi „B“ (Kaczensky et al., 2008). Der Asiatische Wildesel steht seit 1953 in der Mongolei unter vollem Schutz und ist seit 2006 in der Roten Liste der Weltnaturschutzunion als „gefährdet“, seit 1973 im Appendix I des Washingtoner Artenschutzübereinkommen, für den internationalen Handel mit gefährdeten Arten freilebender Tiere und Pflanzen, und seit 2002 im Appendix II der Bonner Konvention, zur Erhaltung der wandernden wild lebenden Tierarten, gelistet (Kaczensky und Walzer, 2008). Der Asiatische Wildesel war früher auf den Steppen und Wüsten des Mittleren Osten und Zentralasiens allgemein verbreitet. Heute existiert der Asiatische Wildesel nur mehr auf 5 % seines früheren Verbreitungsgebiets (Kaczensky und Walzer, 2008). Die Populationsgröße ist, auf Grund von Konfliktsituationen mit mongolischen Hirten, Wildereien und Habitatzerstörung, signifikant kleiner geworden (Kaczensky et al., 2007, Kuehn, 2006). Basierend auf historischen Aufzeichnungen, überlappten die Streifgebiete des Przewalskipferdes und des Asiatischen Wildesels in der Dzungarischen Wüste schon bevor das Przewalskipferd in der freien Wildbahn ausgestorben war (Boyd und Houpt, 1994). Das mongolische Hauspferd (Equus ferrus caballus, LINNAEUS 1758) lebt, meist ungezähmt und wenig behirtet über das ganze Jahr auf großen Weiden, nur wenige Hindernisse beeinträchtigen ihre verwilderte Lebensweise.
Nur sehr wenige parasitologische Untersuchungen wurden an diesen Spezies früher durchgeführt, im Speziellen keine vergleichenden Studien. Das Ziel dieser Studie war, die 2 parasitäre Bürde dieser drei Spezies zu evaluieren und eventuelle Assoziationen zu Streifgebietgröße, Sozialstruktur und Ressourcennutzung herzustellen. Weiters wurden die Ergebnisse mit einer parasitologischen Studie verglichen, die in den Jahren 2001 bis 2002 in der Großen Gobi „B“ durchgeführt wurde (Elias et al., 2002).
3
1 2) PUBLIKATION 2
3 COMPARATIVE PARASITOLOGICAL EXAMINATION ON SYMPATRIC EQUIDS IN THE GREATER
4 GOBI “B” STRICTLY PROTECTED AREA, MONGOLIA
5
1,5 1,2 2, 3, 4 1 1, 2 6 J. PAINER , P. KACZENSKY , O. GANBAATAR , K. HUBER , C. WALZER
7 1 Research Institute of Wildlife Ecology, University of Veterinary Medicine, Austria;
8 2 International Takhi Group, Mongolia;
9 3 Department of Zoology, Faculty of Biology, National University of Mongolia, Mongolia
10 and 4 Gobi B Strictly Protected Area Administration, Mongolia;
11 5 : corresponding author: [email protected], 0043 - 650 - 477 16 64
12
13 ABSTRACT:
14
15 The Przewalski’s horse (Equus caballus przewalskii) became extinct in the wild during the
16 1960’s. Based on a successful captive breeding program with 13 founder individuals,
17 Przewalski’s horse was reintroduced to the Greater Gobi Part “B” Strictly Protected Area
18 (SPA) in SW Mongolia in the late 1990’s.
19 The Asiatic wild ass (E. hemionus hemionus), Przewalski’s horse and sometimes domestic
20 horses live sympatricly in the Gobi B SPA. Previously published data demonstrates that these
21 equids select for different resources. As a result of their different requirements and utilization
22 of the park’s resources, their home-range size and social structure differs. Asiatic wild asses
23 live in fission-fusion groups, with recorded group sizes up to 1000 individuals and have a 10
24 times larger home range than the Przewalski’s horses, which live in well structured and stable
25 harem groups or bachelor-groups. Parasitological examinations in the three equid species
26 show how the factors “home range, social structure and resource selection” significantly 4
27 impact the parasitic burden. Asiatic wild asses are potentially exposed to a higher risk of
28 parasite re-infection, due to their temporal aggregation in very large groups. This study
29 demonstrates a highly significant greater parasite load in the Asiatic wild ass for the majority
30 of parasites evaluated (Dictyocaulus arnfieldi, Trichostrongylus axei, Strongyloides westeri,
31 Parascaris equorum), compared to Przewalski’s horses and domestic horses in the same
32 habitat. Domestic horses had higher parasite loads for eggs of strongylids, eggs of
33 anoplocephalidae and Eimeria leuckarti. The potential risk of cross infection between
34 sympatric living equids is high, as is the cross infection between ruminants and equids.
35 Furthermore, this study reports for the first time the occurrence of lungworms in free-ranging
36 Przewalski’s horses. Whereas, Asiatic wild asses and Przewalski’s horses seem to cope very
37 well with the sometimes high parasite burden, Mongolian domestic horses manifested typical
38 parasite-burden symptoms.
39
40 KEYWORDS: Przewalski’s horse, Asiatic wild ass, Mongolian domestic horse, parasites,
41 sympatric, cross-infection, home range
42
43 INTRODUCTION:
44
45 The Greater Gobi “B” Strictly Protected Area (SPA) in SW Mongolia is one of the few places
46 in the world where habitats of different wild equids overlap, and the only area where Asiatic
47 wild ass and Przewalski’s horse live sympatricly and seasonally share pastures with domestic
48 horses.
49 Przewalski’s horse (Equus caballus przewalskii, locally known as “Takhi”, POLIAKOV 1881)
50 was once widespread over the central Asiatic steppes. It was discovered by the western world
51 in the late 19th century and, until 1947, was captured and transported to zoological gardens.
52 The last sightings of wild individuals were in the Dzungarian desert, in south-western 5
53 Mongolia. In the late 1960’s the Przewalski’s horse was declared extinct in the wild (Boyd
54 and Houpt, 1994). The species was successfully bred ex-situ, based on a reproductive founder
55 population of only 13 individuals (Mohr and Volf, 1971). First efforts to start a reintroduction
56 program were undertaken in 1979, but it was only in 1992 that the first individuals were
57 transported to the Takhin Tal reintroduction site (45.53.80 N, 93.65.22 E). After the
58 establishment of the International Takhi Group (ITG) in 1999, the project was extended in
59 accordance with the International Union for the Conservation of Nature (IUCN)
60 reintroduction guidelines (Walzer et al., 2004; IUCN/SSC, 1998). Since the onset of the
61 project, 89 individuals have been transported from 24 zoo’s world wide (Kaczensky et al.,
62 2005). In the beginning, Przewalski’s horses were kept in adaptation enclosures with the first
63 harem group released into the wild in 1997 (Walzer et al., 2004). Today some 145 free-
64 ranging Przewalski’s horses, in 10 harem groups and a varying number of bachelor-groups,
65 live in the protected area (ITG, 2009, http://www.takhi.org).
66
67 The Asiatic wild ass (Equus hemionus hemionus, locally known as “Khulan”, PALLAS 1775)
68 population is estimated at 19,000 – 20,000 individuals in Mongolia, with less than 5,000
69 individuals remaining outside Mongolia (Kaczensky et al., 2006). Approximately 2,000
70 Asiatic wild asses live in the Greater Gobi “B” SPA (Kaczensky et al., 2008). The Asiatic
71 wild ass has been under full protection in Mongolia since 1953, listed as vulnerable in the
72 IUCN-Red List since 2006, in Appendix I of CITES since 1973 and in Appendix II of the
73 Convention on Migratory Species since 2002 (Kaczensky and Walzer, 2008). The Asiatic
74 wild ass was historically common on the steppes and deserts of the Middle East and central
75 Asia. Today, Asiatic wild ass exists only in 5% of its former range (Kaczensky and Walzer,
76 2008). The population size has decreased significantly due to wild ass conflicts with
77 Mongolian herders, poaching and habitat loss (Kaczensky et al., 2007; Kuehn, 2006). Based
78 on historic records, the former distribution ranges of Przewalski’s horse and Asiatic wild ass 6
79 overlapped in the Dzungarian desert before Przewalski’s horse became extinct in the wild
80 (Boyd and Houpt, 1994).
81 The Mongolian domestic horse (Equus ferrus caballus, LINNAEUS 1758) lives in a semi-feral
82 fashion, moderately herded during the year and largely selecting pasture with few outside
83 constraints.
84 Previously very few parasitological investigations have been performed on these species,
85 particularly not comparative studies. The goal of this study was to evaluate parasite burden in
86 these three equid species and explore possible linkages to home range-size, social system
87 structure and resource selection. Furthermore, we compared the results of this study with a
88 previous parasitological study performed in the Greater Gobi “B” in 2001 and 2002 (Elias et
89 al., 2002).
90
91 MATERIAL AND METHODS
92
93 STUDY AREA
94 In 1974 the Mongolian government declared 9,000 km² between the Altai range and the
95 Chinese border in the south-western part of Mongolia a protected area: the Greater Gobi Part
96 “B”. This area was declared a “strictly protected area” (category 1a) by the IUCN in 1991.
97 The Greater Gobi “B” is the fourth largest UNESCO Biosphere reserve in the world and
98 home to numerous wild animals (ITG, 2009, http://www.takhi.org). The climate is continental
99 with temperatures ranging from +40°C in the short summer periods to -40°C in the extended
100 winter periods (Kaczensky et al., 2007). Average annual precipitation is < 100 mm with a
101 peak in summer. Average snow cover lasts 97 days (Kaczensky et al., 2008). Extreme
102 climatic conditions, with episodes of drought in summer and harsh winters, appear to have
103 become more frequent. Failing Soviet-era mechanical wells have forced herders and their
104 livestock to abandon large areas of Gobi pastureland (Kaczensky et al, 2006). The area 7
105 consists mainly of desert steppes and semi-deserts and exhibits the dynamics of a non-
106 equilibrium model of rangeland vegetation. Ungulate population fluctuations in the area are
107 driven by the amount and timing of rainfall events (Fernandez-Giminez and Allen-Diaz,
108 1999). Six large water points and one intermittent river are found within the park (Kaczensky
109 et al., 2005). As water is a key resource in the Gobi Area, not only for wildlife populations,
110 but also for humans and their livestock, competition between humans and wildlife for access
111 to fresh water has increased (Kaczensky et al., 2006).
112 Two of the most important wildlife species are Przewalski’s horse and Asiatic wild ass. Other
113 large ungulates include the black-tailed gazelle (Gazella subgutturosa), argali (Ovis ammon)
114 and ibex (Capra sibirica). Mammalian carnivores present in the area are wolves (Canis
115 lupus), lynx (Lynx lynx), Pallas’ cat (Otocolobus manul), red fox (Vulpes vulpes), corsac fox
116 (V. corsac), snow leopards (Unica unica) and Eurasian badgers (Meles meles) (Kaczensky et
117 al., 2006).The majority of mammalian species are rodents, of which 25 species can be found,
118 including 9 jerboa, 4 gerbil, and 6 hamster species. There are 6 reptile species and 97 bird
119 species found in the Greater Gobi B SPA (Kaczensky et al., 2005). The area is sparsely
120 vegetated. Salty meadows with Stipa gobica, Nanophyton spp., Cargana spp., Stipa glareosa,
121 Achnaterum spp., Haloxylon, Reuamuria and Nitraria are vegetation types found on Gobi
122 pastures (Kaczensky et al., 2006).
123
124 PARASITOLOGICAL EXAMINATION
125
126 Between July and August 2008, 113 faecal samples were collected in the Greater Gobi “B”
127 SPA. Forty samples were taken from Przewalski’s horses, 31 from Asiatic wild asses and 29
128 from Mongolian domestic horses. Thirteen samples were invalid due to procedural errors. The
129 faecal samples were collected in the morning, stored as cool as possible (< 20oC) and
130 analysed during the afternoon or evening of the same day. For Przewalski’s horses and 8
131 domestic horses, age and sex differentiation was possible in most cases. For Asiatic wild ass,
132 owing to the shyness and the absence of sexual dimorphism, it was not possible to determine
133 age and sex. To avoid mistaking Asiatic wild ass faeces with that of other equids, samples
134 were only collected in areas where Przewalski’s and domestic horses had not recently been
135 sighted by rangers and other researchers. Additionally, wild ass faecal pellets differ
136 significantly in shape and size from those of Przewalski’s and domestic horses.
137
138 Each sample was examined with the Combined Sedimentation Flotation Method (CSFM,
139 modified Stoll-Method using sugar concentrations of 1250 g /1 l of Aqua font.), the
140 Sedimentation method (Benedek-method) and was tested for lungworms (Baerman-method)
141 (Schnieder et al., 2006). Based on morphology and size, parasite stages were differentiated
142 under a microscope (Schnieder et al., 2006). We performed a semi-quantitative evaluation of
143 egg, oocysts and larval output under 100 x magnification similar to the method described by
144 Hoby et al. (2006). The strongyles including Trichostrongylus axei per 10 g, sum of egg or
145 oocyst output for each individual parasite species per 10 g and sum of larval output per 20 g
146 faeces were recorded for each sample. Additionally, we recorded which water point the group
147 was using, in which area their home range was situated and, if possible, group-size, age and
148 sex.
149
150 VISUAL OBSERVATIONS
151
152 To avoid disturbance of the herds, Przewalski’s horses and domestic horse-groups were
153 observed from a distance of approximately 50-100 meters. We used a Vector GIS-Binocular,
154 which is able to measure the distance and the angle to the observed object via laser-distance
155 measurement (Leica Vector 1500), in combination with a Global Positioning Satellite (GPS)
156 fix from a hand-held unit (Garmin, GPS 60Cx) to recover individual faecal samples. 9
157 In contrast, Asiatic wild ass in the Gobi “B” are extremely shy and skittish and could only be
158 observed during the day from distances > 1 kilometre, or from a hide at a water point.
159
160 STATISTICAL ANALYSIS
161
162 We used generalized linear models and ANOVA’s to compare the different variables:
163 individual egg count, oocyst count and lungworm larvae count and strongyles including T.
164 axei with variables like home range-size, resource selection type, social system type, sex, age,
165 watering location, and group-size. We used the statistical software R 2.8.1. (R-development
166 Core Team, 2008). The level for statistical significance was set to p ≤ 0.05.
167
168 RESULTS
169
170 The following parasites were found in all three species (listed from highest to lowest burden):
171 Dictyocaulus arnfieldi (COBBOLD, 1879), T. axei (COBBOLD, 1879), strongyles excluding T.
172 axei (MÜLLER, 1780), Strongyloides westeri (IHLE, 1917), eggs of anoplocephalidae (GOEZE,
173 1782), Parascaris equorum (GOEZE, 1782), Eimeria leuckarti (FLESCH, 1883) as well as
174 occasional sightings of Gasterophilus spp. (DE GEER, 1776) larvae in the faeces (Table 1,
175 Figs. 3, 5, 7).
176 Age was a significant factor when comparing the egg count for each parasite species
177 (ANOVA, DF = 4, p = <0.007) for Przewalski’s horses and domestic horses. In younger
178 individuals the load of S. westeri was significantly higher (glm, DF = 62, p = < 0.004,
179 Estimates = -0.93). P. equorum also tended to be present in higher numbers in younger
180 individuals, though this was not significant. E. leuckarti showed no significant difference of
181 load in older or younger individuals, though sample size was too low for this comparison
182 (only 2 domestic horses tested positive). The other parasite species (D. arnfieldi, T. axei, eggs 10
183 of strongylids excluding T. axei, eggs of anoplocephalidae) produced a slightly higher or
184 equal burden in adult equids. Yearlings showed a non-significant higher variability in parasite
185 species present with similar quantitative levels as adult horses. There was no significant
186 relationship between sex and parasite levels.
187
188 In the study area the prevalence of each parasite in Przewalski’s horse (see Fig. 4) was 65.0%
189 for D. arnfieldi, 67.5 % for T. axei, 32.5 % for strongyles excluding T. axei, 12.5 % for S.
190 westeri, 2.5 % for P. equorum and eggs of anoplocephalidae, and 0 % for E. leuckarti. In
191 Asiatic wild ass (see Fig. 6) the prevalence was: 64.5% for D. arnfieldi, 74.3 % for T. axei,
192 6.4 % for strongyles excluding T. axei, S. westeri and P. equorum, and 0 % for eggs of
193 anoplocephalidae and E. leuckarti. Prevalence in the Mongolian domestic horse (see Fig. 8)
194 were 72.4% for D. arnfieldi, 86.2% for T. axei, 51.8 % for strongyles excluding T. axei, 0 %
195 for S. westeri and P. equorum, 3.4 % for eggs of anoplocephalidae and 6.8 % for E. leuckarti.
196 The prevalence of parasite infection in each herd was high with 87.5 % for Przewalski’s horse
197 herds, 90.3 % for Asiatic wild ass herds, and 100 % for Mongolian domestic horse herds.
198 Means, bootstrap confidence intervals and medians for the prevalences are listed in Table 1.
199
200 Comparing strongyles including T. axei between the three species we found a highly
201 significant difference (ANOVA, p = 0.004). Asiatic wild ass had the highest parasitic burden
202 of strongyles including T. axei (mean = 814.87 eggs in 10g of faeces with CSFM), followed
203 by domestic horses (mean = 674.03 eggs in 10 g of faeces with CSFM), while Przewalski’s
204 horses had the lowest burden of strongyles including T. axei (mean = 198.52
205 eggs in 10g faeces with CSFM) (Fig.1). Comparing only the two wild equid species, the
206 significant difference in their burden of strongyles including T. axei was even higher
207 (ANOVA, p ≤ 2e -16). 11
208 When testing the differences in burden based on individual parasite species among the three
209 equid species, only the difference in parasite load of D. arnfieldi L1 larvae and eggs was
210 significant (ANOVA, DF = 10, p ≤ 0.0021). Again, Asiatic wild ass had the highest burden
211 followed by the domestic horse and Przewalski’s horse. When comparing the number of eggs
212 of T. axei between Asiatic wild ass and Przewalski’s horses, the Asiatic wild asses had a
213 significantly higher burden (ANOVA; DF = 50, p = <0.036).
214 Gasterophilus spp. larvae were found in some faecal samples of all three equid species, as
215 well as in the stomach of a Przewalski’s horse euthanized due to a trauma.
216
217 DISCUSSION
218
219 The present work evaluated the parasitic burden and parasite diversity of three sympatric
220 living equids in the Greater Gobi part “B”, in Mongolia. In this park Przewalski’s horses live
221 together, completely free-ranging, with Asiatic wild asses and Mongolian domestic horses.
222 Qualitative and semi-quantitative analyses of faecal samples were performed with CSFM.
223 Elias et al. (2002) suggested that the determination of parasite prevalence within a herd is
224 more sensitive when using CSFM, compared to McMaster. Since samples were only collected
225 in summer, we could not test for any seasonal influence on the results.
226 D. arnfieldi, T. axei, strongyles excluding T. axei, Str. westeri, eggs of anoplocephalidae, P.
227 equorum, E. leuckarti and occasionally Gasterophilus spp. larvae were detected in the faeces.
228 Individual parasite burden, as well as sum of strongyles including T. axei and parasite
229 prevalence within a herd were compared with previous studies to see if any associations could
230 be found.
231 Strongyles excluding T. axei had prevalences of 32.5% in Przewalski’s horses, 6.4% in
232 Asiatic wild asses and 51.8% in Mongolian domestic horses. This is lower than prevalences
233 previously reported of 75.9%, 96.2% and 98.7% respectively (Elias et al., 2002). Prevalences 12
234 between 80 and 100 % for small strongylids and 17 – 100% for large strongylids have also
235 been recorded (Beelitz et al., 1996; Ogbourne, 1976; Reinemeyer et al., 1984). Our lower
236 prevalences may be explained by the short sampling period of only two months.
237 Eggs of anoplocephalidae showed a prevalence of 2.5 % for Przewalski’s horses, 0 % for
238 Asiatic wild asses and 3.4 % for Mongolian domestic horses during our sampling period.
239 These values are lower than those found in wild equids by Elias et al. (2002), with
240 prevalences of 6.1 % and 1.9 % respectively and higher than their reported prevalence of 1.3
241 % for the domestic horses. Tapeworms seem to be shed at a maximum in spring (Elias et al.,
242 2002), which was not the period of our study. Furthermore, tapeworms have a lower
243 prevalence in equids that are not dewormed, due to higher competition with other parasites
244 (Elias et al., 2002, pp. 52-56). Coproscopic examinations are not the method of choice to
245 determine an anoplocephalid infection since eggs are shed by the host only sporadically (Elias
246 et al., 2002).
247 Prevalences for P. equorum in our study were: in Przewalski’s horses 2.5 %, in Asiatic wild
248 asses 6.4 % and 0 % in Mongolian domestic horses. The literature suggests prevalences
249 between 3 – 18 %. Adult equids establish a protective immunity against ascarids and positive
250 samples could only be found in groups with foals. Asiatic wild asses do not appear to have a
251 similar protection against ascarids as adults still show a burden (Elias et al., 2002). Elias et al.
252 (2002) found prevalences of ascarid burden to be 0.9 %, 25.0 % and 7.6 % respectively.
253 Presence of E. leuckarti was only found in Mongolian domestic horses, in 6.4 % of our
254 samples, and by Elias et al. (2002) in only one Przewalski’s horse. Coccidiosis in equids is
255 rare with a prevalence of about 1% (Bauer and Bürger, 1984). Furthermore, the egesting rate
256 seems to be low and therefore not easily detectable (Bauer and Bürger, 1984).
257
258 In this study, T. axei had the highest prevalences with 67.5% in Przewalski’s horses, 74.3% in
259 Asiatic wild asses and 86.2% in Mongolian domestic horses. No trichostrongylids were found 13
260 in the previous study by Elias et al. (2002). At that time Przewalski’s horses and ruminants
261 were not being grazed on the same pastures and cross-infection between ruminants and equids
262 may have occurred only during times when their home ranges overlapped. T. axei, primarily a
263 ruminant abomasal parasite (Schnieder et al., 2006, Elias et al., 2002), only occurs in equid
264 species grazing on the same pastures as ruminants (Eysker et al., 1986). The most common
265 wild ruminant in the Greater Gobi B is the black-tailed gazelle. Domestic ruminants are the
266 cashmere goat, sheep and cattle. Herders graze them close to the park border and they are
267 tolerated by the authorities in the park's buffer zone during very harsh periods in winter and
268 spring.
269 D. arnfieldi showed prevalences of 65.0 % in Przewalski’s horses, 64.5 % in Asiatic wild
270 asses and 72.4 % in Mongolian domestic horses in our study. This is a slightly higher
271 occurrence than expected (Lyons et al., 1985; Pandey, 1980). In the previous study no
272 infection with lungworms (D. arnfieldi) was found (Elias et al., 2002). At that time only one
273 harem group of Przewalski’s horses was living in the wild, with a small home range and
274 without antiparasitic treatment. Presumably there was not much overlap between home ranges
275 of Asiatic wild asses, Przewalski’s horses and domestic horses. Our study reports for the first
276 time lungworm infections in free-ranging Przewalski’s horses. Donkeys are the major host
277 and most important reservoir for equid lungworms. They are considered to act as the source of
278 infection; horses play only an ancillary role and become infected after pastured with donkeys
279 (Schnieder et al., 2006; George et al., 1981; Beelitz et al., 1996; Mehlhorn et al., 1993; Morris
280 et al., 2004). As expected from the literature, lungworm infection in this examination shows
281 that Asiatic wild asses have a significantly higher load of lungworms than Przewalski’s
282 horses. The Przewalski’s horses may have only become infected with lungworms after some
283 years of overlapping home ranges with Asiatic wild asses. Patent infections usually only
284 occur in donkeys, mules and asses, whereas in horses larval development is often arrested in
285 the fifth stage. Large numbers of parasites can accumulate in the lungs of asses without any 14
286 clinical disease. A horse-to-horse transmission has been reported, where D. arnfieldi caused
287 non-patent infections with signs of coughing, increased respiratory rate and nasal discharge
288 (Boyle and Houston, 2006). We found these signs in Mongolian domestic horses, however,
289 they were absent in their wild counterparts. Co-evolution of the parasites and the wild equids
290 in the Gobi have possibly engendered immunologic advantages.
291
292 Age differences were highly significant in Przewalski’s horses and domestic horses.
293 Depending on the parasite species, younger or older individuals had a higher burden. Some
294 parasites like S. westeri, E. leuckarti, and P. equorum are more commonly seen in foals and
295 younger individuals as immunity provides sufficient protection as they age, whereas other
296 parasites, like eggs of anoplocephalidae., strongyles excluding T. axei, T. axei and D.
297 arnfieldi, are commonly seen in individuals of all ages because protective immunity is
298 insufficient (Schnieder et al., 2006; Wakelin, 1996; Beelitz et al., 1996; Bauer & Bürger,
299 1984). As described in the literature, we found that S. westeri was significantly more often
300 present in younger individuals in the current study, and P. equorum also showed this age
301 difference, though it was not significant. However, E. leuckarti showed no significant
302 difference between older or younger individuals, possibly due to the low sample size. D.
303 arnfieldi, T. axei, strongyles excluding T. axei and eggs of anoplocephalidae showed higher or
304 equally high burden in adult equids, as predicted by the literature. Young horses, aged up to 1
305 year, showed slightly higher variability in parasites with similar quantitative levels as adult
306 horses, though the results were not statistically significant (Schnieder et al., 2006; Elias et al.,
307 2002). This higher variability may be due to the young host's immune system establishing a
308 protective immunity to some parasites, thus decreasing the parasite variability with age
309 (Schnieder et al., 2006). Immunity to gastrointestinal parasites seems to be inefficient in
310 young animals and is effectively depressed during pregnancy and lactation. Reproductive
311 females therefore provide an infection source for their susceptible offspring, who may become 15
312 chronically infected. Due to these effects, pastures then become heavily contaminated and
313 ensure transmission to newborns, immunosuppressed and easy susceptible individuals
314 (Wakelin, 1996). In Przewalski’s horses this effect is thought to be greatly reduced, due to the
315 non existence of a peripaturient – rise in parasite infections in Przewalski’s horses (Elias et al.
316 2002).
317 Some nematode infections can result in good immunity to parasites with a low risk of re-
318 infection. However, many intestinal nematode infections cause chronic infections with no
319 effective immunity in their host. In the field, chronic infections cannot be assumed to reflect
320 absolute inability to develop resistance, as factors like age, health, diet, physiological state,
321 level and frequency of infection all influence the development and expression of immunity
322 (Wakelin, 1996). Immunological resistance is influenced by population density, pasture
323 contamination and pathological factors of the host (Boyle & Houston, 2006; Wakelin, 1996;
324 Morris et al., 2004; Elias et al., 2002). However, the ability of animals to resist helminth
325 infections is also genetically determined and variable between individuals of a given host
326 species (Stear and Wakelin, 1998). Foals younger than 1.5 months (5 individuals) did not test
327 positive for any parasite. This may be due to factors like: galactogenic nutrition only or in
328 case of galactogenically transmitted parasites, the foals might have been in the prepatent
329 phase or their mothers might simply have not been infected (Schnieder et al., 2006).
330
331 The strongyles including T. axei compared between the species was highly significant, with
332 Asiatic wild ass having the highest parasitic burden, followed by domestic horses and then
333 Przewalski’s horses, which had a much lower burden (Fig. 1, 3-8). Comparing only the two
334 wild equid species, Przewalski’s horse and Asiatic wild ass, the significant difference in their
335 sum of strongyles including T. axei burden was even higher. This trend could also be seen for
336 the majority of parasites (D. arnfieldi, T. axei, S. westeri, P. equorum) evaluated in this study.
337 This data can be analysed in view of a study by Kaczensky et al. (2008) concerning resource 16
338 selection by sympatric wild equids in the Mongolian Gobi. Between November 2001 and May
339 2004, Kaczensky et al. (2008) satellite-radio-collared nine Przewalski’s horses and seven
340 Asiatic wild asses, to investigate resource selection in these sympatric wild equids. Their
341 results showed (inter alia) sympatric Asiatic wild asses and Przewalski’s horses select
342 different plant communities for grazing. Asiatic wild asses have a 10 times larger home range
343 than Przewalski’s horses and they have a completely different social structure. Kaczensky et
344 al. (2008) concluded that these two sympatric wild equids are not in direct competition. Based
345 on their data, the Gobi B is a perfect habitat for Asiatic wild asses, though not necessarily for
346 Przewalski’s horses. Przewalski’s horses select the most productive plant communities, which
347 are rare in this part of the Gobi. Asiatic wild ass use plant communities relative to their
348 availability. Differences in resource selection strategies can be linked to the different social
349 systems (Kaczensky et al., 2008). The home range of Przewalski’s horses is 471 km² (range:
350 152-826 km²) and 5860 km² (range: 4449-7186 km²) for Asiatic wild asses (Kaczensky et al.,
351 2008). Przewalski’s horses live in stable harem groups (average 5.6 adult mares and 11.1
352 offspring) with one dominant stallion, or in bachelor groups with varying stability. Asiatic
353 wild asses are often sighted in groups of hundreds of individuals, characterized by loose
354 associations and single individuals (Kaczensky et al., 2008; Feh, 2002). Kaczensky et al.
355 (2008) suggested that Asiatic wild asses in the Gobi are likely to be organized in fission-
356 fusion groups (mean group size 28.4 animals; range: 1-1000 km²), which has previously been
357 described for other equids in arid environments (Sundaresan et al., 2006). The social structure
358 of fission-fusion groups in Asiatic wild asses allows far more individuals to live temporarily
359 at high concentrations in the same area. Sometimes unstructured groups of 500 – 1000+
360 animals were observed. This limited space increases the environmental infectious doses (Ortiz
361 et al., 2006). Being nomadic animals they do not remain in one place long, however, most
362 parasites do not need a long external maturation time in order to be infectious, therefore re-
363 infection may occur quite often. 17
364 Przewalski’s horse, socially structured in small, stable harem groups or in bachelor groups,
365 have far smaller home ranges and therefore have a significantly lower exposure to
366 contaminated patches (Fig. 2).
367 Mongolian domestic horses stay in groups of 10-50 horses. Herders move them from one
368 green pasture to another, without paying attention to which horses were grazing and
369 defecating there before. Furthermore, these domestic equids could differ immunologically
370 with respect to parasites from their wild counterparts, are handled occasionally by herders and
371 may suffer more from stress (Elias et al., 2002; Sharkhuu et al., 2000).
372
373 CONCLUSION
374 Despite the sometimes quite high egg- and larval output, Przewalski’s horses and Asiatic wild
375 asses appear to cope well with their respective parasitic fellow passengers and parasites
376 appear to be, at the most, a minor pathogen for them. In comparison, domestic horses
377 obviously have some problems with the parasite infection as manifested by diarrhoea, loss of
378 weight, coughing and scrubby fur. The risk of cross-infection can be high between the
379 sympatric equids, but also between ruminants and equids, living in the Gobi B. It is
380 interesting to note that Przewalski’s horse, after many generations in captivity, appears to
381 have retained this wild equid advantage vis-á-vis gastrointestinal parasite infection.
382 There are few investigations concerning the infestation status of parasites in wild equids,
383 particularly in the Asiatic wild ass and the Przewalski’s horse. The results may help further
384 management of both wild and captive populations. More detailed information regarding
385 interactions between the three species and possible effects of these interactions on parasite
386 burden would be an interesting approach for future research, though it can not be discussed
387 with our data. This study highlights the importance of not only the common influences to
388 immunity like sex, age or pathological findings, but also population density and pasture 18
389 contamination. Variables such as home range-size, resource selection and social systems may
390 impact on the immunity of sympatric hosts to parasites.
391
392 ACKNOWLEDGEMENTS:
393 Thank you very much to R. Drury, N. Enkhsaikhaan, Aagi, T. Ruf, A. Zedrosser, F.
394 Tiedeman, V. Sahlén, ITG staff, the local rangers and their families, as well as everyone who
395 was somehow involved in the project for their exceedingly great support.
396
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486 TABLE 1: PARASITE EGGS, OOCYSTS AND LARVAES
Amount per parasite stages in equid species, means and medians (intensity evaluation)
Species Dictyocaulus Trichostrongylus strongyles Strongyloides Parascaris Anaplo- Eimeria strongyles
arnfieldi axei excluding westeri equorum ceph- leuckarti including
T. axei alidae. T.axei
Przewalski 9,420 6,016 1,925 116 20 11 0 7,941
mn, md 235.5, 207.5 150.4, 53.5 48.1 2.9 0.5 0.3 0 198.5,
53.5
Asiatic wild 12,552 24,786 475 123 352 0 0 25,261
ass
mn, md 404.9, 79 799.5, 558 15.3 3.9 11.3 0 0 814.9,
558
Domestic 9,869 13,447 6,100 0 0 44 41 19,547
mn, md 343.3, 103 480.2, 309 217.8, 17 0 0 1.5 1.4 674.0,
534
Prevalence and bootstrap confidence interval of parasite stages in the three equid species
Przewalski 65.0% 67.5% 32.5% 12.5% 2.5% 2.5% 0% 70%
Asiatic 64.5% 74.3% 6.4% 6.4% 6.4% 0% 0% 74%
wild
Domestic 72.4% 86.2% 51.8% 0% 0% 3.4% 6.8% 96%
487 The results from a comparative parasitological examination on three sympatric equids collected
488 between July and August, 2008. Amount per parasite stages per equid species, counted in CSFM. D.
489 arnfieldi L1 larvae were not included in the intensity evaluations (top), but in the list for prevalences
490 (bottom). Confidence intervals were analyzed as bootstrap confidence intervals (bCI). Mean (mn),
491 median (md), lower 95% bootstrap confidenz interval ( 492 interval (>bCI) are listed. 493 *) Prevalence was too low to generate medians and bootstrap confidence intervals. 494 23 495 FIG. 1: STRONGYLES INCLUDING T. AXEI COUNTS OF INDIVIDUALS FROM ONE SPECIES COMPARED 496 BETWEEN THE THREE EQUID SPECIES 497 498 Domestic horses, Asiatic wild asses, Przewalski’s horses - in the Gobi Desert Ecosystem. 499 Presented as a grouped sample for every equid species. Semi-quantitative egg count with 500 CSFM. 501 502 Horizontal axis: equid species: D = domestic horses, K = Khulan, Asiatic wild ass, 503 T = Takhi, Przewalski’s horse 504 Vertical axis: strongyles including T. axei from every equid species. 505 Asiatic wild ass: mean = 814.87 eggs in 10g with CSFM 506 Domestic horses: mean = 674.03 eggs in 10g faeces with CSFM 507 Przewalski’s horses: mean = 198.52 eggs in 10g faeces with CSFM 508 509 24 510 511 FIG. 2: THE MEAN HOME RANGE-SIZE OF THE TWO WILD EQUID SPECIES COMPARED TO THEIR 512 MEAN PARASITE BURDEN OF STRONGYLES INCLUDING T. AXEI 2000 1000 0 471 5860 513 Przewalski’s horse Asiatic wild ass 514 515 Przewalski’s horse (T) and Asiatic wild ass (K) in relation to their mean burden of strongyles 516 including T. axei burden of individuals from each species in the Gobi Desert Ecosystem. 517 Horizontal axis: Mean home range size of Przewalski’s horses (T) = 471 km², mean home 518 range size of Asiatic Wild Asses (K) = 5860 km². 519 Vertical axis: strongyles including T. axei parasite egg count with CSFM per individual per 520 10gram of faeces. Asiatic wild ass: mean = 814.87 eggs in 10g with CSFM; Przewalski’s 521 horses: mean = 198.52 eggs in 10g faeces with CSFM 522 523 25 524 FIG. 3: PRZEWALSKI’S HORSE PARASITE BURDEN Przewalski's horse, mean parasite burden 250.0 235.5 198.5 200.0 150.4 150.0 Przewalski 100.0 48.1 amount of stages of amount 50.0 2.9 0.5 0.3 0.0 0.0 T. axei D. arnfieldi Str. westeriP. equorum E. leuckarti strongylid eggs strongyles incl. T.axei anoplocephalidae eggs Parasite 525 526 The figure shows the mean parasite burden of 40 free ranging Przewalski’s horses, living in 527 the Greater Gobi B, SPA in Mongolia. 528 26 529 FIG. 4: PREVALENCES (%) OF PARASITE STAGES FROM PRZEWALSKI’S HORSES Przewalski's horse prevalences 80 70 70 65 67.5 60 50 40 32.5 Przewalski 30 Prevalence in % in Prevalence 20 12.5 10 2.5 2.5 0 0 T. axei S. westeri D. arnfieldi P. equorum E. leuckarti strongylid eggs strongyles incl. T.axei anopolocephalidae eggs Parasite 530 531 27 532 FIG. 5: ASIATIC WILD ASS PARASITE BURDEN Asiatic wild ass, mean parasite burden 900.0 799.5 814.8 800.0 700.0 600.0 500.0 404.9 Asiatic wild ass 400.0 300.0 amount of stages of amount 200.0 100.0 15.3 4.0 11.4 0.0 0.0 0.0 T. axei D. arnfieldi Str. westeriP. equorum E. leuckarti strongylid eggs strongyles incl. T.axei anoplocephalidae eggs Parasites 533 534 The figure shows the mean parasite burden of 31 free ranging Asiatic wild ass, living in the 535 Greater Gobi B, SPA in Mongolia. 536 28 537 FIG 6: PREVALENCES OF PARASITE STAGES FROM ASIATIC WILD ASS Asiatic wild ass prevalences 80 74.3 74 70 64.5 60 50 40 Asiatic wild ass 30 20 Prevalences in % in Prevalences 10 6.4 6.4 6.4 0 0 0 T. axei S. westeri D. arnfieldi P. equorum E. leuckarti strongylid eggs strongyles incl. T.axei anopolocephalidae eggs Parasites 538 539 540 29 541 FIG. 7: MONGOLIAN DOMESTIC HORSES PARASITE BURDEN Domestic horses, mean parasite burden 800.0 674.0 700.0 600.0 480.3 500.0 400.0 343.4 Domestic 300.0 217.9 amount of stages of amount 200.0 100.0 0.0 0.0 1.6 1.5 0.0 T. axei D. arnfieldi Str. westeriP. equorum E. leuckarti strongylid eggs strongyles incl. T.axei anoplocephalidae eggs Parasites 542 543 The figure shows the mean parasite burden of 29 Mongolian domestic horses, living in the 544 Greater Gobi B, SPA in Mongolia. 545 30 546 FIG. 8: PREVALENCES OF PARASITE STAGES FROM MONGOLIAN DOMESTIC HORSES Domestic horses prevalences 120 100 96 86.2 80 72.4 60 51.8 Domestic 40 Prevalences in % in Prevalences cc 20 6.8 0 0 3.4 0 T. axei S. westeri D. arnfieldi P. equorum E. leuckarti strongylid eggs strongyles incl. T.axei anopolocephalidae eggs Parasites 547 548 549 31 3) DEUTSCHE ZUSAMMENFASSUNG Das Przewalskipferd (Equus caballus przewalskii) wurde in den 1960er Jahren von der Weltnaturschutzunion (IUCN, International Union for Conservation of Nature and Nature Resources), als “ausgestorben in freier Wildbahn“, erklärt. Augrund eines sehr erfolgreichen Zuchtprogramms, basierend auf nur 13 Gründer Individuen, konnte das Przewalskipferd erfolgreich in den Naturschutzpark der Großen Gobi, Teil „B“, im Südwesten der Mongolei in den späten 1990er Jahren wiedereingeführt werden. Der Asiatische Wildesel (E. hemionus hemionus), das Przewalskipferd und gelegentlich das mongolische Hauspferd, leben sympatrisch im Naturschutzpark der Großen Gobi „B“. Kürzlich veröffentlichte Daten über diese drei sympatrisch lebenden Equiden, beschreiben deren unterschiedliche Ressourcen Nutzung. Auf Grund der unterschiedlichen Anforderungen an den Schutzpark und Nutzungen der Ressourcen des Schutzparks, variiert deren Streifgebietgröße und deren Sozialstruktur. Während die Asiatischen Wildesel in so genannten Fission – Fusion Gruppen leben, mit beobachteten Gruppengrößen von bis zu 1000 Individuen und einem zehnmal größeren Streifgebiet als Przewalskipferde, leben Przewalskipferde in gut strukturierten und stabilen Harems- oder Junggesellengruppen. Die parasitologischen Untersuchungen der drei sympatrischen Equiden haben gezeigt, dass Faktoren wie „Streifgebietgröße, Sozialstruktur und Ressourcen Selektion“ die parasitologische Bürde signifikant beeinflussen können. Der Asiatische Wildesel hat ein höheres Risiko einer parasitären Reinfektion aufgrund seiner temporären Ansammlung in großen Fission - Fusion Gruppen. Diese Studie zeigt auf, dass der asiatische Wildesel eine stark signifikant höhere Bürde für die Mehrheit der Parasiten (Dictyocaulus arnfieldi, Trichostrongylus axei, Strongyloides westeri, Parascaris equorum) trägt, als das Przewalskipferd, obwohl sich beide im selben Lebensraum befinden. Man kann das Potenzial eines Risikos an Kreuzinfektionen zwischen den sympatrischen Equiden, als auch zwischen Wildwiederkäuern, domestizierten Wiederkäuern und den drei Equiden als hoch ansehen. Weiters beschreibt diese Studie zum ersten Mal das Auftreten von Lungenwürmern in frei lebenden Przewalskipferden. Die Przewalskipferde und die Asiatischen Wildesel erwecken den Anschein, als ob sie gut mit der durchaus hohen Parasitenbürde zurechtkämen. Deren domestiziertes Pendant, das mongolische Hauspferd, weist jedoch typische parasitär bedingte Symptome auf. Schlüsselwörter: Przewalskipferd, Asiatischer Wildesel, mongolisches Hauspferd, Parasiten, sympatrisch, Kreuzinfektionen, Streifgebiete 32 4) SUMMARY, ENGLISH The Przewalski’s horse (Equus caballus przewalskii) became extinct in the wild during the 1960’s. Based on a successful captive breeding program with 13 founder individuals, Przewalski’s horse was reintroduced to the Greater Gobi Part “B” Strictly Protected Area (SPA) in SW Mongolia in the late 1990’s. The Asiatic wild ass (E. hemionus hemionus), Przewalski’s horse and sometimes domestic horses live sympatricly in the Gobi B SPA. Previously published data demonstrates that these equids select for different resources. As a result of their different requirements and utilization of the park’s resources, their home-range size and social structure differs. Asiatic wild asses live in fission-fusion groups, with recorded group sizes up to 1000 individuals and have a 10 times larger home range than the Przewalski’s horses, which live in well structured and stable harem groups or bachelor-groups. Parasitological examinations in the three equid species show how the factors “home range, social structure and resource selection” significantly impact the parasitic burden. Asiatic wild asses are potentially exposed to a higher risk of parasite re-infection, due to their temporal aggregation in very large groups. This study demonstrates a highly significant greater parasite load in the Asiatic wild ass for the majority of parasites (Dictyocaulus arnfieldi, Trichostrongylus axei, Strongyloides westeri, Parascaris equorum), compared to Przewalski’s horses and domestic horses in the same habitat. Only for eggs of strongylids, eggs of anoplocephalidae and Eimeria leuckarti, domestic horses had a higher load. The potential risk of cross infection between sympatric living equids is high, as is the cross infection between ruminants and equids. Furthermore, this study reports for the first time the occurrence of lungworms in free ranging Przewalski’s horses. Whereas, Asiatic wild asses and Przewalski’s horses seem to cope very well with the sometimes high parasite burden, Mongolian domestic horses manifested typical parasite-burden symptoms. Keywords: Przewalski’s horse, Asiatic wild ass, Mongolian domestic horse, parasites, sympatric, cross-infection, home range