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© 2018 Journal compilation ISSN 1684-3908 (print edition) http://mjbs.num.edu.mn Mongolian Journal of Biological http://biotaxa.org./mjbs Sciences MJBS Volume 16(1), 2018 ISSN 2225-4994 (online edition) http://dx.doi.org/10.22353/mjbs.2018.16.06 Original Ar cle

Ectoparasites on Meso-carnivores in the - of

Tserendorj Munkhzul1, James D. Murdoch2 and Richard P. Reading3

1Mammalian Ecology Laboratory, Institute of General and Experimental Biology, Mongolian Academy of Sciences, Ulaanbaatar, Mongolia 2Rubenstein School of Environment and Natural Resources, University of Vermont, George Aiken Center, Burlington, Vermont 05405 USA 3International Conservation Coalition, Denver, Colorado 80220 USA, Butterfl y Pavilion, Westminster, Colorado 80020 USA & Mongolian Conservation Coalition, Ulaanbaatar, Mongolia

Abstract

Key words: Carnivore, Studying fl ea community structure on wild carnivores is important for identifying fl ea disease. ectoparasite, vectors for potential infectious diseases and providing information needed to design fl ea, tick programs for human and wildlife health. We collected ectoparasites from 4 of meso-carnivores in an arid Desert-steppe ecosystem of Mongolia. We captured four meso-carnivore species, including corsac (V. corsac, n = 7), ( vulpes, n = 4), Asian ( leucurus, n = 4), and Pallas’s cat (Otocolobus Article information: manul, n = 4), and recorded 207 fl eas representing 14 species from 7 genera of 4 Received: 06 Sept. 2018 families, and 2 ticks from 1 species. We collected 86 fl eas (6 species) from corsac Accepted: 27 Sept. 2018 , 89 fl eas (6 species) from red foxes, 14 fl eas (5 species) from , and 18 Published online: fl eas (8 species) from Pallas’s cats. The fl ea community was dominated by two species 16 October 2018 (Pulex irritans, Chaetopsylla homoeus), which accounted for 72% of all ectoparasites collected. Pulex irritans was the most common species on corsac and red foxes, and Paraceras melis was the most common species on badgers. Three species were most commonly collected on Pallas’s cats, including Pulex irritans, Paraceras melis, and Chaetopsylla appropihquans. Among fl eas, 8 species occurred only on a single meso- carnivore species, 1 species occurred on two meso-carnivore species, and 5 species occurred on 3 meso-carnivore species. The tick, Dermacentor nuttalli only occurred Correspondence: on corsac fox and badger. Our results provide baseline information on the associations tsmunkhzul@yahoo. of fl eas and ticks with wild carnivores that represent potential vectors of disease, com which can inform disease management strategies in Mongolia. Cite this paper as: Munkhzul, Ts., Murdoch, J. D. & Reading, R. P. 2018. Ectoparasites on meso- carnivores in the desert-steppe of Mongolia. Mong. J. Biol. Sci., 16(1): 43-48.

Introduction

In Mongolia, after more than a century of fl ea 159, based on their own collections. More recently, research, scientists have recorded 6 families, 37 Kiefer et al. (2012) reported 162 species of fl eas genera, 101 species and 12 subspecies obtained known to exist in Mongolia and the adjacent Tuva from 53 species of host- (Puntsagdulam Republic of . & Altanchimeg, 2005). Bavaasan (1974) Fleas are highly specialized ectoparasites catalogued 130 fl ea species, and just 7 years later with a wide range of hosts, including birds and Kieff er et al. (1984) expanded the number of fl ea mammals. Fleas alternate between periods of species and subspecies known from Mongolia to direct occurrence upon the host’s body and in the

43 44 Munkhzul et al. Ectoparasites of meso-carnivores in desert-steppe substrate of their host’s nest or den. The degree northern edge of the Gobi Desert Ecosystem at of host specifi city of fl eas varies greatly among the transition between steppe and desert habitats species, ranging from highly host-specifi c to (referred to as desert-steppe; Reading et al., opportunistic (Marshal, 1981). In addition to 2011). More specifi cally, Ikh Nart contains sparse their role as ectoparasites, fl eas have relevance vegetation at the interface of dry steppe and semi- as vectors of pathogens that infect humans and desert steppe ecotypes. Vegetation types include (Dobler & Pfeff er, 2011). shrublands, tall grasslands, and open plains of Carnivores represent important mammalian short grasses, forbs, and semi-shrubs (Jackson et hosts of fl eas (Krasnov, 2008), and several al., 2006). Ikh Nart has an arid, continental climate studies have suggested that wild carnivores characterized by relatively dry, hot summers (to represent disease reservoirs or play a role in 43°C), cold winters (to -40°C), and dry and windy the transmission cycles of fl ea-borne infections, springs with extremely low humidity. Most of the such as plague, bartonelloses, and rickettsioses. limited precipitation (~ 60 cm/yr) falls in summer For instance, ( spp.) and foxes as rain (Reading et al., 2011). (Vulpes macrotis and cinereoargenteus) In the mid-2000s, a research project began that are suspected to be reservoirs of Bartonella focused on the ecology of meso-carnivores and rochalimae (Lopez-Perez et al., 2017), which their prey. The project focused primarily on the has been associated with bacteremia in humans ecology of red foxes (Vulpes vulpes) and corsac (Eremeeva et al., 2007). Also, researchers have foxes (Vulpes corsac), but that also included identifi ed wild canids as carriers of Yersinia pestis Pallas’s cats (Otocolobus manul), Asian badgers (the causal agent of plague) among prairie (Meles leucurus), and ( lupus) (Cynomys spp.) colonies (McGee et al., 2006). (Murdoch et al., 2006, 2010, 2016; Munkhzul et Many fl ea species that function as important vectors al., 2012, Davie et al., 2014, Lkhagvasuren et al., of fl ea-borne diseases (e.g., Pulex spp., Oropsylla 2016). This study involved capturing and radio- spp., and Ctenocephalides spp.) have been recorded collaring animals as part of a broader project from mammalian carnivores, such as wild felids, on protected area management in the reserve canids, and mustelids (McGee et al., 2006; Marquez (Reading et al., 2016). et al., 2009; Lopez-Perez et al., 2017) Methods. We live trapped four meso-carnivore Knowledge on the spectrum of parasites species (red fox, corsac fox, Asian badger, and carried by host species and determination of their Pallas’s cat) from 2004 to 2007, and collected ectoparasite infestation levels is essential for fl eas from captured animals. We trapped meso- understanding the dynamics of relevant diseases carnivores using box traps (Tomahawk Live Trap and establishing control policies. Nevertheless, Company, Tomahawk, Wisconsin, USA) and in the case of meso-carnivores, very few studies padded soft-catch leg-hold traps (Woodstream provide quantitative data on the level of infestation Corporation, Lititz, Pennsylvania, USA). We placed of external parasites, both in terms of prevalence each captured corsac fox, red fox and Pallas’s cat and abundance. In this study, conducted as part in a large cloth bag for handling without chemical of a research project on the ecology of meso- restraint. We chemically immobilized badgers using carnivore in Mongolia, we sampled a relatively an anaesthetic (Ketamine HCL). Handling followed large number of animals that we captured as part protocols established for kit foxes (O’Farrell, 1987) of a radio-collaring study. Our results contribute and followed guidelines of the American Society of to fi lling our gap in knowledge of ectoparasites in Mammalogists (Sikes, 2016). meso-carnivores in this region. For each , we recorded age, sex, health, and morphological measurements, collected Material and Methods hair and tissue samples, and inspected them for ectoparasites. Each animal was inspected Study area. We captured and surveyed systematically for fl eas by combing for 5 min. parasites from meso-carnivores in Ikh Nart Nature We particularly focused areas around the ears Reserve, which was established in 1996 to protect and necks, body parts that proved to host higher 66,592 km2 (Maygmarsuren & Namkhai, 2012). numbers of ectoparasites. We placed fl eas in Ikh Nart is located in north-western Dornogobi a cryovial containing 70% ethanol and stored Aimag (45°43’ N, 108°39’ E) and lies on the them in liquid nitrogen. To observe the structures Mongolian Journal of Biological Sciences 2018 Vol. 16 (1) 45 required for identifi cation, we placed the fl eas in dominated the fl ea community: Pulex irritans and 2% saline with Tween 80 detergent (2 drops/liter). Chaetopsylla homoeus (Table 1). These species We placed fl eas individually in single petri dishes accounted for 72.2% of all ectoparasites collected. for examination using a stereo microscope and Pulex irritans was the most common species on identifi ed morphologically using a taxonomic key corsac foxes (42.5%) and red foxes (79.8%), and (Loff et al., 1965; Smith, 1967, 1973; Bavaasan Paraceras melis was the most common species et al., 1977). on badgers (26.7%). Three species were most commonly collected on Pallas’s cats, including Results Pulex irritans, Paraceras melis, and Chaetopsylla appropihquans. Among fl eas, 8 species (57.1% of We captured and collected fl eas and other total) occurred only on a single meso-carnivore ectoparsites from 7 corsac foxes, 4 red foxes, 4 species, 1 species (7.1% of total) occurred on two badgers, and 4 Pallas’s cats (Table 1). Among meso-carnivore species, and 5 species (35.7% of captured animals, we collected 207 fl eas total) occurred on three meso-carnivore species (Aphaniptera) representing 14 species belonging (Table 1). We collected 1 tick from a corsac fox to 7 genera of 4 families, and 2 ticks from 1 and another from a badger. species (Dermacentor nuttalli) (Table 1, Fig. 1). We collected 86 fl eas (6 species) from corsac Discussion foxes, 89 fl eas (6 species) from red foxes, 14 fl eas (5 species) from badgers, and 18 fl eas (8 Our results revealed patterns of fl ea assemblages species) from Pallas’s cats (Table 1). Two species of wild meso-carnivores in Mongolia. Regarding

Table 1. Number of ectoparasites by species collected on corsac foxes (Vulpes corsac; n = 7), red foxes (V. vulpes; n = 4), Asian badgers (Meles leucurus; n = 4), and Pallas’s cats (Otocolobus manul; n = 4) captured in Ikh Nart Nature Reserve, Dornogobi Aimag, Mongolia from 2004 to 2007.

Species Corsac fox Red fox Badger Pallas’s cat Aphaniptera Ceratophyllidae Ceratophyllus lunatus 2 Ceratophyllus paradoxus 2 Ceratophyllus scaloni 3 Ceratophyllus tesquorum 1 Paraceras melis 44 Leptopsyllidae Frontopsylla luculenta 6 Mesopsylla hebes 1 Pulicidae Ctenocephalides canis 512 Ctenocephalides 1 Pulex irritans 37 71 4 Vermipsyllidae Chaetopsylla appropihquans 124 Chaetopsylla globiceps 67 1 Chaetopsylla homoeus 34 2 3 Chaetopsylla trichosa 3 Parasitiformes Ixodidae Dermacentor nuttalli 11 46 Munkhzul et al. Ectoparasites of meso-carnivores in desert-steppe

Figure 1. Percent of fl eas by taxonomic family collected from four meso-carnivore species (corsac fox Vulpes corsac, red fox V. vulpes, Asian badger Meles leucurus, and Pallas’s cat Otocolobus manul) in Ikh Nart Nature Reserve, Dornogobi Aimag, Mongolia from 2004 to 2007. host identity, we can distinguish some trends of the Neal & Cheeseman, 1996). Paraceras melis fl ea assemblages. Of the 14 fl ea species collected is an important vector in the transmission of from 4 meso-carnivore hosts, Pulex irritans and trypanosomes (Pierce & Neal, 1974). In the case Chaetopsylla homoeus dominated. Several studies of the Asian badger and Pallas’s cat, very few agree with our fi ndings that fl eas belonging to the studies provide quantitative data relative to the genus Pulex are the most abundant and prevalent level of infestation of the main external parasites. on wild canids (Harrison et al., 2003). The Pulex Knowledge of fl ea faunal composition and fl ea genus comprises six species (Whithing et al., infestation rates of wild meso-carnivores not only 2008), but only two of them, P. simulans and identifi es potential fl ea vectors, but also provides P. irritans, are reported to infest wild carnivore information needed to design and implement hosts (Harrison et al., 2003; McGee et al., 2006; programs to manage fl ea-borne diseases for Salkeld et al., 2007; Gabrel et al., 2009; Dobler & purposes of human and wildlife health. Pfeff er, 2011). In concordance with our fi ndings, P. irritans usually predominates and is often the Acknowledgments most common fl ea on the genus Vulpes, while P. simulans is typically the most common fl ea This study was supported by the Denver on gray foxes (Urocyon cinereoargenteus) and Zoological Foundation, Mongolian Conservation coyotes (Canis latrans) (Harrison et al., 2003; Coalition, Earthwatch Institute, Institute of McGee et al., 2006; Salkeld et al., 2007; Gabrel General and Experimental Biology of the et al., 2009; Dobler & Pfeff er, 2011). As might be Mongolian Academy of Sciences, and National expected, we found that P. irritans had a broader Center for Zoonosis Diseases, Mongolia. We host distribution than other species. thank D. Ganbold and J. Battsetseg for their help We found fl eas Paraceras melis and in identifying fl ea species. Chaetopsylla trichosa and a tick belonging to the family Ixodae (Dermacentor nuttalli), from References badgers in Ikh Nart. In contrast, for European badgers (Meles meles) from western Europe, Bavaasan, A. 1974. Epizootic role of fl eas and the main ectoparasites were the biting louse Lagomorpha in plague centers of Mongolia. Trichodectes melis, Paraceras melis, a host- Transactions of the Irkutsk State Scientifi c specifi c fl ea (Siphonaptera), and ticks belonging Anti-Plague. Institute of and Far East, to the genus Ixodes (Butler & Roper, 1996; 10: 200–202. (In Russian) Mongolian Journal of Biological Sciences 2018 Vol. 16 (1) 47

Bavaasan, A., Tsevelmaa, S. & Eregdendagvaa, Ecology of Fleas: a Model for Ecological D. 1977. Identifi cation Key to the Flea of the Parasitology. Cambridge University Press, Mongolian People’s Republic. Proceedings of Cambridge, 593pp. Science teaching methodology, 1:107–123. (In Lkhagvasuren, M., Murdoch, J. D. Munkhzul, Ts. Russian) & Strong, A. M. 2016. Predicting the eff ects Butler, J. M. & Roper, T. J. 1996. Ectoparasites of habitat loss on corsac fox occupancy in and sett use in European badgers. Animal Mongolia. Journal of Mammalogy, 97: 1153– Behaviour, 52: 621–629. 1163. Davie, H. S., Murdoch, J. D., Lhagvasuren, A. & Loff , I. G., Miculin, M. A. & Scalon, O. I. 1965. Reading, R. P. 2014. Measuring and mapping Handbook for the idenfi cation of fl eas of the infl uence of landscape factors on livestock Central and . Moscow. pp predation by wolves in Mongolia. Journal of 1–370. (In Russian) Arid Environments, 103:85–91. Lopez-Perez, A. M., Osikowicz, L., Bai, Y., Dobler, G. & Pfeff er, M. 2011. Fleas as parasites Montenieri, J., Rubio, A., Moreno, K., Gage, of the family . Parasites & Vectors, 4: K., Suzan, G. & Kosoy, M. 2017. Prevalence 1–12. and phylogenetic analysis of bartonella Eremeeva, M., Gerns, H., Lydy, S., Goo, J., species of wild carnivores and their fl eas in Ryan, E., Mathew, S., Ferraro, M., Holden, J., Northwestern Mexico. Ecohealth, 14:116–129. Nicholson, W., Dasch, G. & Koehler, J. 2007. Marquez, F. J., Millan, J., Rodriguez-Liebana, J. Bacteremia, fever, and splenomegaly caused J., Garcia-Egea, I. & Muniain, M. A. 2009. by a newly recognized Bartonella species. Detection and identifi cation of Bartonella sp. in The New England Journal of Medicine, 356: fl eas from carnivorous mammals in Andalusia. 2381–2387. Medical and Veterinary Entomology, 23: 393– Gabrel, M.W., Henn, J., Foley, J.E., Brown, R.N., 398. Kasten, R.W., Foley, P. & Chomel, B.B. 2009. Marshal, A. G. 1981. The Ecology of Ectoparasite Zoonotic Bartonella species in fl eas collected Insects. Academic Press, London. 446 pp. on gray foxes (Urocyon cinereoargenteus). Maygmarsuren, D., & Namkhai, A. 2012. Special Vector Borne Zoonotic. Disease, 9: 597-602. protected areas of Mongolia. Fourth edition. Harrison, R. L., Patrick, M.J. & Schmitt, C.G. Mongolian Environmental Protection Agency 2003. Foxes, fl eas, and plague in New Mexico. and GTZ (German Technical Cooperation The Southwest Naturalist, 48: 720–722. Agency), Ulaanbaatar. pp 119-120. Jackson, D., Murdoch, J. &Mandakh, B. McGee, B. K., Butler, M. J., Pence, D. B., 2006. Habitat classifi cation using Landsat Alexander, J. L., Nissen, J. B., Ballard, W. -7ETM+imagery of the Ikh Nart Nature B. & Nicholson, K. L. 2006. Possible vector Reserve and surrounding areas in Dornogobi dissemination by swift foxes following a and Dundgobi Aimags, Mongolia. Mongolian plague epizootic in black-tailed prairie Journal of Biological Sciences, 4: 33–40. in northwestern Texas. Journal of Wildlife Kiefer, D., Stubbe, M., Stubbe, A., Gardner, S. Disease, 42: 415–20. L., Tserenorov, D., Samiya, R., Otgonbaatar, Munkhzul, Ts., Buuveibaatar, B., Murdoch, J. D., D., Sumiya, D. & Kieff er, M. S. 2012. Reading, R. P. & Samiya, R. 2012. Factors Siphonaptera of Mongolia and Tuva: Results aff ecting home ranges of red foxes in Ikh Nart of the Mongolian German Biological Nature Reserve, Mongolia. Mongolian Journal Expeditions since 1962-years 1999-2003. of Biological Sciences, 12: 51–58. Erforschung Biologischer Ressourcen der Murdoch, J. D. & Buyandelger, S. 2010. An Mongolei, 12:153–167. account of badger diet in an arid steppe region Kieff er, M., Krumpal, M., Tsendsuren, N., of Mongolia. Journal of Arid Environments, Lobachev, V. S. & Khotolkhu, N. 1984. 74:1348–1350. Checklist, distribution and bibliography Murdoch, J. D., Davie, H.,Galbadrah, M. & of Mongolian Siphonaptera. Erforschung Reading, R. P. 2016. Factors infl uencing Biologischer Ressourcen der Mongolei, pp red fox occupancy probability in central 91–123. Mongolia. Mammalian Biology - Zeitschrift Krasnov, B. 2008. Functional and Evolutionary für Säugetierkunde, 81: 82–88. 48 Munkhzul et al. Ectoparasites of meso-carnivores in desert-steppe

Murdoch, J. D., Munkhzul, Ts., Buyandelger, Reading, R. P., Murdoch, J. D., Amgalanbaatar, S., Reading, R. P. & Sillero-Zubiri. C. 2010. S., Buyandelger, S., Davie, H., Jorgensen, Seasonal food habits of corsac and red foxes M., David, K., Munkhzul, Ts., Onolragchaa, in Mongolia and the potential for competition. G., Lynn, R., Schneider, J., Selenge, T., Stotz, Mammalian Biology - Zeitschrift für E., Tuguldur, E. & Wingard, G. 2016. From Säugetierkunde, 75: 36–44. “Paper Park” to model protected area: The Murdoch, J. D., Munkhzul, Ts. & Reading, R. P. transformation of Ikh Nart Nature Reserve, 2006. Pallas’ Cat ecology and Conservation Mongolia. Parks, 22.2: 25–36. in the Semi-desert of Mongolia. CAT Salkeld, D. J., Eisen, R. J., Stapp, P., Wilder, A. News, 45: 18–19. P., Lowell, J., Tripp, D. W., Albertson, D. & Neal E. G. & Cheeseman, C. 1996. Badgers. Antolin, M. F. 2007. The potential role of swift Poyser Natural History, 271 pp. foxes (Vulpes velox) and their fl eas in plague O’Farrell, T. P. 1987. Kit fox. Wild Furbearer outbreaks in prairie dogs. Journal of Wildlife Management and Conservation. Ministry of Disease, 43:425–431. Natural Resources, Ontario, Canada.pp 422- Sikes, R. S. 2016. The Animal Care and Use 431. Committee of the American Society of Pierce, M.A. & Neal, C. 1974. Trypanosoma Mammalogists. Journal of Mammalogy, 97: (Megatrypanum) pestanai in British badgers 663–688. (Meles meles). International Journal for Smith, F. G. A. M. 1967. Siphonaptera of Parasitology, 4: 439–440. Mongolia. Results of the Mongolian-German Puntsagdulam, J. & Altanchimeg, D. 2005. On Biological Expeditions since 1962. 43: 77–115. the knowledge of the Mammalian fl ea fauna Smith, F. G. A. M. 1973. Some Siphonaptera from (Siphonaptera) in Mongolia. Mongolian Mongolia. Results of the Mongolian-German Education University Scientifi c paper, 4(4): Biological Expeditions since 1962. Aus dem 58-66. Zoology Museum, in Berlin. 49: 47-48. Reading, R. P., Kenny, D. & Steinhauer-Burkart, Whithing, M. F., Whithing, A. S., Hastriter, M. W. B. 2011. Ikh Nart Nature Reserve. Second & Dittmar, K. 2008. A molecular phylogeny of edition. ECO Nature Edition Steinhauer- fl eas (Insecta: Siphonaptera): origins and host Burkart OHG, Germany. pp 64. associations. Cladistics, 24: 677–707.

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