On the Helminthofauna of Moschus Moschiferus

Abstract

A helminthological study of the digestive tracts of 15 Far Eastern musk deer (Moschus moschiferus turovi ) of Primorsky Krai detected single nematodes, which were assigned to the following taxons: Spiculopteragia spiculoptera , Nematodirus filicolis , Pygarginema skrjabini , and Trichuris sp. The species S. spiculoptera was registered for musk deer for the first time. Analyses of the literature data on the species composition of musk deer helminths concluded that there was a necessity for further helminthological studies examining these ruminants.

Keywords

Musk deer ; Moschus moschiferus ; Helminths

Introduction

Helminthofauna of musk deer (Moschus moschiferus L., 1758) represents a particular interest for researchers. Musk deer combine the features of ancient and modern ruminants and occupy an important place in mountain taiga ecosystems, which often define a characteristic of regional Asian faunas ( Prikhodko, 2003 ). The way of life of musk deer and the inaccessibility of their habitat significantly limit this research. Data concerning helminthic fauna of musk deer are fragmentary and, in certain cases, contradictory. The purpose of this study was to investigate the species composition of digestive tract helminths of Far Eastern musk deer (M. m. turovi ) and analysis of the published data on musk deer helminthic fauna.

Materials and Methods

This helminthological research study of the digestive tract of 15 Far Eastern musk deer (nine adult males, two adult females, one young male and three young females) used standard methods (Ivashkin et al., 1971 ). The material was collected in Primorsky Krai, a Terneisky area during the snow seasons (November–February) from 2010 to 2014.

Nematodes were cleared with 10% aqueous glycerin in temporary total preparations (Ivashkin et al., 1971 ). Species identification was performed on the basis of morphology, and specifically on reproductive system peculiarities according to data obtained from Skrjabin et al. (1954) , Pryadko (1976) , and Kuznetsov (2006) . The female species was not determined.

Results and Discussion

Individual nematodes were found in the contents of the gastrointestinal tract of all examined animals (in most cases — in the abomasum and small intestine). The intensity of the infection ranged from one to six nematodes. In two animals, there were only female nematodes observed in two and four individuals. In two cases, there were only males observed in one and three individuals. Spiculopteragia spiculoptera and Nematodirus filicolis were registered. In addition, one individual of the Spiruridae family was detected: Pygarginema skrjabini in the abomasum of one of the animals. In addition, we found 66 of these nematodes in the contents of the omasum in another musk deer. Two individuals of Trichuris sp. were detected in the colon of a young female musk deer.

One of these species (S. spiculoptera ) was registered for the first time in musk deer.

It has been proposed that helminthiasis comprises a significant group of parasitic diseases of musk deer. However, there is currently little information on helminths of musk deer (Prikhodko, 2003 ). Indeed, the only one publication dedicated directly to the helminthic fauna of musk deer in the territory of the former USSR is the article of Kadenazii (1958) . This author presents his own data of 13 animal autopsies performed during the period between 1933 and 1941, and declares the discovery of 11 helminth species for musk deer (2 cestode species — Moniezia expansa and Taenia hydatigena and nine species of nematodes — Trichostrongylus axei , Trichostrongylus colubriformis , Ostertagia ostertagi , N. filicolis , Capillaria bovis , Trichocephalus ovis , Setaria kabargi , Pneumocaulus cadenazii and Nematodirus sp.). Data on the last two species are cited from articles by Shults and Andreeva (1948) who described a new species P. cadenazii of musk deer in the Moscow Zoo; and by Sokolova (1955) who found Nematodirus sp. of musk deer in Kazakhstan. Importantly, 6 musk deer of 13 animals examined by Kadenazii (1958) were maintained for some time in the Moscow Zoo, where they could obtain non-specific types of worms.

Information on helminthological studies of musk deer in different regions of the former Soviet Union was also presented by Asadov (1960) , Safronov (1961) , Oshmarin and Parukhin (1963) , Gubanov (1964) , and Pryadko (1976) . However, a portion of these data overlaps, and the other portion of these data is contradictory.

According to Safronov (1961) in Yakutia, musk deer have cestode T. hydatigena . The results of N.M. Gubanovs research (1954–1962) resulted in the discovery of fluke Dicrocoelium lanceatum orientalis , cestodes Moniezia baeri and T. hydatigena , and nematodes Pneumocaulus kadenazii , S. kabargi , Nematodirus oiratianus , and Trichocephalus skrjabini in musk deer in Yakutia. In the study of musk deer in the Sikhote-Alin Reserve, Oshmarin and Parukhin (1963) found two species of helminths, P. kadenazii and P. skrjabini .

There is a range of contradictions in the literature concerning the species composition of helminths of musk deer and the citation system used by the authors does not always clarify these contradictions. Thus, in a monograph on helminths of ruminants in the USSR, Asadov (1960) lists only five helminth species of musk deer (for unknown reasons), although the article by Kadenazii (1958) , listed in the bibliography of the mentioned monograph, counts 11 species. Asadov (1960) indicated that only Dicrocoelium moschiferi , Dicrocoelium orientalis , Moniezia benedeni , P. kadenazii , and S. kabargi have been found in musk deer. Thus, the species composition of helminths of musk deer provided by this author is different from that provided by Kadenazii (1958) , which corresponds in only 2 species.

The monograph by Pryadko (1976) , which generalises data on global helminthic fauna of Cervidae, listed 20 species of helminths in musk deer: Dicrocoelium lanceatum , M. expansa , M. benedeni , M. baeri , Thysaniesia giardi , T. hydatigena , C. bovis , Armocapillaria moschiferi , T. ovis , T. skrjabini , S. kabargi , Protostrongylus moschi , P. kadenazii , T. axei , T. colubriformis , Trichostrongylus skrjabini , O. ostertagi , N. filicolis , N. oiratianus , and Nematodirella longissimespiculata . The monograph has a reduced list of references, which enable the determination of data sources on helminth of musk deer, including the geography of their identification.

There is no data on the helminths of musk deer inhabiting the Himalayas and China. Seidel (1993) (quoted in Prikhodko, 2003 ) reported that musk deer from China housed in the Berlin zoo, were parasitised by nematodes from the Trichostrongylus and Ostertagia genera, Dictyocaulus viviparus and protostrongylids. It is clear that a portion of these helminths infected animals that were already housed at the zoo.

Conclusions

Research studies were performed on helminthic fauna of the digestive tract of 15 individuals of musk deer from Primorsky Krai. All examined animals had single nematodes, which were assigned to the following taxons: S. spiculoptera , N. filicolis , P. skrjabini , and Trichuris sp. The species S. spiculoptera was registered in musk deer for the first time.

This study was supported by an RFBR grant #13-04-00341a . The authors gratefully acknowledge support from Wildlife Conservation Society (USA).

References

1. Asadov, 1960 S.M. Asadov; Helminthofauna of Ruminants in the USSR and its Ecological and Geographical Analysis; Academy of Sciences of Azerbaijan SSR, Baku (1960)
2. Gubanov, 1964 N.M. Gubanov; Helminthofauna of Game Mammals in Yakutia; Nauka, Moscow (1964)
3. Ivashkin et al., 1971 V.M. Ivashkin, V.N. Kontrimavichius, N.S. Nazarova; Methods of Collection and Study of Helminthes of Terrestrial Mammals; Nauka, Moscow (1971)
4. Kadenazii, 1958 A.N. Kadenazii; To the knowledge of helminthofauna of musk deer (Moschus moschiferus L.)  ; Proceedings of Institute of Zoology, 9, Academy of Sciences of the Kazakh SSR (1958), pp. 107–110
5. Kuznetsov, 2006 D.N. Kuznetsov; A method for differentiation of nematodes of subfamily Ostertagiinae; Transactions of All-Russian, 43, K. I. Skryabin Institute for Helminthology (2006), pp. 271–278
6. Oshmarin and Parukhin, 1963 P.G. Oshmarin, A.M. Parukhin; Trematodes and nematodes of birds and mammals of the Sikhote-Alin Reserve; Proceedings of Sikhote-Alin Reserve, 3 (1963), pp. 121–181 (Vladivostok, Russia)
7. Prikhodko, 2003 V.I. Prikhodko; Musk deer. Origin, taxonomy, ecology, behavior and communication; Geos, Moscow (2003)
8. Pryadko, 1976 E.I. Pryadko; Helminths of Deer; Nauka, Alma-Ata, Kazakh SSR (1976)
9. Safronov, 1961 M.G. Safronov; About the species composition of pathogens echinococcosis in animals and humans in the Yakut ASSR; Proceedings of Yakutsk Scientific Institute of Agriculture, 3 (1961), pp. 11–12
10. Seidel, 1993 B. Seidel; Keeping Chinese deer in captivity – a veterinary review [Deer of China] ; N. Ohtaishi, H.-I. Sheng (Eds.)Elsevier science publishers B.V (1993), pp. 390–400
11. Shults and Andreeva, 1948 R.S. Shults, N.K. Andreeva; On the morphology and biology of new nematoda from lungs of musk deer; Proceedings of the USSR Academy of Sciences, vol. 62 (6) (1948), pp. 114–116
12. Skryabin et al., 1954 K.I. Skryabin, N.P. Shikhobalova, R.S. Shults; Essentials of nematodology; Trichostrongyloids of animals and man, vol. 3, Academy of Sciences USSR, Moscow (1954)
13. Sokolova, 1955 I.B. Sokolova; The analysis of helminthofauna of wild ruminants in Kasakhstan; Proceedings of Institute of Zoology, 3, Academy of Sciences of the Kazakh SSR (1955), pp. 73–100