Oribatid mites (acari: oribatida) as an intermediate host of tapeworms (cestoda) in the soil ecosystem of Viet Nam

JOURNAL OF SCIENCE OF HNUE Chemical and Biological Sci., 2014, Vol. 59, No. 9, pp. 74-80 This paper is available online at ORIBATID MITES (ACARI: ORIBATIDA) AS AN INTERMEDIATE HOST OF TAPEWORMS (CESTODA) IN THE SOIL ECOSYSTEM OF VIETNAM Vu Quang Manh1, Do Thi Duyen1 and Chu Thi Hanh2 1Center for Biodiversity Resources Education & Development, Hanoi National University of Education 2Education and Training’s Department of Vinh Phuc Province Abstract. Oribatid mites (Acari: Oribatida) are an important component in all biological processes that take part in the soil ecosystem. Some of them play as intermediate hosts of tapeworms (Cestoda). This report presents the study results on the role of oribatid mites as intermediate hosts for Cestoda: Anoplocephalidae, and to review their role of transmission for Cestoda in the soil ecosystem of Vietnam. In the soil ecosystem of the grassland and cultivated land within Cat Ba National park, the percentage of oribatid individuals found to be cestode carriers is in following descending order: Spring > Autumn > Summer > Winter. The percentage of oribatid species found to be cestode carriers is in following descending order: Summer > Winter > Autumn > Spring. Ten tapeworm species (Cestoda: Anoplocephalidae) are known to parasitize 21 animal species of Vietnam, with oribatid mites being intermediate hosts. Introduced was also the two-host life cycle of tapeworm Bertiella species, with oribatid mites serving as intermediate hosts prior to transmission to the definitive host. Keywords: Oribatid mite (Oribatida), Tapeworm (Cestoda), Intermediate host, Vietnam soil ecosystem. 1. Introduction Oribatid mites (Arachnida: Acari: Oribatida) are small arachnids, with a body length of 0.1 - 0.2 to 1.0 - 1.5 mm. They constitute the main component of micro-arthropod (Microarthropoda) populations in the soil ecosystem, and are an important component in all biological processes that take place in the soil ecosystem, including the improvement of soil fertility. The Oribatida community structures, particularly their species diversity, population densities and distribution are easily Received November 11, 2014. Accepted December 16, 2014. Contact Vu Quang Manh, e-mail address: vqmanh@gmail.com 74 Oribatid mites (Acari: Oribatida) as an intermediate host of tapeworms (Cestoda)... recognized features, and are closely related to natural and anthropogenic conditions. Recently, Oribatida community structures and their bioindicator’s role of agricultural intensification, of sustainable development of ecosystems, and of climate environmental changes, have been studied around the World (Behan-Pelletier 1999, Appita et al. 2004, Berch et al. 2007, Gergocs & Hufnagel 2009) [5, 6, 11]. A number of oribatid species sequester calcium and other minerals in their thickened cuticle. They disperse bacteria and fungi, both externally on their body surface, and when they are feeding and spores do survive during passage through their alimentary tracts (Gilyarov et Krivolutsky 1975) [1, 3]. Many oribatid mites play a role as intermediate hosts for a number of important tapeworms (Cestoda) (Stunkard 1937, 1940, Hag 1994) [5, 6, 8]. In Vietnam, the first study of oribatid fauna was done by Balogh and Mahunka (1967), followed by studies done by Vu Quang Manh in 1980 and 1985) [9, 12]. Although the scientific result obtained is limited, it served as a valuable scientific base for future study. It is hoped that a means for sustainable management of soil ecosystem can be proposed (Vu Quang Manh 2007, 2013) [10, 11]. This report presents the study results on the role of oribatid mites as intermediate hosts for tapeworms (Cestoda: Anoplocephalidae) in the soil ecosystem of Cat Ba National park, as well as to review a role of oribatid mites as intermediate hosts for a tapeworm (Cestoda) of the soil ecosystem of Vietnam. 2. Content 2.1. Materials and methods The study was conduced in the grassland and cultivated land of Cat Ba National park, Hai Phong, coordinates 2047’N  10704’E. During the period of 2012 - 2013, soil samples (5  5 10) cm3 were collected using rectangular metal samplers that have a 5  5 cm2 surface area, 20 cm in depth, and are open on both ends. Soil samples were taken in three vertical layers (-I) 0 - 10 cm, (-II) 11 - 20 cm and (-III) 21 - 30 cm, and in four seasons: Winter (December 2012), Spring (March 2013), Summer (June 2013) and Autumn (September 2013). They were taken with five replications. Modifications of Berlese-Tullgren funnels were used for extraction of soil oribatid mites from the soil samples. The extraction process was carried out for seven days in the laboratory at a temperature of 25 - 30 C. The sampling and extraction methods are described in detail by Edwards (1991) [2]. Oribatid mites are identified mainly after Balogh (1992, 2002) and Subias (2013), but also referring to the works of Gilyarov & Krivolutsky (1975), Aoki (1999), Weigmann (2006), Krantz & Walter (2009) [1, 4]. The identification of the tapeworm (Cestoda) was made under microscope with reference to Georgiev (2003) [3]. 75 Vu Quang Manh, Do Thi Duyen and Chu Thi Hanh 2.2. Results and discussion 2.2.1. Oribatid mites as a transmission vector of the Cestoda tapeworm (Cestoda) in the Cat Ba National Park, Hai Phong Table 1 presents the findings of this study on the role of oribatid mites as intermediate hosts for tapeworms (Cestoda: Anoplocephalidae) in the soil ecosystem of Cat Ba National park, Hai Phong. Table 1. Percentage of Oribatid mites hosting tapeworms (Cestoda) in the National Park Cat Ba according by seasons Season Oribatida mites Spring Summer Autumn Winter hosting tapeworm March June September December Average (Cestoda) (%) 2013 2013 2013 2012 2012 - 2013 Percentage of oribatid mites by individual 51.85 32.26 38.10 25.29 36.12 Percentage of oribatid mites by species 42.8 80.00 50.00 61.54 76.00 Table 1 showed that in the soil ecosystem of grassland and cultivated land of Cat Ba National park, the percentage of oribatid individuals that are tapeworm’s (Cestoda) carriers are in the following descending order: Spring > Autumn > Summer > Winter, at 51.85%, 38.10%, 32.26% and 25.29%, respectively. The average percentage of oribatid individuals found to be tapeworm’s (Cestoda) carriers in the study area was 36.12%. The percentage of oribatid species found to be tapeworm’s (Cestoda) carriers in the study area was in the following descending order: Summer > Winter > Autumn > Spring, at 80%, 61.54%, 50.0% and 42.80%, respectively. The average percentage of oribatid species found to be tapeworm’s (Cestoda) carriers in the study area was 76.00% (Table 1). The percentage of oribatid individuals found to be tapeworm’s carriers (36.12%), and the percentage of oribatid species found to be tapeworm’s carriers (76.00%), are both unexpectedly high. It is suggested that additional investigations be carried out over a longer period of time, and in different habitats within Cat Ba National Park. 2.2.2. Oribatid mites as intermediate hosts for tapeworm (Cestoda: Anoplocephalidae) parasitizing animals in Vietnam There are a number of oribatid species, which disperse bacteria and fungi both externally on their body surface, and by feeding with subsequent survival of spores during 76 Oribatid mites (Acari: Oribatida) as an intermediate host of tapeworms (Cestoda)... passage through their alimentary tracts. Other mites also play the role of intermediate host in the transmission of tapeworm, which parasitize animals. Studies on oribatid fauna of Vietnam, including their role as an intermediate host of the tapeworm (Cestoda) were carried out by a Vietnam-Russian collaborative project from 1995 - 2005. The study findings were thought to be significant (Krivolutsky, Vu, Phan 1997) [6]. The study found ten tapeworm species (Cestoda: Anoplocephalidae) which were parasitizing 21 animal species of Vietnam. These ten tapeworm species were found to be carried by oribatid mites that serve as an intermediate host in their transmission (Table 2). Of the ten tapeworm species mentioned above, after Le et al. (2003), only the species Bertiella studeri (Blanchard, 1891) parasitizes humans [7]. Table 2. Anoplocephalidae species (Cestoda) using oribatid mites as intermediate hosts and their animal-hosts Tapeworm species Animal species: (Cestoda: Anoplocephalidae) using Oribatida as an intermediate host Hosts of Anoplocephalidae (Cestoda) species 1. Anoplocephala manubriata Railliet, Henry & Bauche 1914 1. Elephans indicus: 1 host/species 2. Anoplocephala perfoliata (Goeze, 1782) 2. Equus caballus: 1 host/species 3. Bertiella studeri (Blanchard, 1891) 3. Macacus cynomolqus, Macaca mullata, Pygatbrix nemaeus, Hylobates concolor: 4 hosts/species 4. Bertiella anapolitica Baylis, 1934 4. Ruttus ruttus, R. exulans: 2 hosts/species 5. Moniezia benedeni (Moniez 1879) 5. Cervus unicolor, Bos indicus: 2 hosts/species 6. Moniezia expansa (Rudolph, 1810) 6. Bos indicus, Capra biscus, Ovis aries tragulus: 3 hosts/species 7. Mosgovoyia pectinata (Goeze 1782) 7. Lepus peguensis: 1 host/species 8. Paronia bocki Schmelz, 1941 8.Magalaema faiostricta, M. laglanfieri, M. asiatica: 3 hosts/species 9. Paronia pycnonoti Yamaguti, 1935 9. Pycnonotus sinensis, P. jacosus, Criniger pallidus: 3 hosts/species 10. Pseudanoplocephala crawfordi Baylis, 1927 10. Sus scrofa: 1 host/species Total: 10 tapeworm Total: 21 animal host/species (Cestoda: Anoplocephalidae) species 77 Vu Quang Manh, Do Thi Duyen and Chu Thi Hanh 2.2.3. Life cycle of tapeworms in the genusBertiella Stiles et Hassall, 1902 (Cestoda: Anoplocephalidae) Tapeworms of the genus Bertiella Stiles et Hassall, 1902 (Cestoda: Anoplocephalidae) are commonly parasites of non-human primates. However, B. studeri and B. mucronata have been found in children that have had contact with non-human primates (Xin Sun et al. 2006) [14]. The life cycles of Bertiella species are not completely known. It is generally believed that the genus undergoes a two-host life cycle, the first is an arthropod intermediate host (usually an oribatid mite), and the second is a vertebrate definitive host. For those species implicated in human infection, the vertebrate definitive host is usually non-human primates. The two-host life cycle of Bertiella species is shown in Figure 1 ( dpdx/ HTML/ Bertiella.htm) [14]. Figure 1. The two-host life cycles of Bertiella species tapeworm with intermediate hosts Oribatida (No. 2) As can be seen in Figure 1, the eggs and prognostics are passed in the feces of the definitive host. Oncospheres are ingested by the arthropod intermediate host. 78 Oribatid mites (Acari: Oribatida) as an intermediate host of tapeworms (Cestoda)... This host is believed to be one or several species of oribatid mites (No. 2 in Figure 1). In the arthropod intermediate host, the oncospheres develop into cysticercoids. The definitive hosts become infected after ingesting oribatid intermediate hosts that are carrying cysticercoids. The adult tapeworms reside in the small intestine of the definitive host, where they attach to the mucosa with the aid of an unarmed scolex. Very rarely humans also serve as definitive hosts for Bertiella tapeworm. Normally, human found to be bertiellosis carriers have had contact with primates. Xin Sun et al. (2006) [13] found two species in human: Bertiella mucronata and Bertiella studeri. The B. studeri is found in Africa and Asia. Humans have been known carriers of Cestoda in Argentina, Brazil, Borneo, China, Cuba, Saint Kitts, India, Java, Malaysia, Mauritius, Paraguay, Singapore, the Philippines, Sri Lanka, Thailand and Yemen. The first known case [7] of a Bertiella studeri tapeworm infestation in human in Vietnam was recorded by Le Thi Xuan et al. (2003). 3. Conclusion It is found that, in the soil ecosystem of grassland and cultivated land of Cat Ba National park, the percentage of oribatid individuals found to be cestode carriers is in following descending order: Spring > Autumn > Summer > Winter. The percentage of oribatid species found to be cestode carriers is in following descending order: Summer > Winter > Autumn > Spring. Ten tapeworm species (Cestoda: Anoplocephalidae) have been found to be parasitizing 21 animal species in Vietnam, with oribatid mites serving as an intermediate host for tapeworms. Introduced was also the two-host life cycle of tapeworm Bertiella species, with oribatid mites serving as intermediate hosts prior to transmission to the definitive host. Acknowledgements. 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