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Cestoda: Hymenolepididae) from Rodents on Luzon Island, Philippines

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Cestoda: Hymenolepididae) from Rodents on Luzon Island, Philippines Syst Parasitol (2015) 90:27–37 DOI 10.1007/s11230-014-9528-x Description of two new species of Hymenolepis Weinland, 1858 (Cestoda: Hymenolepididae) from rodents on Luzon Island, Philippines Arseny A. Makarikov • Vasyl V. Tkach • Scott M. Villa • Sarah E. Bush Received: 4 September 2014 / Accepted: 23 September 2014 Ó Springer Science+Business Media Dordrecht 2014 Abstract Our helminthological examination of Hymenolepis in the relative position of both poral and murid rodents on Luzon Island, Philippines, revealed antiporal dorsal osmoregulatory canals, which are a remarkable diversity of Hymenolepis Weinland, shifted bilaterally towards the margins of proglottides 1858. Here we describe two new species based on in relation to the ventral canals, and in possession of specimens from murid rodents Rattus everetti (Gu¨n- testes situated in a triangle and eggs with very thin ther) and Apomys datae (Meyer) collected from Luzon outer coat. A total of seven species of Hymenolepis are Island. Hymenolepis alterna n. sp. differs from all known from the Philippine archipelago. This total known species of Hymenolepis in having irregularly includes the cosmopolitan species Hymenolepis di- alternating genital pores. This feature has not been minuta (Rudolphi, 1819), which was likely introduced reported from any previously known member of to the island with invasive rats. Strikingly, all seven Hymenolepis. Additionally, Hymenolepis alterna n. known species occur on the island of Luzon alone. By sp. also differs from other Hymenolepis spp. in the comparison, only six Hymenolepis spp. are known relative position of both poral and antiporal dorsal from the whole Palaearctic and seven from the osmoregulatory canals which are shifted towards the Nearctic despite a much better level of knowledge of middle of the proglottis in relation to the ventral canals rodent helminths in these zoogeographical regions, as on both sides of the proglottides, and in having curved well as vast territories, diverse landscapes and very or twisted external seminal vesicle, covered externally rich rodent fauna. This suggests that Hymenolepis spp. by a dense layer of intensely stained cells. Hymenol- may have undergone an unusually active radiation in epis bilaterala n. sp. differs from all known species of the Philippines. Possible explanations of this phenom- enon are discussed. A. A. Makarikov Institute of Systematics and Ecology of Animals, Russian Academy of Sciences, Siberian Branch, Frunze Str. 11, Introduction 630091 Novosibirsk, Russian Federation Cestodes in the genus Hymenolepis Weinland, 1858 V. V. Tkach (&) Department of Biology, University of North Dakota, 10 primarily parasitise rodents. A few species parasitise Cornell Street, Grand Forks, ND 58202, USA bats and one parasitises hedgehogs. Members of this e-mail: [email protected] genus share several morphological features such as: an unarmed scolex containing a rudimentary rostellar S. M. Villa Á S. E. Bush Department of Biology, University of Utah, 257 South apparatus, ventral osmoregulatory canals connected 1400 East, Salt Lake City, UT 84112, USA by transverse anastomoses, cirrus-sac with well- 123 28 Syst Parasitol (2015) 90:27–37 pronounced muscular walls, vagina surrounded by Ehrlich’s haematoxylin, dehydrated in an ethanol circular musculature, saccate uterus, and eggs with a series, cleared in methyl salicilate (after Mayer’s thick outer coat (Mas-Coma & Tenora, 1997; Gulyaev haematoxylin) or clove oil (after Ehrlich’s haematox- & Mel’nikova, 2005; Makarikova et al., 2010; Mak- ylin) and mounted in Damar gum. Some specimens arikov & Tkach, 2013; Makarikov et al., 2013). A were mounted in Berlese’s clearing medium to morphologically similar genus Talpolepis Gulyaev & facilitate the examination of the cirrus armature and Mel’nikova, 2005 was erected based largely on the the organization of the eggs. presence of two distinct characters: dorsal osmoreg- Type-material was deposited in the parasite collec- ulatory canals asymmetrically shifted relative to tion of the Harold W. Manter Laboratory (HWML) of ventral canals, and thin cirrus-sac wall lacking obvious the University of Nebraska, Lincoln, Nebraska. The musculature. The distinction between Hymenolepis types were deposited at HWML with the understand- and Talpolepis is clouded by the recent discovery and ing that some will ultimately be repatriated to description of two species from the Philippines that collections in the Philippines. Hosts were deposited exhibit intermediate morphological characters. at the University of Kansas Natural History Museum, Although placed in the genus Hymenolepis, H. bicau- Lawrence, Kansas (KUMNH). da Makarikov, Tkach & Bush, 2013 and H. hau- Syntypes and vouchers of Hymenolepis uranomidis kisalmii Makarikov, Tkach & Bush, 2013 have dorsal Hunkeler, 1972 deposited in the Geneva Museum of osmoregulatory canals shifted in relation to the ventral Natural History (MHNG INVE 18679, INVE 18680, canals and cirrus-sac with muscular walls. With INVE 1868, INVE 18685) were studied for compar- continued biotic surveys in the Philippines, we have ative purposes. Measurements are given in microme- discovered two more species with morphological tres except where otherwise stated. characters that are intermediate between Hymenolepis and Talpolepis. Like H. bicauda and H. haukisalmii these two new species also have osmoregulatory Hymenolepis alterna n. sp. canals shifted in relation to the ventral canals and cirrus-sac with muscular wall. Despite some similar- Type-host: Philippine forest rat Rattus everetti (Gu¨n- ities, these cestodes have unique morphological char- ther) (Rodentia: Muridae). The new cestode species acters clearly differentiating them from all other was found in both specimens of R. everetti examined previously described Hymenolepis species. Herein, in the type-locality. we describe these two new species and discuss the Type-locality: IDC Forestry land, Barangay Casapsi- validity of the morphological criteria used to define the pan, Municipality of Casiguran, Aurora Province, genus Talpolepis. Luzon Island, Philippines (N 16.293, E 122.186; 1 m a. s. l.). Site in host: Small intestine. Materials and methods Type-material: Holotype, HWML-75062 (one speci- men on two slides; field number P.2902#1A, 1B, host Rodents were collected in the summers of 2009 and KUMNH # 167932), labelled: ex. Rattus everetti,IDC 2011 at several sites on Luzon Island, Philippines, Forestry land, Barangay Casapsipan, Municipality of as a part of a biodiversity survey of terrestrial Casiguran, Aurora Province, Luzon Island, Philip- vertebrates and their parasites. The two new species pines, 1.vii.2009, coll. V. Tkach. Paratypes, HWML- described in the present work were found in the 75063 (one specimen on two slides; field number Philippine forest rat Rattus everetti (Gu¨nther) in the P.2902#2A, 2B); HWML-75063 (one specimen on Aurora Province and the Luzon montane forest two slides; field number P.2902 slide1, slide2) and mouse, Apomys datae (Meyer) in the Cagayan HWML-75063 (field number P.2904, host KUMNH # Province. 167933) (all labelled identical to the holotype). Animals were trapped using live traps and pitfall Etymology: The species name refers to the very traps. Cestodes were removed from the intestine, distinctive morphological feature of the species, rinsed in saline, heat-killed in hot water, and preserved namely the irregularly alternating genital pores, which in 70% ethanol. They were stained with Mayer’s or is unique among species of Hymenolepis. 123 Syst Parasitol (2015) 90:27–37 29 Description (Figs. 1–2) 130–144; 169 9 137; n = 12), with thick muscular walls, not reaching lateral margins of scolex. Rhyn- [Based on 5 specimens; measurements of the holotype chus unarmed, 49 9 7 (39–49 9 4–7; 45 9 5; n = 3), are followed by the range, mean values and number of invaginated in rostellar pouch 152 9 85 (152–175 9 measured specimens in parentheses]. Fully developed 82–90; 162 9 85; n = 3); rostellum absent (Fig. 1A, strobila 165 (165–170; n = 2) mm long, with B). Rostellar pouch with muscular wall, osmoregula- maximum width at pregravid or gravid proglottides, tory canals penetrate through rostellar pouch wall. 2.9–3.8 mm. Strobila consisting of 390–421 craspe- Neck 347 (295–347; n = 3) wide. dote proglottides. Scolex slightly flattened dorso- Ventral osmoregulatory canals 107–172 (105–172; ventrally, 380 (380–410; 389; n = 3) wide, not clearly 135; n = 13) wide, connected by transverse anasto- distinct from strobila (Fig. 1A, B). Suckers unarmed, moses. Dorsal osmoregulatory canals 25–41 (20–41; round or oval, 160–170 9 130–141 (154–189 9 31; n = 13) wide, shifted on both sides towards middle Fig. 1 Hymenolepis alterna n. sp. A, Holotype (HWML-75062), dorsoventral view of scolex; B, Paratype (HWML-75063, P.2902#2B), dorsoventral view of scolex; C, Holotype, male mature proglottides; D, Holotype, hermaphroditic mature proglottides; E, Holotype, genital ducts, dorsal view. Scale-bars: A, B, E, 200 lm; C, D, 500 lm 123 30 Syst Parasitol (2015) 90:27–37 Fig. 2 Hymenolepis alterna n. sp. A, Paratype (HWML-75063, P.2904), cirrus and vagina, ventral view; B, Paratype (HWML-75063, P.2902#2A), egg; C, Holotype (HWML-75062), postmature proglottides from dorsal side, showing uterine development; D, Paratype (HWML-75063, P.2902#2B), pregravid proglottides from ventral side, showing appearance of ventral uterine diverticula; E, Paratype (HWML-75063, P.2902#2B), gravid proglottis from ventral side, showing saccate uterus with ventral
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