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New species of Oochoristica (Cestoda; Linstowiidae) and other endoparasites of Trachylepis atlantica (Sauria: Scincidae) from Fernando de Noronha Island, Brazil CHARLES R. BURSEY1, CARLOS FREDERICO D. ROCHA2, VANDERLAINE A. MENEZES2, CRISTINA V. ARIANI2 & DAVOR VRCIBRADIC3 1 Department of Biology, Pennsylvania State University, Shenango Campus, 147 Shenango Avenue, 16146-1537, Sharon, Pennsylvania, U.S.A.. E-mail:
[email protected]. 2 Departamento de Ecologia, Instituto de Biologia Roberto Alcântara Gomes, Universidade do Estado do Rio de Janeiro, R. São Francisco Xavier 524, 20550-011, Rio de Janeiro, RJ, Brazil 3 Departamento de Zoologia, Universidade Federal do Estado do Rio de Janeiro. Av. Pasteur 458, Urca, 22240-290, Rio de Janeiro, RJ, Brazil. E-mail:
[email protected]
Abstract Oochoristica noronhae n. sp. from the small intestines of Trachylepis atlantica Schmidt (Sauria: Scincidae) from Fernando de Noronha, Brazil is described and illustrated. Prevalence of infection was 81%, mean intensity 30. ± 1.8, range (1–7). Oochoristica noronhae n. sp. represents the 88th species assigned to the genus and the 14th species from the Neotropical region. Of the 14 Neotropical species, O. noronhae n. sp. is most similar to O. parvula and O. vanzolinii in that these three species have circular suckers and fewer than 30 testes per proglottid. These three species can be separated on the basis of number of lobules per ovarian lobe; in O. vanzolinii the ovarian lobe is entire, O. parvula has 3–5 lobules/ lobe, O. noronhae has 8–10 lobules/lobe. In addition to O. noronhae n. sp., two species of Nematoda, Moaciria alvarengai Freitas and Spinicauda spinicauda (Heterakidae), one species of Pentastomida, Raillietiella freitasi (Cephalobaenidae) and an undetermined species of Acanthocephala, as a cystacanth, were found. Key words: Oochoristica noronhae n. sp., Trachylepis atlantica, Moaciria alvarengai, Spinicauda spinicauda, Raillietiella freitasi
Introduction The Noronha skink, Trachylepis atlantica Schmidt, is endemic to Fernando de Noronha, a small volcanic archipelago in the equatorial South Atlantic, some 350 km off the northeastern Brazilian coast. It has been shown that T. atlantica belongs to the clade of Afro-Malagasy Mabuya (now in the genus Trachylepis; see Bauer 2003) rather than the South American radiation (Mabuya s. str.) and apparently represents an independent transmarine colonization from the west coast of Africa (Mausfeld et al. 2002; Carranza & Arnold 2003). Three other terrestrial reptiles occur on Fernando de Noronha: two species of introduced lizards, the tropical house gecko, Hemidactyus mabouia (Moreau de Jonnès) (Gekkonidae), and the black and white tegu, Tupinambis merianae Duméril & Bibron (Teiidae), and one endemic lizard, Ridley’s worm lizard, Amphisbaena ridleyi Boulenger (Amphisbaenidae). Until recently, the only reports of endoparasites from the herpetofauna of Fernando de Noronha were descriptions of two nematodes Moaciria alvarengai Freitas and Parapharyngodon alvarengai Freitas and one pentastomid Raillietiella freitasi (Motta & Gomes) and records of the trematode Mesocoelium monas (Rudolphi), all from the same host species: the scincid Trachylepis atlantica (= Mabuya maculata) (Freitas 1956, 1957, 1963, 1967; Motta & Gomes 1968). Recently, Ramalho et al. (2009) published a survey of helminths from one introduced (Tupinambis merianae) and two endemic lizards (T. atlantica and Amphisbaena ridleyi) of Fernando de Noronha, presenting qualitative and quantitative data on infection parameters. They found five helminth species infecting T. atlantica, including two nematodes, M. alvarengai and Spinicauda spinicauda (Olfers), two digeneans, M. monas
Accepted by N. Dronen: 2 Nov. 2010; published: 7 Dec. 2010
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and an undetermined species of Platynosomum, and one cestode, an undetermined species of Oochoristica. The purpose of this article is to describe that cestode as a new species, as well as present the results of our survey of endoparasites of T. atlantica.
Material and methods Thirty-six individuals of Trachylepis atlantica ranging from 65.5 to 103 mm in snout-vent length were collected along a trail near the Americano beach (3º 50’ 48.9” S; 32º 25’ 55.9” W), on the western coast of Fernando de Noronha island, on 29 October 2005 (see Rocha et al. 2009 for details). After capture, each lizard was euthanized with ether and fixed in 10% formalin. Lizards were opened by a longitudinal incision and the digestive tract was removed and searched for helminths. The body cavity, lungs and liver of each lizard were also examined. Nematodes were cleared in a drop of lactophenol, a coverslip was placed over the specimen and identifications were made with a compound microscope. Cestodes were regressively stained in hematoxylin, mounted in Canada balsam and identified with a dissecting microscope. Pentastomids were cleared in Hoyer’s medium. Voucher specimens of endoparasites were deposited in the United States National Parasite Collection (USNPC), Beltsville, Maryland, USA and the parasite collection of the Universidade Regional do Cariri (LZ-URCA), Crato, Ceará, Brazil (see Appendix). The lizards were deposited in the reptile collection of the Museu Nacional, Rio de Janeiro, Brazil (MNRJ 19027-62).
Results Five species of endoparasites were recovered: a new species of cestode in the genus Oochoristica (Linstowiidae), two species of Nematoda (Moaciria alvarengai and Spinicauda spinicauda [Heterakidae]), one species of Pentastomida (Raillietiella freitasi [Cephalobaenidae]) and an undetermined acanthocephalan cystacanth. Thirtyfour (94.4%) of the 36 lizards examined were infected by at least one endoparasite. There were 2.1 ± 0.8 (1-4) parasite species per infected host. Of the infected skinks, 13 (45%) harbored 1 parasite species, eight (28%) harbored two species, seven (24%) harbored three species, and one (3%) harbored four species. Prevalence, mean intensity and range of infection by endoparasite species (sensu Bush et al. 1997) are given in Table 1. TABLE1. Number of specimens (N), prevalence (P), mean intensity (MI), range of infection and accession number by endoparasite species in the lizard Trachylepis atlantica from Fernando de Noronha island, Brazil. Species
N
P (%)
MI ± 1SD
Range
Accession #
Oochoristica noronhae n. sp.
87
80.5
3.0 ± 1.8
1–7
USNPC103503
Moaciria alvarengai
17
36.1
1.3 ± 0.8
1–4
USNPC103505
Spinicauda spinicauda
357
72.2
13.7 ± 35.7
1–176
USNPC103506
Acanthocephala indet. (cystacanth)
1
2.8
1
---
USNPC103507
Raillietiella freitasi
11
8.3
3.7 ± 1.1
3–5
LZ-URCA300-311
Family Linstowiidae Fuhrmann, 1932 Genus Oochoristica Lühe, 1898 Oochoristica noronhae n. sp. (Figs. 1–4) Type host. Trachylepis atlantica (Schmidt), Noronha skink (Scincidae) Symbiotype: MNRJ 19047; collected on 29 October 2005. Type locality. Fernando de Noronha island, Brazil (3º 51’ S; 32º 25’ W).
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Site of infection. Small intestine. Type specimens. Holotype, USNPC 103503; paratypes, USNPC 103504; Etymology. The new species is named for its collection locality. Description. With characters of the genus: scolex with 4 suckers and without rostellum or armature; proglottids acraspedote; genital pores irregularly alternating; genital ducts lie between osmoregulatory canals; uterus ephemeral; testes posterior to vitellarium. Based on 5 intact specimens. Total length 23–29 mm; proglottid number 46–54; 10–18 immature proglottids, wider than long; 14–19 mature proglottids, isodiametric to longer than wide; 17–24 gravid proglottids, longer than wide; maximum width of strobila, 0.15–0.20 mm. Scolex, distinctly set-off from neck, 0.83–1.02 mm wide; with four circular suckers, 140–158 µm in diameter; neck length, 0.64–0.76 mm. Excretory system of four longitudinal ducts visible throughout length of strobila; genital pores irregularly alternating, situated in anterior quarter of proglottid; genital atrium, 30 µm wide, 30 µm deep; cirrus sac length, 85–140 µm, width 18–24 µm; vagina immediately posterior to vas deferens. Ovary on midline divided into 2 lobes, each subdivided into 8–10 lobules; ovary width 43–61 µm; vitelline gland on midline behind ovary, width 21–27, length 31–42 µm; ootype and Mehlis’ gland complex between ovary and vitelline gland. Testes lie posterior to vitelline gland in a single field; testes number 18–26 per proglottid. In gravid proglottids uterine capsules, 43–49 µm in diameter, each contain a single egg; oncosphere, 27–34 µm in diameter, oncospheal hook 17–20 µm in length. Vagina, vas deferens, and cirrus pouch visible in gravid proglottids. On average 110–130 eggs in terminal proglottid, eggs not occurring lateral of excretory ducts.
FIGURES 1–4. Oochoristica noronhae n. sp. 1. Scolex. 2. Mature progottid. 3. Oncosphere. 4. Terminal, gravid proglottid. Scale bar in micrometers.
Remarks. The 88 species currently assigned to Oochoristica that infect reptiles are presented in Table 2 (data were taken from original papers). One additional species is known, Oochoristica eremophilia Beveridge from the marsupial mammal Antechinus rosamondae Ride (Dasyuridae) from Australia (Beveridge 1977). Of the 14 neotropical species (Table 2) only two, namely O. parvula and O. vanzolinii have circular suckers and fewer than 30 testes per proglottid, as does O. noronhae n. sp. These species can be separated on the basis of number of lobules per ovarian lobe; in O. vanzolinii the ovarian is entire, O. parvula has 3–5 lobules/lobe, O. noronhae has 8– 10 lobules/lobe. In addition, the scolex of O. noronhae is distinctly set off from the neck, while the scolex of O. parvula is of similar width to the neck. Of the remaining 74 species, 17 also have circular suckers and testes numbering 30 or less, namely O. novaezealandae (from Australian realm), O. jonnesi and O. najdei (from Ethiopian realm), O. macallisteri (from Nearctic realm), O. aulicus, O. celebesensis, O. excelsa, O. hemidactyli, NEW SPECIES OF OOCHORISTICA
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NEW SPECIES OF OOCHORISTICA
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O. javaensis, O. junkea, and O. lygosomatis (from Oriental realm), O. brachysoma, O. elongata, O. feliui, O. japonensis, O. okinawaensis, and O. sobolevi (from Palaearactic realm). These species differ from O. noronhae n. sp. in the following ways. In O. brachysoma, O. hemidactyli, O. japonensis, O. okinawaensis, and O. najdei, the testes occur in two clusters. In O. elongata, O. excelsa, O. junkea, and O. novaezealandae, the ovarian lobes are not subdivided into lobules; while in O sobolevi each ovarian lobe consists of more than 24 lobules. Oochoristica celebesensis and O. feliui have scoleces greater than 500 µm in diameter. The suckers of O. javaensis are less than 100 µm in diameter. Oochoristica lygosomatis has one pair of osmoregulatory canals. In O. jonnesi and O. aulicus, the cirrus pouch is greater than 150 µm in length. In O. macallisteri, the scolex is not distinctly set off from the neck.
Discussion Moaciria alvarengai was described by Freitas (1956) from Trachylepis atlantica (as Mabuya maculata) collected on Fernando de Noronha, Brazil. It has also been reported from Anolis scriptus collected in the Caicos Islands, in the Caribbean (Goldberg et al. 1996). Spinicauda spinicauda was originally described by Olfers (in Rudolphi 1819) from the lizard Tupinambis merianae (as T. teguixin) (Teiidae) collected in Brazil and has also been reported in various other Neotropical lizards such as Ameiva ameiva (Teiidae), Anolis armouri, Anolis leachi and Anolis oculatus (Polychrotidae), Basiliscus basiliscus (Corytophanidae), and Enyalioides praestabilis (Hoplocercidae) (McAllister et al. 2010). It was first reported from Trachylepis atlantica by Ramalho et al. (2009), who suggested that S. spinicauda may have been introduced to Fernando de Noronha along with Tupinambis merianae in the 1960s. The pentastomid Raillietiella freitasi was described based on specimens recovered from the lungs of T. atlantica and of the toad Rhinella jimi (= Bufo paracnemis) (Motta & Gomes 1968), and is currently unknown from other hosts. Acanthocephalan cystacanths are here reported for the first time in T. atlantica; these parasites are not infrequently found in reptiles, which are believed to act mainly as paratenic hosts (e.g. Bolette 1997; Bursey et al. 2007). For acanthocephalans parasitic in terrestrial animals the intermediate hosts are usually insects (Nickol 1985), so that their occurrence in insectivorous vertebrates such as lizards is to be expected. Unsurprisingly, the results of our helminth survey of Trachylepis atlantica were very similar to those of Ramalho et al. (2009), with three of the species (Oochoristica noronhae n. sp. and the two nematodes) being recorded in both studies. However, we did not record any trematodes in our survey, whereas Ramalho et al. (2009) recorded two species of that group. On the other hand, Ramalho et al. (2009) did not record any acanthocephalans or pentastomids in their survey. The prevalence and infection intensity of S. spinicauda was similarly high in both studies, but the prevalence of Oochoristica noronhae n. sp. was much higher in our study (81% vs 16%). It is noteworthy that neither our survey nor that of Ramalho et al. (2009) recorded the presence of the nematode Parapharyngodon alvarengai in T. atlantica, despite the fact that this nematode had been originally described from that host species (Freitas 1957). This suggests that P. alvarengai may be no longer present in the T. atlantica population or, at least, that it occurs with very low prevalences in that host. Ramalho et al. (2009) suggested that the current high prevalence of the probably introduced species S. spinicauda may explain the apparent absence of P. alvarengai in T. atlantica, implying that competitive exclusion may have occurred. Based on the data from the present study as well as those from previous studies, the endoparasite fauna of T. atlantica is currently known to total eight species, including one cestode (Oochoristica noronhae n. sp.), three nematodes (Moaciria alvarengai, Parapharyngodon alvarengai and Spinicauda spinicauda), two trematodes (Mesocoelium monas and Platynosomum sp.), one pentastomid (Raillietiella freitasi), and one indeterminate acanthocephalan.
Acknowledgments This study was partially supported by research grants from the Conselho Nacional do Desenvolvimento Científico e Tecnológico (CNPq) (processes # 307653/03-0 and 477715/06-0). Permission to collect the lizards was conceded by the Instituto Brasileiro do Meio Ambiente e Recursos Naturais Renováveis—IBAMA (License # 055/05DIFAS). We are thankful to M. A. Silva, Director of the IBAMA office in Fernando de Noronha Island, for
NEW SPECIES OF OOCHORISTICA
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logistical support. We also thank W. O. Almeida of the Universidade Regional do Cariri (Ceará, Brazil) for his help in identifying the pentastomids.
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