Parasitol Res (2010) 106:817–820 DOI 10.1007/s00436-010-1732-2
ORIGINAL PAPER
Description of Lemuricola (Lemuricola) pongoi—male (Nematoda: Enterobiinae) parasitising orangutan Pongo abelii Ivona Foitová & Vlastimil Baruš & Božena Koubková & Šárka Mašová & Wisnu Nurcahyo
Received: 24 November 2009 / Accepted: 4 January 2010 / Published online: 12 February 2010 # Springer-Verlag 2010
Abstract The study presents the first description of male specimen (allotype) of the pinworm species Lemuricola (Lemuricola) pongoi, parasitising Sumatran orangutan (Pongo abelii) from Sumatra (Indonesia). The male specimen morphology presents all features fully corresponding with diagnose of the genus and subgenus Lemuricola. We are agreeing that Protenterobius is synonymous with Lemuricola because the length of tail appendix in males is not a sufficient feature for separation of the genera or subgenera. For L. (L.) pongoi male are characteristic features: body length (4,803 µm), total oesophagus length (530), tail length (235), tip of tail length (188) and spicule length (90).
Introduction There is only limited information available on orangutan parasites in general (survey in Foitová et al. 2009). Several authors have examined free-ranging, semi-captive and captive orangutans, mainly coprologically (Collet et al. 1986; Djojosudharmo and Gibson 1993; Foitová et al. I. Foitová (*) : V. Baruš : B. Koubková : Š. Mašová Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic e-mail:
[email protected] V. Baruš Institute of Vertebrate Biology, Czech Academy of Sciences, Květná 8, 603 65 Brno, Czech Republic W. Nurcahyo Department of Parasitology, Kedokteran Hewan Faculty, Gadjah Mada University, Yogyakarta, Indonesia
1997; Warren 2001; Foitová 2002, 2005; Mul et al. 2007). From theoretical and practical aspects (presence and medication of helminthosis), Mul et al. (2007) point out parasite identification to the species level. In our focus are enterobiosis caused by pinworms, commonly found in primates and man; fatal infection was reported in a captive chimpanzee (Murata et al. 2002). The Sumatran orangutan Pongo abelii Lesson (Primates: Ponginae) is parasitised by three pinworms (Enterobiinae: Oxyuridae) species: Enterobius buckleyi Sandosham, 1950, Pongobius hugoti Baruš, Foitová, Koubková, Hodová, Šimková et Nurcahyo, 2007 and Lemuricola pongoi Foitová, Baruš, Hodová, Koubková et Nurcahyo, 2008; the last species was described on the female specimens only, because no male was available in the collection of the 2002. During the following works in Sumatra (Indonesia) new material of nematodes were collected with one male specimen. In this report, we describe male specimen of L. pongoi which allow final genus submission of this taxon.
Material and methods The locality of investigation, the village Bukit Lawang (former home to a rehabilitation centre for Sumatran orangutans) is situated on the southwestern border of the Gunung Leuser National Park, northern Sumatra, Indonesia (Baruš et al. 2007). The majority of orangutans in this area live in a semi-wild population. From the fresh faeces of one adult female orangutan (named April), pinworms were collected repeatedly in 2005 and 2006 and immediately fixed in 70% ethanol. These nematodes (one male and five females) were cleared in glycerine (mixture 1:1 with 70% ethanol) and examined under a light microscope equipped with differential interfer-
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ence contrast, digital image analysis system (analySIS FIVE DOCU) and a drawing attachment was used for morphometric analysis. The male specimen was transferred to permanent slide and identify as allotype earlier described taxon L. (P.) pongoi by Foitová et al. (2008), females were deposited as reference material of the same species.
Results Oxyuridae Cobbold, 1864 Lemuricola (Lemuricola) pongoi Foitová, Baruš, Hodová, Koubková et Nurcahyo, 2008 (Plate 1) Figs. 1–7 Male of Lemuricola (Lemuricola) pongoi. 1 Head, apical view (reconstruction). 2 Detail of inner teeth with small spurs (reconstruction). 3 Cephalic end, lateral view. 4 Anterior end with oesophagus, lateral view. 5 Posterior end, lateral view. 6 Spicule. 7 General view. Scale bars: 1—20µm; 2—5µm; 3, 6—50µm; 4, 7—400µm; 5—100µm
Male (one specimen; allotype dimensions in micromole, Fig. 1): Whitish nematode. Cuticle with clear transverse striations; cephalic vesicle present and well developed, with transverse margins. Length of body 4,803, maximum width 329, width at bulb 237, width at excretory pore 292, at cloaca 100. Lateral alae with single crest, beginning halfway between anterior extremity and nerve ring, and ending before caudal bursa. Mouth triangular, surrounded by three small lips (wider than higher) and leading into shallow bucal cavity. Dorsal lip with two hemispherical papillae, two subventral lips bears a hemispherical papilla near ventral rim, and other papilla near lateral rim of lips, with amphid conspicuous opening. Mouth cavity armed with three wide chisel-like
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2 4
3 5
7
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teeth arising from each sector of oesophagus. Inner teeth present, triangular and flat with top oriented anteriorly. Tip of inner teeth is armed by very small spurs. Cephalic vesicle 95 length and 117 maximum width. Total oesophagus length 530, pharynx length 37 and 40 width; corpus length 259 and 52 width; short isthmus present, 53 length and 31 width; bulb length 176 and 102 width. Nerve ring 129; excretory pore 945 from anterior extremity. Rounded caudal cuticular bursa, with four pairs of caudal papillae present, first and fourth pairs pedunculate, second and third sessile, flanking cloacal aperture. Plasmidial tubes begin near origin of peduncules of fourth pair, rooted into long and fine conical tail 235 long, tip of tail 188 long. One spicule present well sclerotised, 90 long, with proximal manubrium 33 width. Spicule width in middle part 4.5, distal part sharp point. Ratios: Total body length/total oesophagus length 9.06; total body length/tail length 20.44; total oesophagus length/ spicule length 5.89. Female (five specimens): Morphology and measurements identical with description by Foitová et al. (2008). Type host: P. abelii Lesson, 1827 (Primates: Hominidae) Type locality: Nothern Sumatra, Bukit Lawang (03°32.983′ N, 098°06.908′ E) Site of infection: Intestine (discharged in faeces) Material: Male and female specimens deposited at the helminthological collection of the Research Centre for Biology LIPI, Zoology Division, Puslit Biology LIPI, Cibinong, Indonesia (Cat. No. MZBNa 412).
Discussion Although the male was not found, the species L. (P.) pongoi were assigned by Foitová et al. (2008) to the genus
Lemuricola Chabaud et Petter, 1959 (subgenus Protenterobius Inglis, 1961: Enterobiinae) only preliminary. Chabaud, Brygoo et Petter (1965) distinguish in this genus four subgenera: Lemuricola (Chabaud et Petter, 1959), Ingloxyuris (Chabaud, Peter et Golvan, 1961), Protenterobius Inglis, 1961 and Madoxyuris Chabaud, Brygoo et Petter, 1965. The three subgenera (Lemuricola, Protenterobius and Madoxyuris) form a homogeneous group in which a parallel evolution of several characters is observed (Petter et al. 1972). Recently, the genus Biguetius Chabaud, Petter et Golvan, 1961 is classify as synonym of Lemuricola by Hugot et al. (1996), which was accepted by Baruš et al. (2007). The monotypic genus Ingloxyuris Chabaud, Petter et Golvan, 1961 was previously classified as subgenus of the Lemuricola. According to Hugot et al. (1996) the species Ingloxyuris inglisi parasitising in Lepilemur mustelinus Geoffroy, 1851 from Madagascar does not share the characters of the subfamily Enterobiinae, and until its precise classification, it should be referred to this species as an Oxyuridae sensu lato. Genus Lemuricola distinguish into two morphology groups (Chabaud et al. 1965; Hugot et al. 1995): (1) in males is present caudal and tail appendix (subgenera Lemuricola and Protenterobius); (2) in males, caudal appendix atrophied or absent, tail appendix absent (subgenus Madoxyuris). We are agreeing with Inglis and Dunn (1963) that Protenterobius is synonymous with Lemuricola because length of tail appendix in males is not a sufficient feature for separation of the genera or subgenera. The male pinworm specimen L. (L.) pongoi described present all features of genus Lemuricola (subgenus Lemuricola) defined by Chabaud and Petter (1959), Inglis and Dunn (1963) and Hugot et al. (1996). This subgenus include six taxons: Lemuricola (Lemuricola) contagiosus Chabaud et
Table 1 Selected different features (dimensions in micromole) of males from genus Lemuricola (subgenus Lemuricola) and genus Pongobius Features/species
L. contagiosus
L. microcebi
Lemuricola sp.
L. nycticebi
L. pongoi
P. hugoti
Body length Total oesophagus length Isthmus Tail length Tip of tail length Spicule length Ratio: tip of tail length/ total tail length (%) Hosts
1,838–2,678 328–436 Present 268–436 248–396 88–119 90.8–92.5
1,201–2,016 245–293 Present 124–156 88–115 53–65 60.2–73.7
1,201–1,523 218–273 Present 130–142 99–109 55–76 76.2–76.8
2,200–2,400 400–450 Present 30–47 10 100 21.3–33.0
2,080–2,920 410–490 Present 40–54 84–96 -
4,803 530 Present 235 188 90 80
2,610 367 Absent 104 80 104 76.9
Cheirogaleus major Madagascar
Microcebus murinus Madagascar
Galago senegalensis Africa
Nycticebus caucang Asia Borneo
N. caucang
Pongo abelii
Hugot et al. (1995)
Hugot et al. (1995)
Hugot et al. (1995)
Baylis (1928); Cameron (1929)
Inglis and Dunn (1963)
Pongo abelii Asia Sumatra Our data
Distribution Authors
Asia
Baruš et al. (2007)
820
Petter, 1959; Lemuricola (Lemuricola) microcebi Hugot, Morand et Gardner, 1995; Lemuricola (Lemuricola) trichuroides (Chabaud, Petter et Golvan, 1961), all species have been described from Madagascarian lemurs; Lemuricola (Lemuricola) nycticebi (Baylis, 1928) [syn. Lemuricola (Lemuricola) malayensis Inglis et Dunn, 1963, described from a loris (Nycticebus caucang Boddaert)] from Malaya and Borneo and L. (L.) pongoi from a orangutan from Sumatra; unnamed species Lemuricola sp. by Hugot et al. (1995) described from Galago senegalensis É. Geoffroy, 1796 with African origin, died in captivity (France, Paris). Hugot et al. (1995) consider a transfer from Microcebus to Galago as the most probable explanation. Thus, Hugot et al. (1995) are unable to conclude whether Lemuricola sp. belongs to a different species or must be interpreted as a population of a known species until more material or information can be obtained. The nematode male specimen collected from Sumatran orangutan (P. abelii) can be differentiated from L. (L.) contagiosus, L. (L.) microcebi and Lemuricola sp. by Hugot et al. (1995), the most closely related species, by morphometric variables (Table 1—body length; total oesophagus length; tail length and spicule length – with exclude L. contagiosus; and tip of tail length). Ratio tip of tail length/total tail length (in percent) differ in species as shown in discussion also: L. contagiosus (90.8–92.5%), L. microcebi (60.2–73.7%), Lemuricola sp. (76.2–76.8%), L. nycticebi (21.3–33.3%) and L. pongoi (80%). The species L. (L.) trichuroides was described on two female specimens only by Chabaud et al. (1961). Morphometrical differences L. (L.) trichuroides with L. (L.) pongoi are evidenced by female body length (L. trichuroides 22 mm; L. pongoi female 9.85–15.46 mm only); total oesophagus length (530 vs. 625–709); bulbus width (160 vs. 226–264); distance of vulva—anterior extremity (2.75 mm vs. 2.046–3.093 mm); eggs (92×48 vs. 48–56× 22–28); length of tail (11.0 mm vs. 2.34–2.79 mm). We note that male specimens from the subgenus Madoxyuris differ clearly in total absence of tail tip. This subgenus contain five species: Lemuricola (Madoxyuris) balthazardi Chabaud, Brygoo et Petter, 1965; Lemuricola (Madoxyuris) banchoti Chabaud, Brygoo et Petter, 1965; Lemuricola (Madoxyuris) daubentonie Petter, Chabaud, Delavenay et Brygoo, 1972; Lemuricola (Madoxyuris) lemuris (Baer, 1937); and Lemuricola (Madoxyuris) vauceli Chabaud, Brygoo et Petter, 1965. Acknowledgement Authors would like to thank the Indonesian Institute of Sciences (LIPI) and PHKA for the research permit to work in Gunung Leuser National Park. The study was financially supported by the Foundation “UMI–Saving of Pongidae” Parasites and Natural Antiparasitics in Orangutan and by the Research Project of Masaryk University no. MSM0021622416. The author would also like to thank anonymous reviewers for their helpful comments.
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