DOI: 10.2478/s11686-011-0067-1 © W. Stefan´ski Institute of Parasitology, PAS Acta Parasitologica, 2011, 56(4), 418–426; ISSN 1230-2821 Gastrointestinal nematodes of Coccymys ruemmleri (Rodentia, Muridae) with the description Montistrongylus giluwensis sp. nov. (Heligmonellidae) and Syphacia coccymyos sp. nov. (Oxyuridae) from Papua New Guinea

Lesley R. Smales Parasitology Section, South Australian Museum, North Terrace, Adelaide, SA 5000, Australia

Abstract Five species of nematode were collected from the digestive tracts of 10 Coccymys ruemmleri from Papua New Guinea. Mon- tistrongylus giluwensis sp. nov. can be distinguished from its congener by its size, in having more ridges in the synlophe, longer spicules and the form of the cuticle on the female posterior end. Syphacia (S.) coccymyos can be distinguished from all other species in the subgenus by having a laterally extended dorso-ventrally constricted oval cephalic plate and both cervical and lat- eral alae, together with the combination spicule length and egg size. The helminth assemblage had similar species richness to that of Chiruromys vates with Odilia mackerrasae the only species in common.

Keywords Montistrongylus giluwensis, Syphacia coccymyos, nematode, Coccymys, murid rodent, Papua New Guinea

Introduction by Musser and Lunde (2009) that C. ruemmleri also spends time in the forest understory. The rodent genus Coccymys (Muridae, Murinae) forms part To the best of my knowledge there have been neither re- of the Old Endemic lineage of murines, the earliest colonists ports of helminths nor records of parasite material in national of the Austro-Papuan, Sahul Region. It is thought to have ar- parasite collections of C. ruemmleri. As part of an ongoing rived in the region about 6–8 million years ago and diversified study of the helminths of New Guinean rodents, specimens of about 5 million years ago (Breed and Aplin 2008). Compris- C. ruemmleri stored as intact bodies in the Bishop Museum, ing two species, Coccymys albidens (Tate, 1951), known only Honolulu, Hawaii (BBM) were examined for helminths. In from the original series of six specimens and C. ruemmleri this paper helminth species are documented, new species are (Tate et Archbold, 1941), the genus has been placed in the described and comments given on the helminths found in Tribe Hydromyini (see Lecompte et al. 2008) within the Chiruromys and Hyomys, the only genera within the Pogono- Pogonomys Division (see Musser and Carleton 2005) of New mys Division for which data are available, and Lorentzimys, a Guinea murines. Coccymys ruemmleri is a montane species New Guinea Old Endemic genus with enigmatic affinities found along the Central Cordillera of New Guinea. There are (Smales 2006, 2011). no first hand observations of the biology of C. ruemmleri (see Musser and Lunde 2009). Its diet may consist only of veg- etable matter (Flannery 1995) or be similar to that of its con- Materials and methods gener Coccymys shawmayeri (Hinton, 1943) and include insects, fruit seeds and vegetation (Musser and Lunde 2009). Complete digestive tracts of 10 individuals of C. ruemmleri Known to be of partly terrestrial habit, having been found on were recovered from intact bodies collected by J.L. Gressitt, fallen logs and on the ground (Flannery 1995), it is postulated A.B. Mirza, Bin Yuo and R. Traub between 1967 and 1977

Corresponding author: [email protected] Nematodes from Coccymys ruemmleri from Papua New Guinea 419

and held at the BBM. Their fixation history was not known A male and an immature female, heligmonellids, were but they had been stored in 70% ethanol following collection found in the small intestine of a host from the southern slopes in Papua New Guinea. Collection localities, with the number of Mt Giluwe, Southern Highlands Province and could not be individuals from each, is given in parentheses. identified further. The male with a body length of 4.9 mm, Coccymys ruemmleri: Southern Highland Province; Doma width 149, oesophagus length 380, simple spicules, 792 long Peaks (1), SSE slopes of Mt Giluwe (2). Morobe Province; Mt a synlophe of about 24 small similar sized ridges midbody and Kaindi 7°21´S, 146°41´E (2), Bulldog Rd 32 km S Wau a relatively large bursa could not be placed in any presently 7°50´S, 146°43´E (1). Chimbu Province; Mt Wilhelm 5°49´S, known genus. 144°57´E (4). The digestive tracts were examined with the aid of a dis- Montistrongylus giluwensis sp. nov. (Figs 1–21) secting microscope and all helminths found were stored in 70% ethanol. Prior to examination nematodes were cleared in General: (Heligmonellidae, Nippostrongylinae). Relatively lactophenol for study as wet mounts. Transverse sections were large robust worms, body usually irregularly coiled. Cephalic prepared by hand cutting with a cataract scalpel and mounted vesicle present with up to 16 fine annulations. Mouth opening in polyvinyl lactophenol. Spicules were mounted in Berlese’s triangular with rudimentary lips; labial and cephalic papillae medium for detailed study. Figures were prepared with the aid not observed. Oesophagus claviform. Nerve ring not observed; of a drawing tube. Measurements, in micrometres unless oth- deirids, large, at about same level as excretory pore, in poste- erwise stated, and presented as the range followed by the mean rior oesophageal region. Synlophe (based on sections from 6 in parentheses, were taken with the aid of an eyepiece mi- worms) of continuous triangular longitudinal ridges in both crometer. All specimens have been returned to the BBM. sexes extends from posterior to cephalic vesicle to immedi- The adequacy of the sample size for determining the ately anterior to bursa or vulva; 14–20 ridges in anterior, 18– species richness of the helminth assemblage was tested 20 in midbody, 17–21 in posterior body; ridges absent on using the bootstrap analysis of Poulin (1998). Terminology dorsal left and lateral right sides. Axis of orientation of ridges for heligmonellid nematodes follows Durette-Desset (1983, from ventral right to dorsal left inclined at about 70° from sag- 1985) and Durette-Desset et al. (1994), for oxyurid nema- gital axis in midbody; 8–9 ridges dorsal side, 9–11 ridges todes follows Hugot (1988) and for bioregions follows Voris ventral side male; 5–8 ridges dorsal side, 8–11 ridges ventral (2000). side female. Ventral ridges slightly larger than dorsal ridges; ridges 5–9 (male), 4–8 (female) larger than 5–9 (male), 4–8 (fe- male). Axis of orientation maintained along body; lacking Results carene. Male: Body length 6.0–8.6 (6.7) mm, width 100–105 Only nematodes were collected from the digestive tracts of 7 (130). Cephalic vesicle 59.5–70 (60.8) long. Oesophageal of the 10 individuals of C. ruemmleri examined. No acantho- length 350–512 (428); deirids, excretory pore 303, 342 from cephalans, cestodes or trematodes were found. The nematode anterior end. Bursa almost symmetrical, right lobe slightly fauna included 5 species, 4 identified to species level, and is larger, pattern of rays 2–3 for both lobes; rays 2, 3 diverge dis- listed, with prevalences, in Table I. Three heligmonellids an tally, recurved ventrally; rays 4 recurved ventrally; ray 6 re- oxyurid and a spirurid were identified. Three hosts harboured curved dorsally; rays 4 more stout than rays 5, 6; rays 2, 3 2, 2 hosts, 3 and 2 hosts 1 nematode species. Using bootstrap more slender. Dorsal lobe longer than laterals, with median analysis it was estimated that the number of gastrointestinal notch; dorsal trunk bifurcates at 2/3 its length, each branch di- helminth species not found in this survey was 0.81 indicating viding again at distal tip; rays 9, 10 symmetrical, rays 8 asym- that 86% of the expected helminth species were found. All metrical, left ray 8 longer arising distally to right ray 8 from were new hosts records and for Odilia mackerrasae and Pro- dorsal trunk, both rays arise proximally to division of dorsal tospirura kaindiensis new locality records. ray. Genital come small, ventral lip with unpaired papilla 0,

Table I. Nematode parasites from 10 Coccymys ruemmleri from Papua New Guinea

Taxon Site in host Prevalence % Heligmonellidae Odilia mackerrasae (Mawson, 1961) small intestine 20 Montistrongylus giluwensis sp. nov. small intestine is missing 50 heligmonellid sp. small intestine 10 Oxyuridae Syphacia (Syphacia) coccymyos sp. nov. caecum 50 Spiruridae Protospirura kaindiensis (Smales, 2001) stomach 10 420 Lesley R. Smales

Figs 1–13. Montistrongylus giluwensis sp. nov., male. 1. Anterior end, right lateral view showing ridges of the synlophe. 2. Genital cone, left lateral view. 3. Genital cone, dorsal view. 4. Tranverse section, anterior body. 5. Spicule tips, separated, left lateral view. 6. Spicule tips sheathed, left lateral view. 7. Spicule, proximal end. 8. Gubernaculum, left lateral view. 9. Transverse section, mid body. 10. Dorsal ray, dorsal view. 11. Transverse section, posterior body. 12. Bursa, dorsal view showing left lateral lobe. 13. Bursa, dorsal view showing right lateral lobe. Abbreviations: d – dorsal, l – left, r – right, v – ventral. Scale bars = 50 µm (1, 10), 25 µm (2–4, 7–9, 11), 10 µm (5, 6), 100 µm (12, 13) Nematodes from Coccymys ruemmleri from Papua New Guinea 421

Figs 14–21. Montistrongylus giluwensis sp. nov., female. 14. Transverse section, anterior body. 15. Anterior end, right lateral view. 16. Trans- verse section, mid body. 17. Ovejector, lateral view. 18. Vagina closed, right lateral view. 19. Transverse section, posterior body. 20. Poste- rior end, lateral view showing blunt tail tip and ventral cuticular pouch. 21. Vagina dilated, right lateral view. Abbreviations: d – dorsal, l – left, r – right, v – ventral. Scale bars = 25 µm (14, 16, 18, 19, 21), 100 µm (15, 17, 20) 422 Lesley R. Smales

dorsal lip with paired papillae 7. Spicules filiform, fused at rior to oesophageal bulb. Cervical and lateral alae small, ir- tips, left tip curved, right tip straight, 580–700 (656) long. Gu- regularly lobed. bernaculum 57.5–62.5 (60.25) long. Male: (measurements of 3 specimens). Body length 1.2– Female: Body length 10.4–16.5(13.9) mm, width 120–185 1.5 (1.3) mm, width 86–125 (103). Oesophageal length 205– (162.5). Cephalic vesicle 55–72.5 (69.9) long. Oesophageal 250 (228); oesophageal bulb 40–63 (53) long, 40–55 (48) length 405–570 (531); deirids, excretory pore 412.5, 446.5 wide. Nerve ring 100, excretory pore 282, 287 from anterior from anterior end. Monodelphic, vulva near posterior end, end. Mamelons, of Syphacia type all with thick muscular 195–262 (225) from tail tip; sphincter 45, shortest element, walls; first 380–610 (503), second 465–710 (582), third 630– vagina 100 and infundibulum 130, longer, vestibule 200, 860 (720) from anterior end. First mamelon 55, second 66, longest element. Cuticle expanded ventrally forming a pouch third 80 long. Tail 235–288 (264) long, caudal tip 180–250 proximal to vulva. Tail reflected ventrally, 42.5–50 (46.5) (217) long. Spicule needle shaped, unornamented 61.2–77.5 long. Tail tip blunt conical. Eggs thin shelled, ellipsoidal, (68.7) long; gubernaculum unornamented, 22–37.5 (31.5) 72.5–75 (74) by 40–45 (42.5). long. Accessory piece unornamented. Two pairs small pre- Type host: Coccymys ruemmleri (Tate et Archbold, 1941). cloacal, 1 pair large post cloacal papillae. Type locality: 2900 m up SSE slopes of Mt Giluwe, South- Female: (measurements of 7 mature specimens). Body ern Highlands Province, Papua New Guinea. length 3.9–5.1 (4.44) mm, width 255–340 (299). Oesophageal Site of infection: Small intestine. length 402–429 (409); oesophageal bulb 94–115.5 (104) long, Prevalence, intensity: 5 of 10 hosts examined; 3–12 worms 94–121 (109) wide. Nerve ring not seen, excretory pore 436– plus pieces. 576 (524), vulva 670–1125 (853) from anterior end. Cuticle Type specimens: Holotype male, allotype female, 4 male, expanded ventrally proximal to vulva. Tail 737–890 (805) 4 female paratypes BBM NG-102008. long. Eggs oval, asymmetrical, smooth thin shelled, shell with Other material examined: 6 males, 9 females, 1140 ft up longitudinal ridge and small operculum, embryonated in utero, Mt Wilhelm, Chimbu Province, BBM NG-100672, 100673, 87.5–99 (94) long, 32.5–39.6 (36.1) wide. 100676, 100681B. Type host: Coccymys ruemmleri (Tate et Archbold, 1941). Etymology: The species is named from the type locality. Type locality: 11400 ft on the slopes of Mt Wilhelm, Remarks: This heligmonellid parasite belongs in the genus Chimbu Province, Papua New Guinea. Montistrongylus because it has a synlophe showing the same Site of infection: Caecum. pattern of pointed ridges oriented from ventral right to dorsal Prevalence, intensity: 4 of 10 hosts examined; 1–19 left, left ventral ridges largest, lacking a carene, a bursa with worms. the right lobe larger, rays 8 asymmetrical and the dorsal ray di- Type specimens: Holotype male, allotype female, 4 female vided distal to the level of the branching of rays 8 from the paratypes BBM NG-100676A. dorsal trunk. In addition the ovejector is of similar proportions Other material examined: 1 male, Bulldog Road 32 km and the female tail of similar shape as occurs in Mon- S Wau, Morobe Province BBM NG-29140; 1 male, 19 fe- tistrongylus. Montistrongylus giluwensis sp. nov. differs from males, Mt Wilhelm, Chimbu Province BBM NG-100673, its only congener, M. ingati Smales et Heinrich, 2010, in being 100681; 2 females, SSE slope Mt Giluwe, Southern Highlands a larger worm (females up to 16.5 mm long compared with Province, BBM NG-101890. 6.5 mm) having up to 21 synlophe ridges rather than 15 at an Etymology: The species name is taken from the host genus axis of orientation from the sagittal plane of about 70° not 55°, name. longer spicules (580–700 compared with 280–365) more com- Remarks: This new species belongs in Syphacia Seurat, plex spicule tips, and females with a posterior ventral cuticu- 1916 because it possesses the suite of characters, including lar expansion, a longer tail (42.5–50 compared with 13–25) morphology of the eggs, ventral cuticular mamelons and gu- and larger eggs (72.5–75 by 40–45 compared with 59.5 by 33) bernaculum proposed by Hugot (1988) to distinguish the (Smales and Heinrich 2010). genus. It falls within the subgenus Syphacia Seurat, 1916 be- cause it has neither the rectangular cephalic plate and the Syphacia (Syphacia) coccymyos sp. nov. (Figs 22–32) well developed triangular lateral alae of the subgenus Crice- toxyuris Hugot, 1988 nor the short conical tail and orna- General: (Oxyuridae, Syphaciinae, Syphaciini). Cuticle with mented accessory piece of the subgenus Seuratoxyuris transverse annulations. Cephalic plate oval, elongated later- Hugot, 1988. Syphacia (Syphacia) coccymyos sp. nov., hav- ally, constricted dorsally and ventrally between mouth open- ing a laterally extended dorso-ventrally constricted oval ing and level of laterally placed amphids and cephalic papillae; cephalic plate, comes closest to Syphacia (S.) abertoni about 45 between amphids in female. Mouth opening sur- Weaver et Smales, 2006, S. (S.) bodjamullaensis Weaver et rounded by 3 relatively large lips. Cephalic vesicle present. Smales, 2010, S. (S.) brevicaudata Weaver et Smales, 2008, Oesophagus with ornamented cuticle lining corpus; distinct S. (S.) carnarvonensis Weaver et Smales, 2010, S. (S.) heli- isthmus terminating in spherical bulb. Deirids not seen. Nerve donensis Weaver et Smales, 2010 and S. (S.) pseudomyos ring surrounding oesophageal corpus, excretory pore poste- Weaver et Smales, 2008 in the key of Weaver and Smales Nematodes from Coccymys ruemmleri from Papua New Guinea 423

Figs 22–30. Syphacia (Syphacia) coccymyos sp. nov. 22. Adult male, lateral view. 23. Anterior end male, lateral view. 24. Cephalic plate, fe- male. 25. Cervical ala, cross section. 26. Lateral ala, cross section. 27. Posterior end female, lateral view. 28. Cephalic end female, lateral view. 29. Vulva, lateral view. 30. Posterior end male, lateral view. Scale bars = 200 µm (22), 100 µm (23, 27), 10 µm (24), 25 µm (25, 26, 28), 50 µm (29, 30) 424 Lesley R. Smales

Figs 31 and 32. Syphacia (Syphacia) coccymyos sp. nov. Light micrographs. 31. Anterior end showing ornamentation of oesophageal lining. 32. Egg showing operculum. Scale bars = 50 µm (31), 10 µm (32)

(2010) to the species of the Sahul bioregion. Syphacia (S.) tion history of the specimens is not known either hypothesis is coccymyos differs from all of the above species in having or- possible. namented cuticle lining the corpus of the oesophagus and both cervical and lateral alae. The only other species of Syphacia with a laterally extended cephalic plate and both Discussion cervical and lateral alae is S. (S.) ohtaorum Hasegawa, 1991 occurring in Mus caroli Bonhote, from Okinawa. Syphacia Although this study presents all the information available on (S.) coccymyos differs from S. (S.) ohtaorum in having or- the helminths of the hydromyin genus Coccymys the results namentation of the cuticle lining the oesophagus, the struc- are limited in that only the gastrointestinal tracts dissected. ture of the first mamelon well defined, a longer spicule Comments on the helminth assemblages found in Coccymys, (61–77 compared with 54–64), a longer male tail (235–288 and other Papua New Guinean hydromyin hosts in the Pogo- compared with 150–186) with longer whip (180–250 com- nomys and Lorentzimys Divisions (Lecompte et al. 2008) for pared with 127–163), a longer female tail (737–890 com- which records are available are valid, however, as all the pared with 254–370) and smaller eggs (87.5–99 compared available information has been gathered using the same with 128–139 long) (Hasegawa 1991). methods. Four other species have been found in Papua New Bootstrap analysis indicated that 86% of gastrointestinal Guinea: namely Syphacia (S.) australasiensis Smales, 2004, helminth species to be found in C. ruemmleri were recovered S. (S.) longaecauda Smales, 2001, S. (S.) lorentzimyos Sma- in this study, suggesting that the five species found thus far les, 2010 and S. (S.) mamelonitenuis Smales, 2010. An demonstrate a species poor helminth assemblage. For Chiru- additional species S. (S.) sulawesiesis Hasegawa et Tarore, romys vates (Thomas), the other member of the Pogonomys 1996 from the Island of Suluwesi has been described from Division of murines that has been studied in any detail, 30 in- the region. Syphacia (S.) coccymyos differs from each of dividuals were examined infected and four nematode species these species in the shape of the cephalic plate and the orna- found (Smales 2011), also a depauperate helminth assem- mentation of the oesophageal lining. Comparative measure- blage. The species poor assemblages of both C. ruemmleri and ments are given in Table II. Ch. vates may be a consequence of an at least partially arbo- The irregular morphology noted for the lateral alae of S. real habitat and a largely herbivorous diet (Flannery 1995, (S.) coccymyos may be either a fixation artefact, the actual Musser and Lunde 2009). Reports from Hyomys dammermani structure being similar to that figured for S. (S.) ohtaorum (see Stein and H. goliath (Milne-Edwards), also from the Pogo- Hasegawa 1991), or a consistent character. Because the fixa- nomys Division, of two nematode species found in the four Nematodes from Coccymys ruemmleri from Papua New Guinea 425

hosts sampled (Smales 2006), is too small a sample to give any indication of probable species richness. 87–99 female

94–121 Lorentzimys nouhuysi Jentink is either the sole taxon in the 436–576 255–340 737–890 402–429 670–1125 3900–5100 Lorentzimys Division (Lecompte et al. 2008) or nested within the Pogonomys Division (Rowe et.al. 2008). An estimated S. coccymyos 100

male 97% of the helminth species assemblage, reported from 11 40–55 61–78 22–38 86–125 235–288 282–287 380–610 205–250

1200–1500 species recorded from 23 individuals, of L. nouhuysi (see Smales 2010) represents a more species rich assemblage than

. Data from Hasegawa found in C. ruemmleri. 77–86 female 96–112 115–145 550–760 288–333 544–670 662–871 378–429 Although no cestodes, trematodes or acanthocephalans 3870–5140

S. muris were found in any of the hosts belonging to the Pogonomys Division three of the 11 helminths found in L. nouhuysi were S. suluwesiensis male 62–77 78–89 31–36 cestodes (Smales 2010). This may reflect the relative propor- 84–100 134–163 139–173 600–935 261–304 915–1310 1650–1910 tions of insects in the diets of the host species. Insects repre- sent about 37% of the diet of L. nouhuysi (Flannery 1995). The assemblage of C. ruemmleri was dominated by helig- 70–88 74–88 female 96–138 360–677 410–912 166–225 269–348

570–1059 monellid nematodes. The only species shared between the host 2310–5030 species was Odilia mackerrasae occurring in Ch. vates and S. muris C. ruemmleri. Odilia mackerrasae is commonly encountered male 38–57 48–56 23–30 70–112 84–108 in both Australian and New Guinean murine hosts (Smales 170–285 208–445 153–234 453–730 1050–1740 1997, 2009; Smales and Heinrich 2010) and appears to be the only heligmonellid species widely distributed across the Sahul

328 region. The finding of Montistrongylus giluwensis may be 72–92 56–63 female 82–107 103–114 313–380 130–181 235–366 950–2000 indicative of a coevolution and speciation event among hosts and parasites in the region, the genus having been previous- ly known only from the hydromyin Paramelomys rubex male S. mamelonitenuis 36–63 66–87 45–75 66–76 41–51 20–32 780–950 264–324 178–251 264–379 (Thomas) in New Guinea. Additional collections of hosts are needed before the third heligmonellid species can be fully characterized and the helminth assemblage fully documented. The oxyurid, Syphacia coccymyos, with a laterally ex- 67–80 87–97 female 385–520 460–620 120–180 410–600 107–125 285–340

2500–3660 tended cephalic plate, is the first species to be found with that character in New Guinea. As such it may represent a link be- lorentzimyos

S. tween the northern species, S. ohtaorum, from Okinawa male 60–80 65–72 67–82 40–50 42–55 17–25 250–335 280–402 147–210

900–1230 (Hasegawa 1991) and the Australian cluster of species recorded from Indonesia and Papua New Guinea, including the cosmopolitan (Weaver and Smales 2010). If this is the case putative ances- tral forms with this shaped plate may yet be found in South- female

94–100 east Asia or the Sunda region. Alternatively this character may 119–127 470–636 310–360 616–850 765–986 408–456 121–127 Syphacia 4000–4400 have arisen independently more than once as murid hosts trav- elled across the regions from Southeast Asia.

S. longaecauda The spirurid Protospirura kaindiensis appears to be distrib- male 76–97 111–148 375–436 600–850 100–160 370–490 240–355

1600–2050 uted in a range of hydromyin hosts throughout the Sahul region. There have as yet been no studies of the New Endemic Rattus 2900

– fauna of the region to determine whether species such as P. kain- 39–47 82–95 73–82 female 355–436 315–570 107–135 436–804 160–268 185–355 diensis are present in both the Old and New Endemic faunas. 1900 As additional murid species are studied for parasites an abundant and diverse helminth fauna is being revealed which 1250 – S. australasiensis male parallels the abundant and diverse murid fauna endemic to 46–55 61–68 29–36 80–102 75–120 297–583 142–181 228–462 148–208 690 Papua and Papua New Guinea (Flannery 1995). Clearly more studies are needed to determine the total number of species present and analyse their origins and relationships.

Comparative measurements (in µm) of species Acknowledgements. This study was partially funded by a travel grant from the ARC/NH&MRC Network for Parasitology. Thanks excretory pore vulva nerve ring are due to Lydia Gaetano for providing access to the material in the bulb width width length Tail length Tail First mamelon Spicule Gubernaculum Body length Anterior to Egg length Oesophagus Table II. Table (1991), Hasegawa and Tarore(1991), Hasegawa and (1996), Smales (2001, 2004, 2010) Bishop Museum. 426 Lesley R. Smales

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(Accepted July 27, 2011)