1 Transactions of the Royal Society of S. Aust. (20--), 000 (0): 00-00 PELECITUS BARTNERI SP. NOV. (NEMATODA: FILARIOIDEA) FROM THE SUBCUTANEOUS TISSUES OF THE LEG OF PSEPHOTUS CHRYSOPTERYGIUS GOULD, 1858 (PSITTACIFORMES). D.M. SPRATT CSIRO Sustainable Ecosystems, GPO Box 284, Canberra ACT 2601. (email dave.spratt@csiro.au) Abstract Pelecitus bartneri sp. nov. (Nematoda: Filarioidea) is described from the subcutaneous tissues of the leg of a Golden-shouldered Parrot, Psephotus chrysopterygius Gould, 1858 (Psittaciformes) from an aviary in Brisbane, Queensland. It represents the first species of Pelecitus described from an endemic bird in Australia, although P. fulicaeatrae Diesing, 1861, previously known from the Nearctic, Palaearctic and Ethiopian regions, has been recorded from the Eurasian coot, Fulica atra, Linnaeus, 1758. The new species is distinguished from P. fulicaeatrae and P. galli by the presence of granular or hyaline inclusions in the caudal alae of males. It is further distinguished from these species and other species of Pelecitus in avian hosts by the combination of morphometrics of males and females, the presence of only four or five pedunculated pre and post-cloacal papillae in each
2 caudal ala and the absence of any semi-pedunculate or sessile papillae in the male. It is clearly distinguished from the only species known from Australian marsupial hosts, P. roemeri (Linstow, 1905) of kangaroos and wallabies, by the much smaller size of males and females, the small number of cloacal papillae, the presence of granular inclusions in the caudal alae of males, and the much shorter length of the left spicule. KEY WORDS: Nematoda, parasite, Filarioidea, new species, Golden-shouldered parrot, Pelecitus. Introduction Bartlett and Greiner (1986) revised the genus Pelecitus Railliet & Henry, 1910, the most widely distributed genus of avian filarioids known. At that time they transferred two filarioid species of mammals, previously placed in the genus Dirofilaria Railliet & Henry, 1911 to Pelecitus suggesting that they had been captured (Chabaud, 1964) from birds. Pelecitus roemeri (Linstow, 1905) Bartlett & Greiner, 1986 occurs near the insertion of the sartorius muscle in the knee region of Macropodidae in Australia (Spratt, 1972a, 1975). Pelecitus scapiceps (Leidy, 1886) Bartlett & Greiner, 1986 occurs around the tendons in the ankle region of Leporidae in North America (Bartlett, 1984b, c). Both species are easily accommodated in Pelecitus as defined morphologically, both species have sheathed microfilariae and both species develop in the fat body of their intermediate hosts, tabanid flies (Spratt, 1972b, 1974) and mosquitoes (Highby, 1943, Bartlett, 1984a) respectively, as does Pelecitus ceylonensis Dissanaike, 1967 the only species from birds studied
3 developmentally (Dissanaike, 1967). Bartlett and Greiner (1986) suggested that consideration of P. roemeri as recently derived from species in birds explained its curious presence in the highly evolved Macropodidae in Australia, in contrast to the absence of Dirofilariinae in the Australian mammal fauna, with the exception of dog heartworm in the dingo, (Spratt & Varughese, 1975) and its absence from marsupials on other continents. While species of Pelecitus were unknown from birds in Australia at that time, they do occur in birds in Southeast Asia. Subsequently, Mawson et al., (1986) recorded Pelecitus fulicaeatrae (Diesing, 1861), previously known from the Nearctic, Palaearctic and Ethiopian faunal regions, from the Eurasian coot, Fulica atra Linnaeus, 1758 in Australia. This paper reports the second occurrence of a species of Pelecitus from birds in Australia and describes a new species, the first from a bird endemic to south and central Cape York Penninsula., Queensland. Materials and Methods Fixed specimens were received from Dr. Shane Raidal, Veterinary School, Charles Sturt University, Wagga Wagga, New South Wales. They were cleared in lactophenol prior to examination. Measurements are given micrometres, unless otherwise stated. Holotype and allotype measurements are presented first in italics followed by the mean and range of measurements of paratypes in parentheses. Morphological terms such as spicules stout and cephalice papillae protuberant follow Bartlett & Greiner (1986). Types have been deposited in the South Australian Museum, Adelaide
4 (SAM), the Queensland Museum, Brisbane (QM) and the Wildlife Parasite and Pathology Collection housed in the Australian National Wildlife Collection at CSIRO Sustainable Ecosystems, Canberra (W/L N ). Histological sections have been deposited in the latter Collection (W/L HC PA147). Pelecitus bartneri sp. nov. (Figs 1-14) Material examined Holotype:, from subcutaneous connective tissues of leg of Psephotus chrysopterygius Gould, 1858, from an aviary in Brisbane, Queensland, coll: S. Raidal, 23.ii.2010, SAM AHC 45770. Allotype:, same, SAM AHC 45771. Paratypes: 4 SAM AHC 45772, 6, SAM AHC 45773; 4, 6, QM G232131; 3, 1, W/L N5460, all same data. Description Short, irregularly curved nematodes, width relatively uniform over much of length of body, tapering gradually towards anterior end in both sexes, broadening towards posterior end in females, both sexes with rounded posterior extremity. Cuticle thick, with conspicuous, closely-spaced, transverse striations. Lateral alae present, asymmetrical. Four pairs of submedian cephalic papillae not markedly protuberant, arranged as inner circle of four minute papillae and outer circle of four slightly larger papillae. Amphids small, lateral, not salient. Oral opening circular, delicate pre-
5 oesophageal ring present. Oesophagus divided into anterior muscular and posterior glandular regions. Male Body length 6.0, 6.8 (5.9-7.3) mm. Maximum width 398, 392 (344-466) generally in posterior half of body. Nerve ring 159, 163 (158-170) and excretory pore 281, 283 (276-291) from cephalic extremity. Muscular oesophagus 265, 272 (260-292) and glandular oesophagus 345, 369 (345-413) long. Posterior end not tightly coiled. Spicules stout, unequal, dissimilar. Left spicule 91, 89 (83-94)80, and right spicule 73 (67-77) long, stout. Gubernaculum absent. Four or five pedunculated caudal papillae in each ala, generally arranged as three or four pre-cloacal and a single post-cloacal. Additional (fifth) papilla usually anterior and in left ala. Alae with granular or hyaline inclusions. Cloaca 62, 53 (48-58) from posterior extremity. Female Body length 15.0, 14.2 (13.3-15.0) mm. Maximum width 689, 700 (530-901) generally in posterior half of body. Nerve ring 170, 171 (159-186) from cephalic extremity. Excretory pore not observed. Muscular oesophagus 318, 313 (280-345) and glandular oesophagus 557, 484 (450-504) long. Vulva 689, 751 (594-1113) from anterior extremity, generally anterior to oesophago-intestinal junction and markedly protruberent in younger females, posterior to junction and much less protuberent in gravid females with uteri and vagina filled with microfilariae. Anus 151, 161 (151-169) from posterior extremity, with delicate external opening. Post-deirids not observed.
6 Microfilaria (10 specimens free in fixative with nematodes) Loose sheath present. Body length 210 (207-212). Maximum width 4 (4-5), tapering to 2 at caudal extremity. Extremities bluntly rounded. Etymology The specific epithet is derived from the names of Cheryl Bartlett and Ellis Greiner in recognition of their excellent revision of the genus Pelecitus and the suggestion that P. roemeri of macropodids represented a hôte de capture from birds. Discussion The genus Pelecitus is well represented in the avian fauna of South America, especially amongst the Psittacidae. Pelecitus bartneri represents the second species of Pelecitus known from avian hosts in Australia following the record of P. fulicaeatrae from the Eurasian coot, Fulica atra, Linnaeus, 1758 in Mawson et al. (1986). The only other species known from the Australasian region is Pelecitus galli Dissanaike & Fernando, 1974 described from the Burmese red jungle fowl, Gallus gallus spadiceus (Linnaeus, 1758) in Pahang State, Malaysia (Dissanaike & Fernando, 1974). Pelecitus bartneri is distinguished from P. fulicaeatrae and P. galli by the presence of granular or hyaline inclusions in the caudal alae of the male. It is further distinguished from these two species and other species of Pelecitus in avian hosts by the combination of morphometrics of males and females, the presence of only three or four pedunculated pre-cloacal papillae and only one post-cloacal papillae in each
7 caudal ala and the absence of any semi-pedunculate or sessile papillae in the male. It is clearly distinguished from P. roemeri of kangaroos and wallabies by the much smaller size of males (1/5) and females (1/10), clearly divided oesophagus of much shorter length, much shorter left spicule, fewer caudal papillae and shorter tail in males, presence of granular or hyaline inclusions in the caudal alae, more posterior position of the vulva and shorter tail in females. Highlighting just how poorly known are filarioids from avian hosts in Australia, Mawson et al. (1986) list only six genera known from birds, only three of which are identified to species, although there are numerous records of unidentified microfilariae. It should be noted however, that adult worms of some species are short lived and disappear after microfilariae are released from gravid females, although the microfilariae themselves may exhibit surprising longevity. In contrast, there is considerable knowledge of the filarioids of marsupials. In addition to two species of Ceropithafilaria and two of Sprattia with a third awaiting description, eighteen species of the genus Breinlia are known from dasyurid, peramelid, pseudocheirid, phalangerid, potoroid and macropodid marsupials in Australia and Papua New Guinea (Mackerras, 1962; Walker & McMillan, 1974; Spratt & Varughese, 1975; Spratt & Hobbs, 2004). Another eight remain to be described, including the first from murid rodents in northwestern Australia (unpublished observations). This nematode genus also occurs in sciurid rodents in South-East Asia. Thus, the possibility exists that the genus was brought to Australia from South-East Asia with rodents and due to the vagility and sometimes
8 indiscriminate feeding behaviour of mosquito vectors, has spread to a range of marsupial hosts irrespective of their phylogenetic relationships. On the other hand, Pelecitus roemeri has a wide geographic and host range exclusively in the recent Macropodidae in eastern and central Australia but is not known from members of the Potoroidae nor from pademelons (Thylogale spp.), rufous and banded hare wallabies (Lagorchestes spp. and Lagostrophus fasciatus (Péron & Johnston, 1857)) and the quokka (Setonix brachyurus). Pelecitus bartneri came from an aviary bird in Brisbane, very distant from its natural occurrence in southern and central Cape York Penninsula. Consequently, the possibility that it was acquired from another possibly exotic bird in that aviary cannot be excluded, as many vertebrates have acquired exotic infections in captive situations like zoos, fauna parks and aviaries. Acknowledgement I wish to thank Shane Raidal for collecting the material in this study. Mike Austin and Ian Beveridge kindly reviewed an earlier draft of the manuscript. References
9 Bartlett, C.M. (1984a) Development of Dirofilariua scapiceps (Leidy, 1886) (Nematoda: Filarioidea) in Aedes spp. and Mansonia perturbans (Walker) and responses of mosquitoes to infection. Canadian Journal of Zoology 62, 112-129. Bartlett, C.M. (1984b) Development of Dirofilariua scapiceps (Leidy, 1886) (Nematoda: Filarioidea) in lagomorphs. Canadian Journal of Zoology 62, 965-979. Bartlett, C.M. (1984c) Pathology and epizootiology of Dirofilaria scapiceps (Leidy, 1886) (Nematoda: Filarioidea) in Sylvilagus flooridanus (J.A. Allen) and Lepus americanus Erxleeben. Journal of Wildlife Diseases 20, 197-206 Bartlett, CM. & Greiner, E.C. (1986) A revision of Pelecitus Railliet & Henry, 1910 (Filarioidea, Dirofiariinae) and evidence for the capture by mammals of filarioids from birds. Bulletin du Musèum national d Histoire naturelle, Paris, 4 e sér., 8, 47-99. Dissanaike, A.S. (1967) Pelecitus ceylonensis n.sp. from the chick and ash dove, experimentally infected with larvae from Mansonia crassipes, and naturallyinfected crows in Ceylon. Ceylon Journal of Science and Biological Sciences 7, 96-104. Dissanaike, A.S. & Fernando, M.A. (1974) Pelecitus galli n. sp. from the Malayan jungle fowl Gallus gallus spadiceus. Journal of Helminthology 48, 199-203.
10 Highby, P.R. (1943) Vectors, transmission, development and incidence of Dirofilaria scapiceps (Leidy, 1886) from the snowshoe hare in Minnesota. Journal of Parasitology 29, 253-259. Mackerras, M.J. (1962) Filarial parasites (Nematoda: Filarioidea) of Australian animals. Australian Journal of Zoology 10, 400 457. Mawson, P.M., Angel, L.M. & Edmonds, S.J. (1986) A checklist of helminths from Australian birds. Records of the South Australian Museum 19: 219-325. Spratt, D.M. (1972a) Aspects of the life history of Dirofilaria roemeri in naturally and experimentally infected kangaroos and wallabies. International Journal for Parasitology 2, 139 156. Spratt, D.M. (1972b) Natural occurrence, histopathology and developmental stages of Dirofilaria roemeri in the intermediate host. International Journal for Parasitology 2, 201 208. Spratt, D.M. (1974) Distribution of third stage Dirofilaria roemeri in the tissues of Tabanidae. International Journal for Parasitology 4, 477 480. Spratt, D.M. (1975) Further studies of Dirofilaria roemeri (Nematoda: Filarioidea) in naturally and experimentally infected Macropodidae. International Journal for Parasitology 5, 561 564.
11 Spratt, D.M. & Varughese, G. (1975) A taxonomic revision of filarioid nematodes from Australasian marsupials. Australian Journal of Zoology, Supplementary Series No. 35, 1 99. Spratt, D.M. & Hobbs, R.P. (2003) Breinlia (Breinlia) ventricola sp.. nov., a nematode parasite from the heart of the red kangaroo, Macropus rufus, in Western Australia. Transactions of the Royal Society of South Australia, 128, 67 71. Walker, J.C. & McMillan, B. (1974) Breinlia mackerrasae n. sp. (Nematoda: Filarioidea) from the peramelid marsupial, Isoodon macrourus, with a note on Breinlia sp. from the mumut Peramelidae. Journal of Helminthology 48, 39 45. Captions to figures: Figures 1-. Pelecitus bartneri sp. nov. from subcutaneous connective tissues of the leg of Psephotus chrysopterygius Gould, 1858. 1, Cephalic extremity, female, apical view. 2, Cephalic extremity, male, lateral view. 3, Anterior end, male, lateral view. 4, Caudal end, male, lateral view. 5, Caudal end, male, ventral view. 6, Protruberent vulva, non-gravid female, lateral view. 7, Caudal end, male, ventral view, with fourth pedunculate pre-cloacal papilla in left ala. 8, Right spicule, right lateral view. 9. Left spicule, left lateral view. 10, Anterior and posterior ends of sheathed microfilaria. 11, Vagina and vulva, gravid female, lateral view. 12, Cross-section body, female, left lateral ala larger than right, 13, Cross-section body, male, left lateral ala larger than right. 14, Posterior end, female, lateral view. Scale bars: 2, 8-10, 25 µm; 1, 3-7, 14, 50 µm; 11-13, 100 µm.