New Host Records, Redescriptions and New Species of Labiostrongylinea (Nematoda: Chabertiidae) from Macropodid Marsupials, with a Revised Host-Parasite Checklist

Summary New host records: from Macropus rufogriseus for Labiosimplex clelandi, M. robustus for Ls. aridus, Thylogale stigmatica for Ls. thetidis, and M. parma for Ls. bancrofti are reported. On re-examination of all material, Labiosimplex quasibancrofti was found to be morphologically indistinguishable from Ls. australis and is therefore a synonym of Ls. australis. A new species of Labiomultiplex, described from a single female from M. parma, is differentiated by the shape of the lateral lips and Lm. kimberleyensis is redescribed from additional material collected from the type-host, Onychogalea fraenata, from Queensland. Two new species of Labiosimplex are described from macropodid marsupials from central Australia. Labiosimplex centralis sp. nov. from the stomach of Petrogale lateralis differs from the most similar of its congenors, Ls. thomasae (both lacking a gubernaculum), in having shorter spicules, a shorter dorsal lobe of the bursa, and in the form of the dorsal ray. Labiosimplex territoriensis sp. nov. from the stomach of M. antilopinus differs from all its congenors in having large multi-lobed oesophago-intestinal diverticula. A new species, Labiostrongylus arnhemensis sp. nov. from the stomach of M. bernardus from the Northern Territory, differs from its congenors in a suite of characters including the position of the deirids, the shape of the oesophago-intestinal diverticula, the length of the dorsal lobe of the bursa, the morphology of the genital cone and gubernaculum and the length of the female tail. A revised host-parasite checklist, including Labiostrongylinea from the island of New Guinea together with those occurring in Potoroidae, is given.

Recent collections of material from macropodid hosts from Queensland and the Northern Territory prompted a re-examination of as yet undescribed material held in the South Australian Museum, Adelaide (SAM) and the CSIRO Wildlife Collection, Canberra (CSIRO) and a re-evaluation of the validity of the species revised or described by Smales (1994Smales ( , 1995Smales ( , 2002, Chilton & Smales (1996) and Smales & Chilton (1997). The results of these analyses are presented below.

Materials and Methods
Specimens dissected from the stomachs of Macropus antilopinus (Gould, 1842), Macropus bernardus Rothschild, 1904, Macropus dorsalis (Gray, 1837 Macropus parryi Bennett, 1835, Macropus robustus Gould, 1841, Onychogalea unguifera (Gould, 1841, and Thylogale stigmatica (Gould, 1860) were fixed in 10% formalin or Berland's fluid and stored in 70% ethanol prior to examination. Other material, from Macropus parma Waterhouse, 1845, Macropus rufogriseus (Desmarest, 1817) and Petrogale lateralis Gould, 1842, registered in the South Australian Museum, Adelaide (SAM), whose collection history is unknown, was also stored in ethanol prior to examination. Worms were examined after clearing in lactophenol, or, if dark brown because of long-term storage in museum collections, in beechwood creosote. Figures were prepared with the aid of a drawing tube and all measurements made with the aid of an ocular micrometer or map measurer. Unless otherwise indicated, measurements of 10 individuals are in micrometres and given as the range followed by the mean in parentheses. All material is now registered in the SAM or the CSIRO Wildlife Collection, Canberra (CSIRO).

New host records
The host range of the following species has been extended.

New and redescribed species
Labiomultiplex sp.
Another collection of material from M. parma (CSIRO N1287) included a single immature female that could not be identified beyond genus level. The measurements of this specimen are as follows: Length 18 mm, width 0.68 mm. Oesophagus 2850 long; nerve ring 2550, excretory pore 2650 from base of lips. Female tail 1050 long, vulva 1800 from tail tip. Vagina 625 long; sphincter longest element of ovejector. The suite of characters available for examination from this specimen, including the morphology of the lateral lip (with a protrusion on the buccal surface, Fig. 2) and cephalic papillae (hook-like) are indicative of it representing an as yet undescribed species.

Female
Measurements of allotype followed by those of 10 specimens, this study.

Remarks
The new material examined for this study confirms the validity of Lm. kimberleyensis. That the specimens are larger overall is probably because they are more mature, with eggs being described for the first time. This new material confirms the proportions of the reproductive systems of the male and female with minor amendments. For the male the spicule tips are both similarly curved, with the alae extending almost to the tips and the paired bifid appendages on the posterior lip of the genital are not relatively long. For the female all the elements of the ovejector are about the same length rather than the infundibulum being the shortest element (Smales 1994).
The morphology of the anterior end has also been clarified. The submedian lips are slightly ridged. The oesophagus, previously interpreted as widening suddenly at about 1/3 its length is now known to widen gradually, ending in a terminal bulb. This form of the oesophageus is intermediate between having two regions of the oesophageal corpus with a terminal bulb, as found in Labiomultiplex, and a simple clavate oesophagus, without a terminal bulb, as in Labiosimplex, and is consistent with the analysis of Smales (2002). The examination of these specimens showed that the position of the excretory pore was variable, being found always posterior to the deirids but either anterior or posterior to the nerve ring.

Remarks
Labiosimplex centralis sp. nov. differs from Ls. thomasae (Smales, 1995), the only other species of Labiosimplex described to date in which a gubernaculum has not been found, in the form of the bursa; all lobes are about the same length in Ls. centralis but the dorsal lobe is longest in Ls. thomasae; the dorsal ray gives off lateral branchlets after bifurcation from the dorsal trunk in Ls. centralis but before bifurcation in Ls. thomasae; the spicules of Ls. centralis (6460-8075) are shorter than those of Ls. thomasae (9000-9900). Labiosimplex centralis is closest to those species of Labiosimplex with lateral lips the same length or longer than the submedian lips and lobes of the bursa separate, namely Ls. clelandi (Johnston & Mawson, 1939) and Ls. bancrofti (Johnston & Mawson, 1939) (see key of Smales 1995). Labiosimplex bancrofti, with the lateral lips longer than submedian lips, differs from both Ls. centralis and Ls. clelandi. Labiosimplex centralis further differs from both these species in the form of the dorsal ray, the length of the spicules (6460-8045 compared with 5400-6100 and 3500-6800 respectively), the shape of the female tail, relatively blunt without terminal knob in Ls. centralis longer and tapering to a tip with or without a terminal knob in Ls. bancrofti and Ls. clelandi. The eggs of Ls. centralis (195-290 by 100-120) are larger than those of Ls. bancrofti (100-140 by 60-75) or Ls. clelandi (135-160 by 80-90).
The host of Ls. centralis is registered in the SAM only as 'rock wallaby,' one animal from Ernabella and 3 animals from Mt. Liebig. The only Petrogale species known to occur in central Australia (South Australian and Northern Territory localities) is P. lateralis (see Strahan 1995). Accordingly this material has been assigned to P. lateralis.
Three other labiostrongylin species, Ls. petrogale (Johnson & Mawson, 1938), Ls. pearsonensis (Smales, 1995) and Labiosimplex sp. 2, are also found in P. lateralis (see Smales 1995). Labiosimplex centralis further differs from Ls. petrogale in the length of the lateral lips which are shorter in Ls. petrogale; the form of the oesophago-intestinal diverticula, bilobed in Ls. petrogale; the form of the bursa, ventral lobes shorter than dorsal lobes in Ls. petrogale; the proportions of genital cone, the posterior lip relatively larger in Ls. petrogale; the vestibule the shortest element of the female ovejector in Ls. petrogale but the same length as the infundibula in Ls. centralis; female tail, short, (720 long) with terminal knob in Ls. petrogale, longer (800-1445) without terminal knob in Ls. centralis. Labiosimplex pearsonensis further differs from Ls. centralis in having longer spicules (9700-12100); the form of the dorsal ray, lateral branchlets are given off before the dorsal trunk bifurcates; the shape of the female tail, tapering, rather than stubby, and a sinuous vagina vera.
A single male worm, found in P. lateralis from Mt Liebig, was described briefly by Johnston & Mawson (1938) as similar to Ls. longispcularis (Wood, 1929) anteriorly, but with shorter spicules 1:5.6 body length; the specimen being 24mm long. Although the spicules of males measured for this study were longer, the males were also longer, giving a similar 1:5, spicule to body length ratio. Consequently this specimen, designated Labiosimplex sp. 2 by Smales (1995), is here considered to be Ls. centralis.
The host, Petrogale lateralis, consists of four subspecies and two as yet unnamed races (Eldridge & Close 1995). Of the three parasite species differentiated above, Ls. petrogale and Ls. centralis occur in the MacDonnell Ranges race from localities in Central Australia while Ls. pearsonensis occurs only in P. lateralis pearsoni from Pearson Island, South Australia.

Remarks
Labiosimplex territoriensis sp. nov. differs from all other species of Labiosimplex in having large multi-lobed oesophago-intestinal diverticula. With lateral lips shorter than submedians and spicules shorter than 6000, it is closest to Ls. robustus (Smales, 1995) and Ls. occidentalis (Smales, 1995) (see key of Smales 1995). Labiosimplex territoriensis further differs from Ls. robustus in having the dorsal ray shorter than the lateral rays, not longer; in the form of the bifid appendages on the dorsal lip of the genital cone; shorter spicules (3400-4165 compared with 4300-5500); shorter vagina (645-850 compared with 1000-1400) and smaller eggs (114 by 60-67 compared with 215-275 by 70-90). Labiosimplex territoriensis further differs from Ls. occidentalis in the form of the dorsal ray, branchlets given off close to bifurcation not after; the form of the dorsal lip of the genital cone, appendages irregularly bifid not long and finger like; shorter female tail (935-1410 compared with 1280-1760) and vulva closer to tail tip (1975-2940 compared with 2880-3480).
Labiosimplex territoriensis has been found only in M. antilopinus from the Northern Territory. A sample of 10 M. antilopinus collected from Mt Surprise, Queensland in 1977, was not infected with any labiostrongylin species. This suggests that the geographic distribution of Ls. territoriensis is limited to the Northern Territory populations of the host.

Remarks
Of the three previously described species of Labiostrongylus, L. labiostrongylus Yorke & Maplestone, 1926, L. grandis Mawson, 1938 andL. narbalekensis Smales, 1994, Labiostrongylus arnhemensis sp. nov. is closest to L. labiostrongylus, both having spicules in the range 4000-5000 long; in the proportions of the dorsal ray and ovejector and in having the female tail ending in a knob (Smales 1994). Labiostrongylus arnhemensis differs from L. labiostrongylus in the position of the deirids, closer to the base of the lips (550-950 as compared with 1040-1280); the oesophago-intestional diverticula not bilobed in L. arnhemensis; the dorsal lobe of the bursa longer than the lateral lobes in L. arhemensis; the paired appendages of the posterior lip of the genital cone trifid in L. arnehemensis but up to 10 irregular projections in L. labiostrongylus; the gubernaculum cordate in L. arnhemensis, sub-rectangular in L. labiostrongylus; the female tail shorter in L. arnhemensis (780-1200 as compared with 1600-2000).
The material, SAM AHC 6386, from M. bernardus, listed by Smales (1995) as Labiostrongylus (Labiosimplex) sp. 4. has been re-examined and here determined to be L. arnhemensis. The specimens from M. bernardus, listed as L. labiostrongylus (see Smales 1995), noted by Smales (1994) as being in poor condition and having differences in the genital cone, were assigned to L. labiostrongylus pro tem. This material is here identified as L. arnhemensis.
Macropus bernardus, found only in a relatively small area of Arnhem Land is occasionally seen in company with M. antilopinus, which has a more extensive range across the monsoonal north (Calaby 1995). A third macropod, the wallaby Macropus agilis (Gould, 1842) is also widely distributed across northern Australia and the tropical east coast (Merchant 1995). Sharman collected M. agilis, M. antilopinus and M. bernardus from Jabiluka in August and September of 1979. The labiostrongylins dissected from M. agilis (SAM AHC 6420) were all, with the exception of a single immature female, identified as L. labiostrongylus (see Smales 1994). This single female, with deirids 670 from the base of the lips, and other measurements congruent with L. arnhemensis rather than L. labiostrongylus is here considered to be L. arnhemensis. Only specimens of L. territoriensis (as described above) were found in M. antilopinus and only specimens of L. arnhemensis were found in M. bernardus.
Macropus robustus is the third of the wallaroo group of kangaroos, found in Arnhem Land. No M. robustus have been collected from Arnhem Land however. The only hosts that have been examined from the Northern Territory were collected near Katherine, and were not infected with labiostrongylin worms. Macropus robustus from central Australia and tropical Queensland have, however, been host to L. grandis Johnston & Mawson, 1938. Additional collecting, therefore, is needed to determine whether Labiostrongylus species are host specific (the exception being an occasional infection where M. agilis are in sympatry) as now appears to be the case.

HOST -PARASITE SPECIES CHECKLIST
List of species of the Labiostrongylinea arranged by host. This list provides an update of the hostparasite species list given in Smales (1995) and includes additional data from potoroid hosts and from the Island of New Guinea (Johnston & Mawson 1940;Smales 1982Smales , 1997aSmales ,b, 1999