Cestode parasites of tree kangaroos (Dendrolagus spp.: Marsupialia), with the description of two new species of Progamotaenia (Cestoda: Anoplocephalidae)

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TransactionsoftheRoyalSocietyofS. Aust. (2004), 128(2), 175-185.
CESTODE PARASITES OF TREE KANGAROOS (DENDROLAGUS SPP.:
MARSUPIALIA), WITH THE DESCRIPTION OFTWO NEW SPECIES
OFPROGAMOTAENIA (CESTODA: ANOPLOCEPHALIDAE)
by I. Beveridge* & P. M. Johnson"1"
Summary
Beveridgr, 1. &Johnson, P. M. (2004). Cestode parasites oftree kangaroos [Dendrolagus spp.: Marsupialia),
withthedescriptionoftwonewspeciesofProgamotaenia(Cestoda:Anoploeephalidae). Trans. R. Soc. S.Aust.
128(2), 175-185,30November, 2004.
Two new species ofProgamotaenia Nybelin, 1917 are described from tree kangaroos: P. dendrolagi sp. n.
efarsotmertnheQusemeanlsllianntde,stiannedsPo.fiDreinadnernosliasgsups. bn.enfnreotmtitahneusinDteestViinse,o1f8D8.7daonrdiaDm.tlsumRhaomlstazyi,Co1ll8e8t3t,fr1o8m84IrfiraonmJanyoar.thA-
re-description ofP. wallabiae Beveridge, 1985, from D. doriamts, a new host for the genus, is given. P.
dendrolagi is highly host specific, being restricted to tree kangaroos, while P. wallabiae occurs also in scrub
wallabiesofthegenusDoreopsis Schlegel & Mueller, 1842 from the islandofNewGuinea. Thephylogenetic
relationships ofP. irianensis with congeners are not clear. The life cycles ofthe cestodes are discussed in
relationshiptothearborealnatureofthehostsandthepresumeduseofterrestrialoribatoidmitesasintermediate
hosts.
Kl£Y Words: Cestoda, Anoploeephalidae, Progamotaenia, Dendrolagus, tree kangaroos, Macropodidae, new
species.
Introduction 1906) in D. ursinus Mueller, 1840 from a European
zoo, while Spratt et al. (1991) and Beveridge et al.
The helminth parasites of tree kangaroos (1992) reported P. zschokkei from D. lumholtzi in
(Dendrolagus spp.) are poorly known (Spratt et al. north-eastern Queensland. Spratt et al. (1991) also
1991), with most parasite records being based upon reported the presence ofan undescribed species of
opportunistic collecting involving one or two host Progamotaenia in D. bennettianus De Vis, 1887
specimens. Astudy ofaseries ofsevenD. lumholtzi from Queensland, while Flannery et al. (1996)
Collett, 1884, from north-eastern Queensland reported two species of cestodes, P. wallabiae
(Beveridge et al. 1992) revealed a relatively Beveridge, 1985 and P. cf. doreopsis Beveridge,
depauperatehelminth community, afactattributed to 1985, from D. doriamts Ramsay, 1883 from Irian
the arboreal nature of the host compared with a Jaya. The fragmentary data available to date
predominantly terrestrial mode of transmission of therefore suggest that tree kangaroos might harbour
most of the helminth parasites of macropodid a numberofspecies ofanoplocephalid cestodes.
marsupials (Beveridge & Spratt 1996). A recent In this report, the species of cestodes present in
examination of a limited number of specimens of tree-kangaroosarereviewedandtwonewspeciesare
Dendrolagus spp. from Irian Jaya (Flannery et al. described, one from northern Queensland and one
1996) has suggested that that some species may from Irian Jaya. A further species found in tree
harbour a more complex community of helminths kangaroos, but formerly known only from scrub
than described in previous publications, with some wallabies, P. wallabiae^ is re-described and the
species of helminths occurring in considerable associations between hosts and parasites are
numbers. considered.
Although the cestode genus Progamotaenia
Nybelin, 1917 is abundant in many macropodid Materials and Methods
species (Beveridge 1976, 1978b, 1980, 1985;
Beveridge&Thompson 1979;Turni& Smales 1999; Cestodes obtained were from animals which had
Beveridge & Turni 2003), records ofthe genus from been collected for other purposes. Specimens ofD.
treekangaroosarefew. Loser(1965)inastudyofthe lumholtzi were obtained as road-kills and frozen
histology of the female genital glands of cestodes prior to examination. At autopsy, cestodes were
reported the occurrence of P. zschokkei (Janicki, washed in water and fixed in AFA (Pritchard &
Kruse 1982). Individuals of D. doriamts were
collected for museum specimens and the entire
* Department of Veterinary Science, University of Melhourne, gastrointestinal tracts had been fixed in formalin
ParkvilleVic.3052.
QueenslandParksandWildlifeService,Townsville,Qld4810. prior to examination. Cestodes were removed,
176 I. BEVFRIDGH& P. M.JOHNSON
Figs 1-5. Progamotaenia dendrolagi sp. nov. I. Scolex. 2. Cirrus sac and genital atrium. 3. Premature segment prior to
patency ofgenital atria, showing vaginae extending to atrial primordia. 4. Mature segment showing patency ofatria,
sperminseminal receptaclesanddisappearanceofvaginae. 5. Prcgravidsegmentsshowingsingleuteruswithnumerous
anteriorandposteriordiverticula.All illustrations from holotype. Scalebars-0.1 mm.
NEWCESTODES FROMTREE KANGAROOS 177
washed in waterand stored in 70% ethanol. composedof170 segments; paratypes28-60 (43,n
Cestodes were stained in Celestine blue, = 3) long, width4 -6 (5,n = 3). Scolex prominently
dehydrated in ethanol and cleared in methyl 4-lobed, 0.76 in diameter in holotype, 0.74 - 1.21
salicylate. In thick or dark specimens, the cleared (1.04, n = 4) in diameter in paratypes, with oval
cestodeswereallowedtoharden in methyl salicylate suckers 0.39-0.42 (0.41, n = 3) long by 0.17 - 0.24
and the tegument and longitudinal muscle layers (0.21, n=3) widein holotype, 0.30-0.38 (0.35, n-
removed with fine forceps to reveal the medullary 10) long by 0.20 - 0.33 (0.27, ti = 10) wide in
organs. In some instances, hand-cut transverse paratypes. Neck absent or very short. Segments
sections were prepared of mature or gravid transversely elongate, with prominent velum
segments. Cestodes were mounted in Canada overhanging subsequent segment; posterior border
balsam. Parts of new species of cestodes were ofvelum straight or slightly undulate; as segments
embedded in paraffin, serially sectioned at a increase in size along strobila, velum covers [h- to2h
thickness of 10 jim and the sections stained with ofsucceeding segment. Premature segments 0.27 -
haematoxylin and eosin. 0.31 (0.29, n = 5) long, 1.56 - 1.01 (1.72, n = 5)
Drawings were made using a drawing tube wide, velum 0.05 - 0.13 (0.09, n = 5) long in
attached to an Olympus BH microscope. holotype; 0.28 -0.44 (0.37, n = 5) long, 2.57 -3.13
Measurementsweremadewithanocularmicrometer (2.95, n = 5) wide, velum 0.20 - 0.24 (0.22, n = 5)
or a ruler and are presented throughout the paper in long in paratypes. Mature segments 0.29 - 0.32
millimetres asthe mean followed, in parentheses,by (0.30, n = 5) long, 1.95 - 2.65 (2.39, n = 5) wide,
the range and the numbers of measurements made velum 0.08 - 0.10 (0.09, n = 5) long in holotype;
(n=). 0.39 - 0.47 (0.42, n = 5) long, 3.04-3.90 (3.50, n =
Type specimens have been deposited in the South 5) wide, velum 0.17 - 0.26 (0.22, n - 5) long in
Australian Museum, Adelaide (SAM). paratypes. Pregravid segments0.47-0.61 (0.52, n=
Host nomenclature follows Groves & Flannery 5) long, 3.12-3.82 (3.56, n= 5) wide,velum 0.19-
(1989), Spratt et al (1991) and Flannery et al 0.26 (0.23, n - 5) in holotype; 0.35 -0.66 (0.51, n =
(1996). 5) long,4.91 -5.93 (5.41, n = 5) wide, velum 0.27 -
0.43 (0.35, n = 5) long in paratypes. Genital pores
Progamotaeniadendrolagisp. nov. paired, in middle of lateral segment margins. In
(FIGS 1-5) prematuresegments, genitalatriumcircularindorso-
ventralviews,notpatent;inmaturesegments,genital
Synonyms: Progamotaenia sp. nov. of Spratt et al. atrium consists of narrow central passage with
1991, p. 62 {Dendrolagus bennettianus); Progamo- numerous anterior and posterior diverticula; when
taenia zschokkei (Janicki, 1906) of Spratt et al. everted, cirrus extrudes from genital papilla formed
(1991), Beveridge et al. (1992) {Dendrolagus by everted genital atrium. Cirrus sac elongate, with
lumholtzi). thick muscular wall, extending beyond
osmoregulatory canals into medulla. Cirrus sac in
Holotype: From Dendrolagus bennettianus De Vis, holotype0.37-0.45 (0.41,n=5)longby0.10-0.14
1887, Bargoo Creek, Mount Windsor State Forest, (0.12, n = 5) in mature segments, 0.58 - 0.68 (0.63,
Queensland(23°38' S 141°40' E), 19.ix. 1986,coll. n - 5) long by 0.16 - 0.20 (0.17, n = 5) wide in
G. Richards, SAMAHC 22654. pregravidsegments; inparatypes0.39-0.61 (0.50,n
=5) longby0.12-0.16(0.14, n= 5)wideinmature
Paratypes: From Dendrolagus lumholtzi Collett, segments, 0.51 - 0.64 (0.58, n = 5) long by 0.17 -
1884 Queensland 3 specimens, Mount Baldy State 0.21 (0.19, n=5)wideinpregravidsegments. Cirrus
: ;
Forest,(17° 17' S 145°27' E), 7.viii.1991, coll. P.M. armed distally with numerous, regularly-arranged
Johnson (SAM AHC 28511-3); specimen, spines; width of cirrus diminishes proximally with
I
Herberton (17° 23' S 145° 23' E), l.i.1990, coll. similar reduction in size of spines; most proximal
P.M. Johnson (SAM AHC 28514-5); fragments of 1 region ofcirrus unarmed, leads into sub-circular or
specimen, Malanda (17° 21' S 145° 36' E), 1993, fusiform internal seminal vesicle; cirrus sac between
coll. P.M. Johnson(SAMAHC28516); 2specimens, distal extremity and internal vesicle filled with
Palmerston(17°32' S 145°40' E), coll. I6.xii.I976, densely-staininggland cells. Internal seminalvesicle
P.M. Johnson (SAM AHC 12231, 22132), (serial in holotype 0.09-0.16 (0.12, n = 5) long by 0.08 -
sections SAM AHC 28517) (1 slides). 0(0..0290,(0n.0-8,5)nl-on5g)biyn0m.a1t2ur-e0s.e1g6m(e0n.t1s3,, t0i.=165)-w0i.d2e8
Site in host: Small intestine in pregravid segments; in paratypes 0.12 - 0.18
(0.16, n = 5) long by 0.08 - 0.10 (0.09, n - 5) in
Description mature segments, 0.12 - 0.20 (0.19, n = 5) long by
Small cestodes, holotype 54 long, 4 wide, 0.08-0.20(0.12,n- 5)wide inpregravid segments.
178 1. BEVKR1DGE & P. M. JOHNSON
External seminal vesicle clearly visible only in post- - 0.11 in diameter; transverse canal. 0.02 - 0.04 in
mature segments, elongate, extends medially and diameter connects ventral canals at posterior margin
anteriorly from proximal pole ofcirrus sac, covered of each segment. Inner longitudinal musculature
with layerofglandularcells; externalseminalvesicle weakly developed, consisting ofelongatebundles of
0.21 -0.27 (0.25, n= 5) longby 0.05 -0.08 (0.07,n up to 12 muscle fibres in medial /one of cortex;
= 5) in holotype, 0.31 - 0.47 (0.38, n - 5) long by transverse muscles form distinct band at cortico-
0.07 - 0.12, n = 5) wide in paratypes; vas deferens medullary junction; dorso-ventral muscles
arises from proximal pole of external seminal prominent, arranged as numerous individual fibres
vesicle.Testesinvariablyarrangedintwocompletely crossingcortex and medulla.
separate groups extending from ventral Development of segments in holotype genitalia
:
osmoregulatorycanalstolevelofseminal receptacle; fully formedby segment 55; genital atrium becomes
3 to 8 rows oftestes in antero-posterior direction; 3 patent and sperm appears in seminal receptacle in
to4 layers indorso-vcntral plane; 36-55 (43,n=5) segment70; uteruscommencesfillinginsegment80;
pergroup in holotype; 35 -47 (43, n = 5) pergroup ovary involuted with remnants of vitellarium still
in paratypes. Testis diameter 0.043 - 0.059 (0.050, present by segment 120; anterior and posterior
n=!0) in holotype, 0.055 - 0.070 (0.062, n = 10) in diverticula of uteri present in segment 125; total
paratypes. numberofsegments 170.
Vagina tubiform, opening to genital atrium
posterior to cirrus sac; connection between vagina Remarks
and genital atrium clearly visible in premature Most species ofProgamotaenia possess two uteri
segments prior to patency of genital atrium; once persegment. Schmidt(1986) separatedthosespecies
genital atrium becomes patent, distal vagina with a single uterus into two genera Adelataenia
atrophies and becomes inapparent. Vagina leads to Schmidt, 1986 and Wallabicestus Schmidt, 1975,
ovoid seminal receptacle on posterior margin of neitherofwhich was accepted by Bcveridgc (1994).
segment medial to cirrus sac; receptacle empty prior Thespeciesdescribed above istherefore allocatedto
to patency of genital atrium, filled with sperm Progamotaenia based on the definition ofthe genus
immediately after genital atrium becomes patent. by Beveridge (1994) which includes species with
Seminalreceptacle inholotype0.21 -0.27 (0.24, n= both single and paired uteri. Species with a single
5) long by 0.15 - 0.20 (0.16, n = 5) wide in mature uterus are P. effigia Beveridge, 1976, P. ewersi
segments, 0.20 - 0.41 (0.34, n = 5) long by 0.16 - (Schmidt, 1975), P. villosa (Lewis, 1914) and P
0.27 (0.21, n = 5) wide in gravid segments; in zschokkei(Janicki, 1906).
paratypes 0.26 - 0.51 (0.37, n = 5) long by 0.16 - The specimens described above differ from P.
0.27 (0.21, n = 5) wide in mature segments, 0.37 - villosa and P. zschokkei in lacking a distinctly
0.55 (0.48, n = 5) long by 0.12 - 0.23 (0.19, n = 5) fimbriated velum and differ from P. effigia and P.
wide in gravid segments. Ovary flabelliform, with ewersiin havingthe testes distributed in two distinct
oocapt nearmedial poleofseminal receptacle; ovary groupsratherthan inasinglecontinuousbandacross
onventralaspectofmedulla. Ovary in holotype0.16 the medulla. Inaddition they differ from P. effigia in
- 0.23 (0.20, n= 5) long, 0.31 - 0.45 (0.40, n = 5) having an external seminal vesicle covered with
wide; in paratypes 0.21 - 0.27 (0.23, n = 5) long, glandularcells(lackinginP. effigia) and in infecting
0.37 - 0.59 (0.44, n = 5) wide. Vitellarium the small intestine ratherthan the bile duct, as is the
horseshoe-shaped, posteriorand dorsal to oocapt; in case with P. effigia. They further differ from P.
holotype0.08-0.10(0.09,n-5)longby0.20-0.23 ewersi in lacking a distal vagina surrounded by
(0.21, n = 5) wide; in paratypes 0.09- 0.12 (0.1 1, n prominent layersofglandularcellsand in havingthe
= 5) long by 0.21 - 0.28 (0.23, n - 5) wide. Mehlis' vagina atrophy following insemination of the
gland spherical, visible only in paratypes, situated in proglottis. The specimens therefore represent a new
U formed by vitellarium, 0.09-0.12 (0.11, n- 5) in species for which the name P. dendralagi is
diameter. Uterus single in each segment situated proposed.
anterior to ovaries; immature uterus tubiform. ThedescriptionofP. dencirolagiisbasedprimarily
extending laterally only to proximal poles ofcirrus upon a single, well-preserved specimen from D.
sacs; in prcgravid segments, uterus develops bennettianus, in which most, but not all features of
numerous anteriorand posteriordiverticula, extends its morphology can be observed. The type series is
laterally, dorsal to osmoregulatory canals, almost completed by a number of specimens from D.
reaching postero-lateral comers of segments. No lumholtzi. The latterspecimens are poorly preserved
gravid specimens present; eggs in all available and while they are not differentiable from the
specimens immature. Paired osmoregulatory canals holotype, are insufficient on their own to permit a
present; ventral canal larger,0.02-0.17 indiameter; fulldescription.Thedescriptionofthenewspeciesis
dorsalcanal external toventral, much narrower, 0.04 therefore based on a collection of specimens from
NEW CESTODES FROMTREE KANGAROOS I7l)
Figs 6-10. Pmgamotaenia ihanensis sp. nov. 6. Scolex. 7. Cirrus sac andgenital atrium. 8. Premature segment showing
patencyofgenitalatria,fillingofseminalreceptacleswithspermbutpoordevelopmentofbothmaleandfemalegenitalia
within segment. 9. Mature segment with fully developed genitalia and single uterus. 10. Pregravid segmentwith fully
developed uteri. Drawingsfromtypes. Scalebars=0.1 mm.
two host species within the same genus and may species which warrants comment isthedevelopment
need to be reviewed if and when more extensive ofthe genital atrium which becomes patent only in
series of cestode specimens from these two host mature segments. This developmental feature has
species become available. One feature of the new only been observed previously in P. capricorniensis
180 I. BEVERIDGE& P. M.JOHNSON
Beveridge & Tumi, 2003 from the black-stripe distally with numerous, regularly-arranged spines;
wallaby, Macropns dorsalis (Gray, 1837), from distal segment of cirrus greatly dilated; width of
&
central Queensland (Beveridge Turni 2003), but cirrus diminishes proximally with similar reduction
provides an additional developmental character in size of spines; most proximal region of citrus
distinguishing the new species from all other unarmed, leads into ellipsoidal or fusiform internal
congeners. seminal vesicle 0.18 - 0.25 (0.23, n = 5) by 0.08 -
0.13 (0.10, n = 5) in mature segments, 0.34 - 0.44
Progamotaenia irianensis sp. nov, (0.40,a=5)by0.15-0.17(0.16,n=5)in pregravid
(FIGS 6-10) segments ; cirrus sac between distal extremity and
internal vesicle filled with densely-staining gland
Synonyms: Progamotaenia cfdorcopsis ofFlannery cells. External seminal vesicleclearly visible only in
etaL, 1996,p. 187. post-mature segments, elongate, extends medially
and anteriorly from proximal pole of cirrus sac,
lloiotype: From Dendrolagus doriamis stellarnm along anteriorborder ofseminal receptacle; covered
Flannery & Seri, 1990, Gunung Ki, Tembagapura, with layer ofglandular cells, 0.33 - 0.51 (0.41, n =
Irian Jaya, Indonesia (4° 05' S, 137° 06' E), 5) by 0.06 - 0.09 (0.08, n - 5); vas deferens arises
collected 19.V.1994 by T. Flannery, SAM AHC from proximal pole of external seminal vesicle.
28512. Testes invariably arranged in two completely
separate groups extending from ventral
Paratvpes: 2 specimens, same data SAM AHC osmoregulatory canals to level of medial pole of
28519-24; serial sections SAM AHC 28525 (5 seminal receptacle; 25 - 47 (37, n = 5) per group; 1
slides), spirit material SAMAHC 32180. to 4 rows oftestes in antcro-postcrior direction; 3-5
layersindorso-ventralplane,0.040-0.060(0.050,n
Site in host: Small intestine. = 10) in diameter.
Vagina tubiform, opening to genital atrium
Description posterior to cirrus sac; connection between vagina
Large, robust cestodes, holotype 95 long, 6 wide, and genital atrium clearly visible in pre-mature
composed of315 segments; paratype 67 long, width segments prior to patency of genital atrium; once
5.0. Scolexprominently4-lobed,0.70-0.80(0.75, n genital atrium becomes patent, distal vagina
= 3) in diameter, with 4 oval suckers 0.36 - 0.44 atrophies and becomes inapparent. Vagina leads to
(0.40, n =4) long by 0.23 - 0.31 (0.26, n =4) wide. ovoid seminal receptacle on posterior margin of
Neck absent or very short. Segments transversely segment medial to cirrus sac and dorsal to female
elongate, with prominent velum overhanging genitalia, 0.35 - 0.62 (0.48, n = 5) by 0.20 - 0.27
subsequent segment; posterior border of velum (0.24, n = 5); receptacle empty prior to patency of
undulate with 29 (27 - 32, n ^ 5) blunt, linguifonn genital atrium, filled with sperm immediately genital
projectionsoverhangingsucceedingsegmentonboth atrium becomes patent. Ovary fiabelliform, 0.24 -
dorsal and ventral aspects of strobila; as segments 0.33 (0.27,n-5)by0.47-0.78 (0.67,n=5),ventral,
increase in sizealong strobila, velumcovers [fc to 2h with oocapt near medial pole ofseminal receptacle;
ofsucceeding segment. Premature segments 0.18 — ovary on ventral aspect of medulla. Vitellarium
0.43 (0.28, n = 5) long, 3.86 - 4.17 (4.02, n = 5) horseshoe-shaped, posterior and dorsal to oocapt,
wide, velum 0.16 - 0.29 (0.20, n = 5) long; mature 0.11 -0.16(0.12, n=5) by0.30-0.39 (0.34, n-5).
segments 0.27 - 0.68 (0.45, n - 5) long, 4.25-5.15 Mehlis'gland spherical, situated in U ofvitellarium.
(4.72, n = 5) wide, velum 0.23 - 0.44 (0.33, n - 5) Uterus usually paired in each segment, occasionally
long; pregravid segments 0.49 - 0.62 (0.56, n = 5) only a single uterus present; situated anterior to
long, 4.91 - 5.85 (5.38, n = 5) wide, velum 0.29 - ovaries; immature uterus tubiform, extending
0.55 (0.40, n = 5) long. Genital pores paired, in laterally only to proximal poles of cirrus sacs; in
middle of lateral segment margins. In pre-mature pregravid segments, uterus develops numerous
segments, genital atrium circular in dorso-ventral anterior and posterior diverticula, extends laterally
views,notpatent; in maturesegments,genital atrium dorsal to osmoregulatory canals, but does not cross
consists of narrow central passage with numerous canals. No gravid specimens present; eggs in all
anterior and posterior diverticula. Cirrus sac available specimens immature. Paired osmo-
elongate, with thick muscular wall, extending just regulatory canals present; ventral canal larger, 0.086
beyond osmoregulatory canals into medulla, 0.59 - -0.094indiameterinmaturesegments,0.094-0.24
0.80(0.69,n=5)long,0.15-0.17(0.16,n=5)wide in post-mature segments; dorsal canal external to
in mature segments, 0.69 - 0.94 (0.81, n - 5) long, ventral,muchnarrower, 0.016-0.031 in diameterin
0.19-0.25 (0.21,n=5)wide in pregravidsegments. mature segments, 0.016 - 0.047 in diameter in post-
Cirrus almost straight or with single flexure; armed mature segments; transverse canal connects ventral
NEWCESTODES FROM TREE KANGAROOS 181
canals at posterior margin of each segment; tiny of the seminal receptacle distinguishes the species
accessory osmoregulatory canal observed medial to from P. lagorchestis in which the testes extend only
ventral canal in sections; transverse canal connects to the poral pole of the seminal receptacle
accessory canals at posterior margin of segment. (Beveridge & Thompson 1979). The cestodes from
Inner longitudinal musculature strongly developed, D. dorianus have a similar number of linguiform
consisting of bundles of up to 20 muscle fibres projectionstothevelumasP. capricorniensis,but in
concentrated in medial zone of cortex; transverse the latter species a single uterus is present
muscles form distinct band at cortico-medullary (Beveridge & Turni 2003). A singular feature of
junction; dorso-vcntral muscles prominent, arranged these specimens appears to be the fact that the uteri
as numerous individual fibres crossing cortex and donotcrossthe osmoregulatorycanals, even in near
medulla. gravidsegments.Thischaracterisunusualwithinthe
Development of segments in holotype: genitalia genus but has been reported in P. zschokkei (see
fully formed by segment 100; genital atrium Beveridge 1976, p. 67). In P. spearei, the uteri only
becomespatentin segment 120andspermappears in cross the canals in the last few segments (Beveridge
seminal receptacle in segment 123; uterus 1980).As fully gravid specimens were not available
commences filling in segment 170; ovary involuted in the current series ofspecimens examined, it may
with remnants ofvitellariun still present by segment be prudent not to rely on this feature as a specific
210; total numberofsegments 315. character, but given the state ofdevelopment ofthe
specimens available, it seems unlikely that a major
Remarks development of the uterus will occur beyond the
The species described above is based on few 300th segment. Consequently, the species described
specimens which are fragmented and imperfectly above can be easily distinguished from all known
preserved. However, because of the difficulty of congeners. It is therefore considered to be new and
obtaining material from tree kangaroos occurring at the specific name is given because these arethe first
high altitudes in Irian Jaya, the description ofanew newrepresentativeofthegenus described from Irian
species based on these specimens, albeit incomplete, Jaya, Indonesia.
is consideredjustified.
The species is characterised by two uteri, a Progamotaenia wallabiae Beveridge, 1985
prominently fimbriated velum and testes distributed (FIGS 11-15)
exclusively in two groups. In a small number of
segments, a single uterus is present, but the same Material examined: 3 specimens from Dendrolagus
phenomenon has been described previously in R dorianus stellarum Flannery & Seri, 1990, Gunung
/estivaby Beveridge(1976, p. 54) and is common in Ki, Tembagapura, Irian Jaya. Indonesia (4° 05' S,
species of the anoplocephalid genus Mosgovoyia 137° 06' E), collected 19.V.1994 by T. Flannery,
Spasskii, 1951 from lagomorphs (Beveridge 1978a). SAM AHC 28526-8; spirit material SAM AIIC
Species with a similar combination of characters 32181.
are: P. thylogale Beveridge & Thompson, 1979, P.
lagorchestis (Lewis, 1914), P. spearei Beveridge, Description
1980, P. dorcopsis Beveridge, 1985 and R Large, robust cestodes, to 108 long, 5.0 wide,
queenslandensis Beveridge, 1980. Ofthese species, composed of225 segments. Scolex prominently 4-
P. queenslandensis frequently has the testes lobcd, 0.99 - 1.17 in diameter, with oval suckers,
distributed in a single band as well as in two groups 0.62-0.70(0.64,n=4)by0.35-0.47 (0.40,n=4).
(Beveridge 1985). The species described above has Neck absentorveryshort,upto0.23 long. Segments
an external seminal vesicle with a distinctive transversely elongate, with prominent velum
covering ofglandularcells, thereby distinguishing it overhanging subsequent segment; posterior border
from P. spearei. The projections of the velum are ofvelum very slightly undulate with c. 30-35 blunt-
distinctly linguiform in this species, differentiating tipped lobes, not separated into individual
them from the triangular projections seen in P. projections, overhanging succeeding segment on
lagorchestis, P. dorcopsis and P. queenslandensis. both dorsal and ventral aspects of segment; as
Thenumberofprojections ofthevelum (27-32) also segments increase in size along strobila, velum
distinguishes the specimens from P. thylogale (18- covers '/:. to 2h of succeeding segment. Premature
2\),P. dorcopsis(13-17)andP. queenslandensis(17- segments 0.23 - 0.39 (0.29, n = 5) long by 3.82 -
20) (Beveridge 1985). The number of testes per 4.91 (4.42, n= 5) wide, velum 0.09-0.18 (0.12,n=
group (25-47) distinguishes the specimens from P. 5) long; mature segments 0.37 - 0.56 (0.44, n = 5)
thylogale (50) and P. dorcopsis (18-25) (Beveridge longby 4.52-6.40 (5.63, n=5) wide, velum 0.21 -
1985), while the distribution ofthe testes from the 0.27 (0.23, n = 5) long; pregravid segments 0.620 -
osmoregulatory canals to anterior to the aporal pole 0.82 (0.73, n = 5) long by 4.29 - 5.30 (5./00, n - 5)
182 I. BEVERIDGE& P. M. JOHNSON
Figs 11-15. ProgamotaeniawallabiaeBeveridgc, 1985. Specimens fromDendrolagusdoriamis, 11. Scolex. 12. Genitalia
ofmaturesegment. 13. Prematuresegmentfollowingpatencyofgenital atriaandfillingofseminal receptacles,butwith
maleand femalegenitaliapoorlydeveloped. 14. Maturesegment. 15. Pregravidsegment. Scalebars=0.1 mm.
wide, velum 0.35 - 0.64 (0.48, n - 5) long. Genital 5) longby0.23-0.25 (0.24,n=5)wideinpregravid
pores paired, in middle of lateral segment margins. segments. Distal cirrus greatly dilated, armed with
In premature segments, genital atrium circular in numerous, regularly-arranged spines, 0.008 long;
dorso-ventral views, notpatent; in mature segments, proximal cirrusnarrow,coiled,with reduction in size
genital atrium consists of narrow central passage ofspines; most proximal region ofcirrus unarmed,
with numerous anterior and posterior diverticula. leadstofusiform internal seminal vesicle0.22 -0.36
Cirrus sac elongate, with thick muscular wall, (0.27, n = 5) long by 0.11 - 0.17 (0.14, n = 5) wide
extending just beyond osmoregulatory canals into inmaturesegments,0.24-0.47(0.35,n=5) longby
medulla; cirrus sac wider near proximal extremity; 0.16-0.20(0.18,n=5)wide inpregravidsegments;
0.70-0.86(0.78, n=5) longby0.16-0.24(0.20, n cirrus sac between distal extremity and internal
=5) wide in mature segments, 0.92- 1.09 (0.97, n= vesicle filled with densely-staining gland cells.
NEWCESTODES FROM TREE KANGAROOS 1X3
External seminal vesicle elongate, 0.27-0.55 (0.43, Remarks
n = 5) by0.09-0.12 (0.10, n= 5), extends medially Progamotaenia wa/labiae was described by
and anteriorly from proximal pole of cirrus sac, Beveridge(1985)basedonthree specimensfrom the
along anteriorborder ofseminal receptacle; covered grey scrub wallaby, Dorcopsis lucfuosa (D'Albertis,
with layer of glandular cells; vas deferens arises 1874) (= D. veterum (Lesson & Garnot, 1826) in
from proximal pole of external seminal vesicle. Spratt et al. 1991) from Papua. Because the species
Testes invariably arranged in two completely was described from such a limited series of
separate groups 30-57 (39, n = 5) per group, specimens and because its occurrence in the tree
extending from ventral osmoregulatory canals to kangaroo, D. doriamts, involves a different host
level of medial part of seminal receptacle; 1 to 4 genus, a description ofthe specimens is provided.
rows oftestes in antero-posteriordirection; atleast2 The occurrence of the species in D. doriamis was
layers in dorso-ventral plane; testisdiameter0.050- first reported by Flannery et al. (1996) and the
0.080 (0.060, n = 10). Vagina tubiform, opening to description presentedhere isbasedon the specimens
genital atrium posterior to cirus sac; connection from the latterreport.
between vagina and genital atrium clearly visible in The new specimens are not gravid, but do not
premature segments prior to patency of genital differsignificantly from the original specimens. The
atrium; once genital atrium becomes patent, distal internal seminal vesicle is apparently larger than in
vagina atrophies and becomes inapparent. Vagina the original description, but all other measurements
leads to ovoid seminal receptacle 0.32 - 0.44 (0.37, conformcloselywiththedescription ofP. wallabiae.
n = 5) by 0.19 - 0.28 (0.24, n - 5), on posterior Beveridge (1985) noted that the broad velum was
margin of segment medial to cirrus sac; receptacle undulate, with about 20 small lobes. In the new
empty prior to patency ofgenital atrium, filled with material, there are 30-35 distinct lobes on each side
sperm immediately genital atrium becomes patent. ofthevelum. Theirarrangement is distinctive in that
Ovary flabelliform, 0.24-0.43 (0.30, n-5) by 0.43 only the tips of the lobes are separated, while the
- 0.57 (0.53, n = 5), with oocapt nearmedialpole of divisions extend anteriorly into the velum without
seminal receptacle; ovary on ventral aspect of separation of the component lobes. This feature is
medulla. Vitellarium horseshoe-shaped, 0.14 - 0.20 unique within the genus as species have either a
(0.16. n = 5) by 0.23 - 0.27 (0.25, n = 5), posterior straight-edged velumoravelumsplitintoprominent
and dorsal to ovarian isthmus. Mehlis' gland triangular or linguiform lobes. In the case of P.
spherical, 0.09 - 0.13 (0.11, n = 5) in diameter, thylogale, the velum is scalloped, but there are no
situated in U of vitellarium. Uterus paired in each thickeningsordivisions extendinganteriorlybeyond
segment, situated anterior to ovaries; immature the edge. The feature described above may be
uterus tubiform, extending laterally to proximal characteristic ofthe species.
poles of cirrus sacs; in pregravid segments, uterus
develops numerous anterior and posterior Discussion
diverticula, crosses osmoregulatory canals dorsally,
extendingtopostero-Iateral marginsofsegments.No The descriptions of cestodes of the genus
gravid specimens present; eggs in all available Progamotaenia presented above suggests that tree
specimens immature. Paired osmoregulatory canals kangaroos, whilenot harbouringahelminth faunaas
present; ventral canal larger, 0.080 - 0.150 in diverse as some other macropodid genera, possess
diameter in mature segments, 0.140 - 0.310 in nevertheless distinctive species of cestodes.
postmature segments; dorsal canal external to Descriptionsarelimitedbythedifficultyinobtaining
ventral, much narrower,0.020-0.060 in diameterin material and by the fact that material obtained can
mature segments, 0.040 - 0.050 in diameter in rarelybepreserved in anideal manner.Nevertheless,
postmature segments; tinyaccessorycanals,0.020 in itispossibletoidentifyspeciesandprovideadequate
diametervisible in some segments, medial to ventral descriptions of them from the material available.
canal; transverse canal connects ventral canals at Notwithstanding the obvious limitations, some
posterior margin ofeach segment, diameter 0.020 - conclusions can be drawn on the species of
0.060; tiny canal connecting dorsal canals 0.012 in Progamotaenia found in tree kangaroos.
diameter. Development of segments in largest Progamotaenia dendrolagi sp. nov. is found in
specimen;genitaliaformedbutimmaturebysegment both of the Australian species of tree kangaroos,
65; genital atrium becomes patent in segment 70; D. htmhoftzi and D. bennettianus, but has not, thus
sperm appear in seminal receptacle in segment 73; far been found in species in New Guinea. The
firstmaturesegment95;uteruscommencesfilling in Australian species of tree kangaroos are closely
segment 110; ovary involuted with remnants of related phylogenetically (Flannery et al. 1996;
vitellarium still present by segment 150; total Bowycr et al. 2003) and may either represent a
numberofsegments 225. recolonisation by the genus from New Guinea
184 I. BEVER1DGF & P. M. JOHNSON
(Winter 1997) or an endemic Australian All species of anoplocephaline cestodes whose
phylogenetic lineage (Bowyer et al. 2003). The life cycles have been fully elucidated utilise
phylogcnetic affinities ofP dendrolagi are not clear oribatoid mites as intermediate hosts (Dencgri
as the (intestinal) species which it most closely 1993). No life cycles ofspecies ofProgamotaenia
resembles, P ewersU is highly distinctive morph- have been elucidated. However, in the case of
ologically. In the absence ofa formal phylogenetic species ofthe related cestode genus Bcrtiella Stiles
analysis of the genus Progamotaenia, the affinities & Hassall, 1902 occurring in Australian possums
ofP dendrolagiare difficultto infer. It is apparently {Trichositrus spp.), also an arboreal mammal, the
highlyhostspecificasthespecieshasnotbeen found initial development of metacestodes has been
&
in other macropodids in north-eastern Queensland observed in oribalid mites (Viggers Spratt 1995)
(Beveridge et al 1989, 1992. 1998). Given the and therefore it seems likely that species of
uncertainty as to the phylogenetic affinities of the Progamotaenia may also utilise oribatoids as
cestode, itsassociationswarrantfurtherinvestigation intermediate host. Ifthis isthecase,the lifecycle is
andmayprovidesignificantinsightsintothemodeof essentially terrestrial as the mites are common in
evolution ofcestodes ofmacropodids. soil and pastures (Denegri 1993). The most
Progamotaenia iriamnsis sp. n. was first reported extensively studied species ofDendrolagus are the
asP. cfdorcopsis(seeFlanneryetal. 1996)basedon Australian species, D. bennettianus and D.
thepresence ofaprominently fimbriated velum, two lumholtzi. D. lumholtzi spends 99% of its time in
uteri andthetestesdistributed intwodistinctgroups. the tree tops and together with D. bennettianus,
Themoredetailedstudypresentedhereindicatesthat subsists primarily on the leaves ofrainforest trees
it is in fact a new species based on the number and and vines (Flannery et at. 1996). Consequently, the
shape ofthe elements ofthe velum. It has only been only opportunity for tree kangaroos to become
found in D. dorianus at a single locality in the infectedwithcestodes occurswhenthey feedon the
mountains of Irian Jaya. The helminths of other ground and accidentally ingest mites which are
macropodids occurring in the area are completely infectedwiththeintermediate stages (cysticercoids)
undocumented and therefore it is not possible to ofthe parasites. This implies thatthey mustfeedon
exclude the hypothesis that the species occurs theground in areaswhere faecescontainingcestode
commonly in other macropodids and may therefore eggshave fallenandconsequently infectedthe local
not be primarily a parasite of tree kangaroos. The mitepopulation. Giventhebiological featuresofthe
scrub wallabies which occur in the same general hosts, it is remarkable that they are infected by any
region, Dorcopsis muel/eri (Schlegel, 1866) and anoploccphalid cestodes. Alternatively, the current
Dorcopsiilus vanheurnei (Thomas, 1922), should studies of host biology may have underestimated
therefore also be considered as potential alternative the extent to which the kangaroos feed on the
hosts. ground. Unpublished observations (PMJ) suggest
Progamotaenia wallabiae was first reported from that in contrast to the published data, both D.
Dorcopsis lucluosa from Papua (Beveridge 1985). bennettianus and D. lumholtzi spend a substantial
The host reported in the original description was D. amount of time on the ground. Were they to feed
veterum, but this species was subsequently consistently on theground in areas in which species
considered a species inqnirenda by Groves & of Dorcopsis also occur, then a ready explanation
Flannery (1989). They indicated that the appropriate could be provided for the occurrence of P.
name for the scrub wallaby from the Port Moresby wallabiae in D. dorianus. More extensive studies
region wasD. luctuosa. ItmaybethatP. wallabiaeis bothoftheoccurrenceofparasitesintreekangaroos
morewidelydistributedinspeciesofDorcopsis,than as well as of host biology are needed before the
currently indicated bypublishedrecords, and infects various questions posed by thepresent studycan be
treekangarooswhich occurin sympatrywithvarious resolved.
species of scrub wallabies. However, the host and
geographical distributions of the species are too Acknowledgements
poorly understood to allowconclusionstobedrawn.
TheoccurrenceofP. wallabiaeintreekangaroosand Our thanks are due to Tim Flannery and Dave
scrub wallabies in New Guinea provides a striking Spratt for providing specimens forthe current paper
contrast with P. dendrolagi in Australia which is and to Dave Spratt forcommenting on adraft ofthe
apparently highly host specific and occurs only in manuscript. The work was supported financially by
tree kangaroos. theAustralian Biological Resources Study.