A new species of Dero (Allodero) (Naididae: Oligochaeta) inhabiting the Wolffian ducts of the green tree frog (Litoria caerulea) in Queensland

6 Pages·1998·2 MB·English

by  Adrian M Finder

A NEW SPECIES OF DERO{ALLODERO) (NAIDIDAE: OLIGOCHAETA)
INHABITING THE WOLFFIAN DUCTS OF THE GREEN TREE FROG
(LITORIA CAERULEA) IN QUEENSLAND
ADRIANM. FINDER, BRUCE D. HILLANDPETERE. GREEN
Pinder, A.M., Hill, B.D. & Green, P.E. 1998 06 29: A new species ofDero (Allodero)
(Naididae; Oligochaeta) inhabiting the Wolffian Ducts ofthe Green Tree Frog (Litoria
caerulea) in Queensland. Memoirs ofthe QueenslandMuseum 42(2): 559-564. Brisbane
ISSN 0079-8835.
A new species ofnaidid oligochaete, Dero (Allodero) litoria^ inhabiting the ureters ofthe
Green Tree Frog (Litoria caerulea), is described from Queensland. This is the firstrecord
ofthis subgenusfrom Australia. Thenewspecies is most similartoAlloderohylae (Good-
child, 1951) ofSE USA, from which it is distinguished by havinggills within a branchial
fossa and mid-segmental dorsal ridges which extend around to the ventral setae. Oligo-
chaeta, Naididae, newspecies, amphibia, commensalism, Queensland, Australia.
AdrianM.Pinder, WesternAustraliaMuseum,FrancisStreet, Perth600J. WesternAustralia
(presentaddress, Wildlife Research Centre, Department ofConservation andLandMan-
agement, P.O Box 51, Wanneroo 6065, Western Australia); Bruce D. Hill, Department of
PrimaryIndustries. Rockhampton VeterinaryLaboratory,Box6014, RockhamptonMailCentre
4702, Queensland; PeterE. Green, Department ofPrimary Industries, AnimalResearch
Institute. LockedMailBagNo. 4, Moorooka4105, Queensland, Australia; 28Jidy, 1997.
Dero Oken, 1815 (Naididae) is diagnosed by a Theother29speciesrecordedinAustralia(Pinder
fossa (cavity) around the anus, which usually & Brinkhurst, 1994)alsooccurinothercontinents.
containsgillfilaments.Threesubgenera,/4w/g'/?/;o- Discovery ofthe new species ofAllodero was
rus.DeromdAlloderome:usuallyrecognised.The an incidental finding made during dissection of
firsttwo are very similar: both have ventral setae Green Tree Frogs (Litoria caeridea). The frogs
that are longer and thinner on anterior segments hadbeensubmittedtotheRockhamptonVeterinary
than onposteriorsegments, afull complementof Laboratorybyafarmerwhowishedtoknowwhy
dorsalsetae,awelldevelopedbranchialfossaand so many ofthis species were found in poor con-
gills and all species are free-living. They differ dition in her locality. All worm specimens have
from each other only in that Dero lacks the pair been deposited with the Queensland Museum
ofelongatepalps foundontheposteriorborderof (QM).
the Aulophorus fossa. By contrast, Allodero is Veiy few oligochaeteshavetakentoasymbiotic
mostly endocommensal in frogs, have all ventral lifestyle compared to the other major clitellate
setaesimilarand(especiallyincommensal speci- group, the leeches. Gelder(1980) reviewed sym-
mens) the dorsal setae and branchial organs are biotic relationships between 13 species of
often reduced orabsent. Enchytraeidae, Naididae and Haplotaxidae and
There are seven species in Allodero. Five of their hosts (worms, molluscs, crustaceans and
these,/I. (Stephenson, 1930),^. hy- fish). Inaddition,threePhreodrilidaeofthegenus
lae (Goodchild, 1951), A. liUzi (Michaelsen, Astacopsidrilus have been found to be ectocom-
1926a),A.floridana Harman, 1971, and the new mensal on Euastacus crayfish in Australia(God-
species, are known to be endocommensal in dard, 1909; Brinkhurst, 1991; Pinder &
frogs, although at leastone(A. lutzi)canexistin Brinkhurst, 1997). Most relationships appear to
afree-livingstate. Asixth,yt. wa/at'a«a(Stephen- involve ectocommensalism, with endocommen-
son, 1931) hassofaronlybeen foundfree-living. salism and endoparasitism restricted to Allodero
The new species described in this paper is the andanothernaididChaetogasterlimnaeivon Baer,
firstrecordofthesubgenusinAustralia,although 1827 (Gelder, 1980). The cosmopolitan C. lim-
the othertwo subgenerahave been recorded pre- naeiis endo-orectocommensal,oreven parasitic
&
viously (Brinkhurst 1971; Pinder Brinkhurst, (depending on the subspecies) on molluscs. In
1994). It is only the second species ofNaididae to Australia, ithas been foundto inhabitthe pulmo-
berecordedonlyfrom Australia, theotherbeing nary chamber and body surface of several lym-
&
a species ofSlavinaPinder Brinkhurst, 1998). naeidand planorbidgastropods(Davies, 1913).
560 MEMOIRS OFTHEQUEENSLAND MUSEUM
MATERIALS AND METHODS
without setae and not clearly segmented while
Between Feb., 1996 and Jan., 1997 the farmer analendsofotherspecimensterminatingabruptly
submittedatotal of52 Green Tree Frogs (27 6S and obviously incomplete, but with intact (or
cafoonrldlte2hc5etier?da9papn)adtroettnhhteeilfllarbheoeqraulaettnhoc.ryyTthooefetsnhtuaemblbsiuesbrhmaiosfrsefiarosonogsns fearrlaamtgoimsoetnntinaattnaidcotn)p.boosBsduiydbdlwiaylnlga,seinnxodutiacleavtiridenepgnrtro.edcuAecnttririoennggebnoy-f
was determined only bythe time availabletothe thickenedbodywalloccurringtowardstheposte-
farmer. Soon after collection they were brought rior of each segment (Fig, IC), creating a ring
to the laboratory, sacrificed by pithing and then level with the setae. This is most noticeable dor-
dissected to remove various internal organs for sally(Fig. 1A)andatthe ventral setal bundles, so
examination. The kidneys and Wolffian ducts that the dorsal setae occur on a ridge and the
were dissected free and placed in a petri dish ventral setae appear to protrude from papillae,
containing phosphate buffered saline (pH 7.1). and is least developed ventrally. This ring is cre-
Using adissecting microscope, fine scissors and ated by enlargement and bunching up ofthe epi-
forceps the Wolffian ducts were opened along dermal cells (Fig. 1C).
theirlength.Oligochaeteswereremovedandplaced Alimentarycanaldifficulttomakeoutandpos-
in 70% alcohol. Tissues intended for histological sibly not continuous in some specimens. Gener-
examination were fixed in 10% buffered neutral ally, a thin walled buccal canal (Fig. lA) leads
formalin, embedded in paraffin and stained with from mouthtoathickenedpharynx in III and IV,
haematoxylin andeosin usingroutinemethods. withmuscularattachmentstodorsalbodywallof
moAulnctoehdolin pCrMeCsPer-v1e0d osrpsetcaiimneednsinwGererneacehietrh’esr VIII.(FPihga.r1yAn)g.eaLlugmleanndintigsustuevperreysnenatrrinowII(IFtiog,IVlAo)r
BoraxCarmine,thencleared in methyl salicylate or not visible. No gut contents visible. In one
and mounted in Permount. specimen, which has aprostomium and brain, so
figTuhrees.foAlUloowdienrgoabIbntrzevv.iabt=ibornasina,rebfu=sberdanicnhitahle tisoobtehnerowmisoeutdhe,vebluoccpaeldcaanvtietryioarlnyd,pthhaerryenaxp.pPeoasr-s
fossa,bu=buccalcanal,c=coelomocytes,cu=cuticle, terior gut often difficult to trace but (in fully
cg=chlorogogen tissue, e=epidermis/epidermai regeneratedspecimens)dorsalanuspresentonthe
cell,g=gill, i=intestine,m=mouth,mu=bodywall last segment. Gut and dorsal blood vessel sur-
muscle, n=nerve cord, p^phaiymx, pg=pharyn- rounded by masses ofbrown chlorogogen tissue
geal gland tissue, rm=retractor muscles. Litoria from VI onwards (Figs lA, 3), which often fills
the entire coeiomic cavity of some segments.
caerula: le=lumenal epithelium ofwoIffian duct,
kp=kidney parenchyma. Chlorogogen cells elongate tear-drop shaped,
arisingfromthewall ofthe intestine, with alarge
SYSTEMATICS deeply staining nucleus and coarsely granular
cytoplasm. Sub-spherical coelomocytes present,
Phylum ANNELIDA with cytoplasm moretransparentthan that ofthe
Class OLIGOCHAETA chlorogogencells. Coelomocytes(Fig. IA)either
FamilyNAIDIDAE free or lying adjacent tothe chlorogogen orbody
Dero Oken, 1815 wall, varying in density from sparseto fillingthe
Dero (Allodero) litoria sp. nov. coelom between the body wail and chlorogogen.
(Figs 1-4) Some specimens with a branchial fossa, varying
MATERIAL. HOLOTYPI:;QMG213863. Immatureon in development from barely apparent to an obvi-
slide, found on Green Tree Frog (Litoria caerula) ouschamber. Intwospecimensthefossacontains
collectedonfarmland.MtLarcom,23.87°S !50.91°E, two pairs of short, rounded, knob-like gill fila-
central Queensland, between ii.i996 and i.l997, coll. ments,notprotrudingfromthefossa(Fig. 1B). The
H.A. Luckey. PARATYPES: QMG2i3864 - 213869, gutandbranchialfossaappeartobemostdeveloped
213871 -213874and213877(l 1 slidemountedimma- when thedorsalsetaearealsomostnumerous.
atQsuMrfGeos2r)1;h3oi81o76t0yp,ael.2c1o3h8o7l5sapnedc2i1m3e8n7s6.(Cionlltehcrteieonvdieatlasi)l,s peBribfuinddvleentarnatlersioertlaye,fursoumalIlIy(3Fiogr.42,Ar-aCre)l,y42toor65
per bundle posteriorly, most 72.5-92.5pm long
DESCRIPTION. Dimensions (preserved and slide with aslightlydistal nodulus. SetaeofII-VI (Fig.
mounted) 3.2mmx 170pm (49 segments) to 2A,B) not especially longer and thinner than
6.2mm x350pm (79 segments). Colour reddish- those in following segments (Fig. 2C), although
brown when alive. Anal end ofsome specimens the most posterior setae often slightly shorter
NEW SPECIES OFDERO(ALLODERO) 561
FIG. l.Alloderolitoriasp. nov. A,anteriorsevensegments,basedonparatypeG213865withdetailsfromother
specimens; B, posterior end ofholotype showing three ofthe four gills, the fourth is obscured by the dorsal
wall ofthe fossa; C, section ofdorsal body wall ofparatypeG213867showingridgecreatedbyenlarged and
bunched epithelial cells. Scales: A=100pm, B^SOpm, C=20pm.
(62.5-70pm) and the nodulus slightly more distal small intermediate tooth (Fig. 2D, E). One short
anteriorly.DorsalsetaefromIV,oftenabsentinsome hair(95pm long)presentinonebundleofasingle
segmentsorabsententirelyinsomespecimens. Each specimen, accompanied by 2 needles (Fig. 2F).
bundle with 1 or2 needles (55-73pm long) with a Worms found within the ureters of Litoria
distal nodulus, bifid tips with short curved outer caerulea(Figs 3, 4).
teeth,thelowertoothmuchthickerandsomewhat DISTRIBUTION. Allodero is circum-tropical
longer than the upper, often with a third very (Africa, SEAsia, Central andSouthAmericaand
562 MEMOIRS OFTHEQUEENSLAND MUSEUM
Goodchild (1951) show these to be similartothe
ridges of^. litoria, except that those o^A. hylae
do not extend to the ventral setae according to
Goodchild(1951). Anothersignificantdifference
betweenA. hylae and the new species is that the
A. hylae specimens observed by Goodchild
(1951) and Harman & Lawler (1975) had only a
rudimentaryfossa(wherepresentatall)andnone
had gills. It is possible that A. hylae would de-
velopgills inafree-livingstate,butnospecimens
ofthisspecieshaveeverbeen foundoutsideofthe
frog hosts, despite a search in ponds frequented
bythe frogs (Harman & Lawler, 1975). llieonly
other Allodero known to have gills within the
branchialfossa\sA.lutziofSouthAmericawhich
has four pairs, as opposed to the two pairs ofA,
litoria. In A. lutzi, the gills are lost when the
worms are within the frogs. Neither gills nor
papillae have been reported for the remaining
threespecies(A.bauchiensis,A.floridianaandA
.
malay^ana). Only a few specimens of the new
FIG. 2. Allodero litoria sp. nov. A, ventral setaofIII; species had fossa and gills which may indicate
B, ventral seta of V; C, ventral seta of a posterior theyhad beenwithinthefrogsforashorterperiod.
segment; D, dorsal needle with bifid tip; E, tip of
dorsal needle with intermediate tooth; F, hair and The apparently incomplete alimentary canal of
needle setae ofXVI ofparatype G213864. Scale = many/I.litoriaspecimenshasalsobeennotedfor
20|im. all other commensal species ofAllodero, includ-
SE North America). The new species from Mt ing/1. hylae (Goodchild, 1951), A. bauchiensis
Larcom (23.87°S 150.91°E) fitsthis pattern. Full (Stephenson, 1930), Brazilian specimens of A.
distribution of the species in Australia has not lutzi(Michaelsen, 1926b)andA.floridiana(Har-
dbiesetnridbeutteerdmiinneNd.anTdheEfAruosgtrhaolsita.spHeocsitesfriosgwsiwdeerley minagne,st1f9o7o1d)w.hiTlheisinsduigegfersotgshtoshtast,tahlethwoourghmsStdepohenno-t
found several hundred metres from the nearest son (1930)suggested that/I. bauchiensisabsorbed
secretions ofthe frogs lachrymal gland through
water(farm dams).
ETYMOLOGY. Forthefroghost. gitoscbhaoedtyewaaslslo.ciGaetlidoenrs,(1d9i8s0c)u,ssiendawrheavtieiswkonfoowlin-
REMARKS. The presence ofa gilled branchial ofAllodero feedingbiology, but did not mention
fossa places the new species in Dero, while the the chlorogogue tissue surrounding the intestine
endocommensal habit, uniform ventral setae and that is particularly abundant in many Allodero,
a tendency to lose the dorsal setae and fossa comparedtootherDeroand otherNaididae. This
indicatesitsplacement inthesubgenusAllodero. tissue, which often fills the coelomic cavity of
The new species is most similar to A. hylae, Allodero, is known to be involved in storage and
which inhabits the ureters ofvarious species of metabolism of glycogen and lipids (Jamieson,
Hyia (Hylidae) in SE USA (Harman & Lawler, 1981). The worms may use the chlorogogue tis-
1975).Thesetaeofy4. hylaeareofsimilarsizeand sue to build up an energy store while feeding
formtothoseofv4. litoria^ exceptthattheneedles outside oftheir hosts: the gut then degenerating
ofthe former are usually one per bundle (one or whentheworms are inhabitingthe frogs. At least
two in A. litoria) and do not have intermediate onespecies,/!, lutzi, is known tooccuroutsideof
teeth. Intermediate teeth are otherwise known its froghosts, in aquatic habitats, where it devel-
only from A. floridiana but in that species they ops gills and dorsal hairs and presumably then
are much more pronounced (Harman, 1971). feeds inthenormalway. Howandwhentheworms
However,thepresenceorabsenceofintermediate find and enter new hosts is not known. Non-
teethon bifid setae isconsideredapoorcharacter commensal Dero are all aquatic and frogs may be
for species separation in Dero and other naidids infectedwhen inwater,whichtheyentertolayeggs.
(Grimm, 1987). A. hylae also has papillae at the Thefrogs,whichweresubjectivelyjudgedbythe
position ofthedorsalsetaeandthe illustrationsof farmer to be thin compared to the general popula-
NEW SPECIES OFDERO{ALLODERO) 563
most severe forms associated with the presence
of Myxidhm trophozoites in the hepatic ducts
(Hilletal., 1997).Theliversofthe 12frogswhich
harboured oligochaetes in their Wolffian ducts
werenormal infourfrogswhiletheremainderhad
hepatitis ofvaryingseverity.
Apart from possible partial obstruction ofthe
Wolffian ducts this new species ofAllodero ap-
pearstohavenoadverseeffectonthehost. Inthis
respect it is similar to the other endosymbiont
oligochaetes,.4. /w/z/(Michaelsen, 1926a)and/I.
hylae (Goodchild, 1951), described in the Wolf-
fian ducts ofthe amphibian genus Hyla. Follow-
&
ingthediscoveryby Markiw Wolf(1983)that
Myxosoma cerebralis, the agent of salmonid
whirlingdisease, required atubificidworm in its
life cycle, Delvinquier (1986) speculated that
Myxidium in amphibiansmayalsorequireasimi-
lar intermediate host. Whether any relationship
exists between the new species of oligochaete
described here and the Myxidium described by
Hill et al. (1997) is presently unknown but is
under investigation.
ACKNOWLEDGEMENTS
Facilities at the Western Australian Museum
andthe Dept ofConservationand LandManage-
ment were kindly made available to Adrian Fin-
derbyDianaJonesandStuartHalserespectively.
Wethank MrsH.A. Leukeforbringingthefrogs,
and hence the worms, to ourattention.
FIG.3. CrosssectionthroughL caerulaWolffianduct
withenclosedspecimenofA. litoriasp. nov. LITERATURECITED
BRINKHURST, RO. 1971. The aquatic Oligochaeta
tion, had a mean body length (SVL) of 8.0cm, known from Australia, New Zealand, Tasmania,
ranging from 6.5 to 10cm. The new species of and the adjacent islands. University ofQueens-
Allodero was foundassociatedwith slightto mod- landPapers3: 99-128.
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frogs. The number of worms removed from the (Annelida, Oligochaeta), with a description ofa
ductsofeach frogisasfollows(withthenumberof 2n0e3w1-s2p0e4ci0e.s. Canadian Journal ofZoology 69:
frogs in parentheses): 1(1), 2(2), 3(2), 5(1), 6(1), DAVIES, O.B. 1913. On two new species of Chae-
10(1), 11(1), 12(1), 15(1), and 23(1). The cloacas togaster. Proceedings of the Royal Society of
were not examined. ^^^iIe the ducts were being Victoria(N.S.)26: 88-98.
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tivelymovetotheproximalportionsadjacenttothe (Protozoa: Myxosporea) ofthe cane Toad, Bufo
kidneys. The worms appearedtobeapproximately marinus, in AustralianAnura,withaSynopsisof
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564 MEMOIRS OFTHEQUEENSLAND MUSEUM
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