Records of the Western Australian Museum 22: 259-263 (2005).

The gastrointestinal nematodes of Varanus rosenbergi (Reptilia: Varanidae)and the effects of habitat change in southern Australia, with particular

reference to the genus Abbreviata (Physalopteroidea)

Hugh.1. JanesSchool of Biomedical and Chemical Sciences, Microbiology, M 502

The University of Western Australia, 35 Stirling Highway, Crawley, Western Australia 6009(email: hjones@cyllene.uwa.edu.au) ,

Abstract - Nine species of nematode were collected from the stomachs of 56Varanus rosenbergi from southern Australia, viz. Abbreviata anomala, A.antarctica, A. confusa, A. hastaspicula, A. levicauda, A. tumidocapitis,Pseudorictularia disparilis, Maxvachonia chabaudi, and Ophidascaris pyrrhus. A.antarctica occurred in 93% of lizards. Sixty-two percent of lizards wereinfected with this species only, and 30% had concurrent infections with fromtwo to five species of Abbreviata. A. levicauda and A. hastaspicula were presentat low prevalence in the drier and hotter parts of this host's range. Intensityof infection with Abbreviata nematodes ranged to more than 400 adults, andmore than 600 Abbreviata spp. larvae. Highest intensity of infection with A.antarctica in Western Australia was east of the agricultural areas, and in orclose to reserves where the ecosystemwas less disturbed. The high prevalenceof nematodes in this genus across a wide range of habitat and climate typessuggests a prevalent arthropod intermediate host, or a wide range of speciesof arthropod, which are susceptible to infection.

Key words: Varanus rosenbergi, Abbreviata nematodes, habitat change, Australia.

INTRODUCTIONVaranus rosenbergi Mertens, 1957 was recognised

as a subspecies of Varanus gouldii by Mertens (1957),and was elevated to species status by Storr (1980). Itis a large predatory diurnal monitor lizard whichoccurs in a wide range of habitats in southernAustralia south of latitude 30° S, principally inWestern Australia and South Australia, withisolated populations in Victoria and New SouthWales (Cogger 1992). Several studies have shownthat nematodes in the genus Abbreviata predominatein Varanus lizards in Australia, frequently reachinghigh intensity and prevalence in larger species(Jones 1983a, 1983b, 1985, 1988). Apart from V.varius in southern Victoria, V. rosenbergi occursfurther south than any other species of Varanus. Itsrange across a number of ecosystems in thissouthern distribution may throw light on factorswhich delimit the distribution of its parasites. Thepresent study was therefore undertaken todetermine which nematode species V. rosenbergisupported, their prevalence, intensity andgeographical range, and to examine the externalenvironmental factors which might influence theworms' occurrence in this host.

MATERIALS AND METHODSNematodes were recovered from 56 Varanus

rosenbergi preserved in the Western Australian

Museum (n: 48), the South Australian Museum (n:4), CSIRO Sustainable Ecosystems, Canberra (n: 3),and one in a private collection. Forty-eight lizardswere from Western Australia, seven from SouthAustralia (five of which were collected on KangarooIsland), and one from the Australian CapitalTerritory. This study includes findings from 7previously reported host specimens (Jones 1983a).All worms were cleaned, cleared inchlorolactophenol for examination, and stored in70% ethanol with 10% glycerine. Specimens havebeen deposited in the Western Australian Museum,South Australian Museum and CSIRO SustainableEcosystems, Canberra. Landsat images provided bythe Western Australian Department of LandInformation were used to compare nematodeoccurrence with surface vegetation cover, andmeteorological maps were consulted on the Bureauof Meteorology website (www.bom.gov.au).

RESULTSNematodes recovered. Nine species of nematode

were recovered: Abbreviata anomala, A. antarctica, A.conJusa, A. hastaspicula, A. levicauda, A. tumidocapitis,Pseudorictularia disparilis, (Spirurata:Physalopteridae), Maxvachonia chabaudi (Oxyurata:Cosmocercidae) and Ophidascaris pyrrhus(Ascaridida: Ascarididae).Prevalence and intensity (Table 1). The

DOI: 10.18195/issn.0312-3162.22(4).2005.259-263

260 H. I. Jones

Table 1 Adult nematodes recovered from 56 V. rosenbergi

Abbreviata anomalaAbbreviata antarcticaAbbreviata con/usaAbbreviata hastaspiculaAbbreviata levicaudaAbbreviata tumidocapitisPseudorictularia disparilisMaxvachonia chabaudiOphidascaris pyrrhus

No. of lizardsinfected

15229814111

prevalence

1.8%92.8%3.6%16.1%14.3%25.0%1.8%1.8%1.8%

intensity(mean, range and SD)

957 (1-341; 67.1)

6 (4-8)14 (10-19; 5.7)28 (1-68; 24.8)6.5 (1-73; 18.8)

112

predominant species was A. antarctica, which wasrecovered from 93% of lizards. It occurred in 46/48hosts from Western Australia, (the remaining twolizards having Abbreviata spp. larvae only), innumbers ranging from one to 341 per host; the onlytwo lizards without infection of either adult orlarval Abbreviata spp. were from mainland SouthAustralia and from Kangaroo Island. Sixty-onepercent also had larval or immature Abbreviata spp.in the stomach lumen, not referable to species, innumbers from 1-606. No larval cysts were seen inthe stomach or peritoneal tissues. A. tumidocapitisoccurred in 14 hosts, A. hastaspicula in nine hosts,and A. levicauda in eight hosts; these three specieswere present at lower mean intensity than A.antarctica. A. confusa was present in two hosts, andA. anomala, P. disparilis, M. chabaudi, and O. pyrrhuswere each recovered from one host.Concurrent infections (Table 2). Sixty-two percent

of lizards supported a single gastric nematodespecies, A. antarctica. Apart from one A. confusa, alleight other nematode species occurred concurrentlywith A. antarctica. Thirty percent supported two ormore species. Twelve out of fourteen A.tumidocapitis infections also occurred concurrentlywith A. hastaspicula and/or A. levicauda, and theywere usually present when other worms were athigh intensity. All nine infections with A.hastaspicula and all eight infections with A. levicaudaoccurred concurrently with one another, and/orwith A. tumidocapitis. Although there was nocorrelation between intensity of A. antarctica andintensity of infection with other species (p>O.l), themean intensity of adult A. antarctica was higherwhen there was concurrent infection with one tofour other species of Abbreviata (80.5 worms; SD101.3; N:14) than in single-species infections (37.2worms; SD 39.4; N:31; p = 0.028). The mean

35

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120

o

122

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KM 200

Figure 1 Number of concurrent species of Abbreviata occurring in Varanus rosenbergi in Western Australia. (L, larvalAbbreviata sp. only). The specimen east of the area of the map refers to a lizard at Eucla. The area north of thedotted line has an average annual precipitation of <400mm; the dashed line shows the February meanmaximum 24°C isotherm. (P: Perth, A: Albany, E, Esperance).

GastricnematodesofVaranusrosenbergi 261

Table2 NumberofspeciesofAbbreviatanematodeperhost

no.oflizards

237*3

1021

no.ofnematodespecies

o12345

~ latitude119°E,where ingeneralthevegetationwaslessdisturbed,Figure2.LizardsfromreservesinorwestoftheWheatbelt (CapeNaturalisteNP,StirlingRangeNP,LakeMagenta NR,PallarupandDunnRocksNRandDragonRocksNR)contained45-341worms perhost(N:6,mean 138).LizardscollectedfromaroundthecitiesofPerthandAlbany andfromtheintensivelyclearedareasoftheWheatbelt supportedlighterinfections,withfromoneto24wormsperhost(N:18,mean9.4).

*includestwolizardswithlarvalAbbreviatasp.only

numberofalladultAbbreviataspeciesinmixedinfectionswas109.6,(N:13).

Geographical distribution. Three speciesofAbbreviata,A. hastaspicula,A. levicaudaandA.tumidocapitis,werewithoneexceptionabsentfromtherelativelycoolerandmorehumidsouth-westofWestern Australia, occurringprincipallyinthenorthernpartsoftherangeofV. rosenbergi.A.levicaudaandA.hastaspiculaoccurredinland,inareaswithanaverageannualrainfalloflessthan400mm and a mean maximum Februarytemperatureinexcessof24°C,Figure1.A.tumidocapitishadasimilardistribution,althoughtherewerethreerecordsnearthesouthcoast.ThetwoA.confusarecordswerefromKangarooIsland,SouthAustralia, andnearQueanbean intheAustralianCapitalTerritory.

A.antarcticaoccurredthroughouttherangeofV.rosenbergi.Intensitywas significantlyhigherinlizardscollectedineasternWestern Australia,east

DISCUSSION

Varanusrosenbergisupportsaconsiderablegastricnematodefaunathroughoutitsgeographicalrange.Fourspeciesofnematodewererecoveredfromonehostonly,andthesewere probablyaccidentalinfectionsresultingfromingestionwith prey;Maxvachonia spp.(Oxyurata)occurintherectumofseveralspeciesofskinks,geckosandagamidlizards(Mawson1972),A.anomalaisfoundinagamidlizardsinthegenusPogona(Jones1986a),andO.pyrrhusinsnakes(Jones1980).P. disparilisisprobablyaparasiteofamphibians(OwensandMoorhouse 1980).AllothernematodeswereinthegenusAbbreviata.A. antarcticahasbeenrecordedfrommany speciesoflargerreptileineastern,southernandnorthernAustralia,butappearstobeabsentfromthehotterdrierinlandareasofthecontinent.Prevalenceandintensityaregreaterinthislizardthaninanyotherreptilehostsofarrecorded.Inthehotteranddrierinlandpartsof

32$

33

34

35

" I118 120,

"BE\\ !'I.,, "

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(ll.;j "

..( , ," ':0,\CP{ ".

,

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122

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Figure2 DistributionandintensityofAbbreviataantarcticainVaranusrosenbergiinWestern Australia. •1-20adultworms; • 21-100adultworms, • >100adultworms.L:larvalAbbreviataonly.Areasofmajorlandclearanceshaded(takenfromsatelliteimages).CF,SwanCoastalPlain,W, Wheatbelt, E.easternagriculturalarea.S,StirlingRangeNationalPark;M, LakeMagenta Nature Reserve;P,PallinupNature Reserve;D,DragonRocksNatureReserve.P,Perth,A,Albany,E,Esperance.

GastricnematodesofVaranusrosenhergi 26]

Table2 Numberofhost

no.oflizards

237'3lO

2

1

ofAbbreVlatanematodeper

no.ofnematodespecies

o1

2

345

oflatitude119°E,where ingeneralthevegetationwaslessdisturbed,Figure2.Lizardsfromreservesinorwest oftheWheatbelt (CapeNaturaliste NP,StirlingRangeNP,LakeMagenta NR,PallarupandDunnRocksNRandDragonRocksNR)contained45-341worms perhost(N:6,mean 138).LizardscollectedfromaroundthecitiesofPerth andAlbany andfromtheintensivelyclearedareasoftheWheatbelt supportedlighterinfections,withfromoneto24wormsperhost(N:18,mean9.4).

,includestwoliz.ardswithlarvalAbbreviatasp.only

numberofalladultAbbreviata speciesinmixedinfectionswas109.6,(N:13).

Geograplzical distribution. Three speciesofAbbreviata, A. Izastaspicllla,A. levicaudaandA.tumidocapitis,werewithoneexceptionabsentfromtherelativelycoolerandmorehumidsouth-westofWestern Australia, occurringprincipallyinthenorthernpartsoftherangeofV. rosenbergi.A.levicaudaandA. Izastaspiculaoccurredinland,inareaswith anaveragearmualrainfalloflessthan400mm and a mean maximum Februarytemperatureinexcessof24°C, Figure 1. A.

tumidocapitishadasimilardistribution,althoughtherewere threerecordsnearthesouthcoast.ThetwoA.confusarecordswerefromKangarooIsland,South Australia, andnearQueanbean intheAustralianCapitalTerritory.

A.antarcticaoccurredthroughouttherangeofV.rosenbergi.Intensitywas significantlyhigherinlizardscollectedineasternWestern Australia,east

E

DISCUSSION

Varanusrosenbergisupportsaconsiderablegastricnematodefaunathroughoutitsgeographicalrange.Fourspeciesofnematodewererecoveredfromonehostonly,andthesewere probablyaccidentalinfectionsresultingfromingestionwith prey;Maxvaclzonia spp.(Oxyurata)occurintherectumofseveralspeciesofskinks,geckosandagamidlizards(Mawson1972),A. anomalaisfoundinagamidlizardsinthegenusPogona (Jones1986a),andO.pyrrlzusinsnakes(Jones1980). P. disparilis isprobablyaparasiteofamphibians(OwensandMoorhouse 1980).AllothernematodeswereinthegenusAbbreviata. A. antarcticahasbeenrecordedfrommany speciesoflargerreptileineastern,southernandnorthernAustralia,butappearstobeabsentfromthehotterdrierinlandareasofthecontinent.Prevalenceandintensityaregreaterinthislizardthaninanyotherreptilehostsofarrecorded.Inthehotteranddrierinlandpartsof

s••

C'P

•

•

-•

•

p

(~-

•

,.......

•

•JI

..-

•~

•

•

Figure2 Distribution andintensityofAbbrcmataantarcticainVaranlls inWestern Australia. • 1-20adultworms; • 21-100adultworms, • >100adultworms. L: Abbreviataonly.Areas ofmajor landclearanceshaded(takenfromsatelliteimages).CP,SwanCoastal Plarn,W, Wheatbelt, E.easternagriculturalarea.S,Stirln,gRange National Park;M, Lake Magenta Nature Reserve; P, Pallinup Nature Reserve; D,

RocksNatureReserve.P,Perth,A,Albany,E,Es!x'ran(:e

,-----

262

Western Australia this species is replaced by A.hastaspicula and A. levicauda; the former attainhighest numbers in V. gouldii and V. panoptes northof the distribution of V. rosenbergi Gones, 1983a),whereas A. levicauda, although common in thesetwo host species, occurs predominantly in V. tristisGones 1986b). These two nematodes were thereforeonly recovered from the northern areas of the rangeof V. rosenbergi, in low numbers. A. tumidocapitis isusually found concurrently with infections of thesetwo species Gones 1983a). The two records of A.confusa were respectively from Kangaroo Island andfrom the isolated population of V. rosenbergi inNSW, near Queanbean. This worm has not beenreported from southern Western Australia, thoughit is found in several species of Varanus in thetropical north of this State Gones 1988).The intensity of A. antarctica infections within the

range of V. rosenbergi was not directly related eitherto mean precipitation or to temperature. Numberswere highest east of approximately 119°E, wherethe vegetation is less disturbed. The only records ofhigh intensity (43 to 329 adult worms) in theSouthwest were from, or close to, National Parks orReserves, suggesting that intensity is reduced byEuropean-induced habitat changes. Nature reservesoccupy only 2.4% of the wheatbelt (in 1978), and astudy of 23 of these reserves found V. gouldii (inwhich V. rosenbergi was included) in only five ofthese, of which the smallest with V. gouldii had anarea of 272 hectares (Kitchener et al., 1980).Relatively high numbers were recorded from nearthe towns of Hopetoun and Esperance, aroundwhich there has been extensive land clearance, butboth satellite images and direct observation (M.Tonts, pers. comm.) show that this easternagricultural area contains extensive pockets andstrips of residual uncleared land, which could act asrefugia for both the lizards and their nematodes'intermediate hosts. The observation that A.antarctica numbers were higher in concurrentinfections with congeneric species which were nearthe southern edge of their range than in single-species infections, indicates the complex interplayof climatic and environmental parameters affectingnematode survival and transmission. It is likelythat climate has an effect, perhaps indirectly, onsurvival of nematode eggs, as well as its effect onintermediate hosts. Several biological variables areunknown, including the specificity of thearthropod intermediate hosts required by A.antarctica, the prevalence of smaller lizardparatenic hosts, and the density and home rangesof V. rosenbergi in different habitats, which can behighly variable (King and Green 1999). V.rosenbergi has a varied diet; on Kangaroo Island,arthropods comprise about 35% of the diet byvolume, and the majority of vertebrate food isprobably obtained from road kills (King and Green

H. I. Jones

1999). The extent of land clearance in theagricultural areas, clearly shown on satelliteimages, the habitat perturbation around cities, andthe higher vehicle numbers on the roads all havean impact on the ecology of reptile hosts, andtherefore on the dynamics of their acquiringinfection. Studies on Abbreviata spp. in elapidsnakes in Western Australia and on O. pyrrhus andthe trematode Dolichoperoides macalpini in Notechisater near Hobart in Tasmania indicate that lowerprevalence or absence may be due to alteredenvironments in these urban areas (Jones 1978,2003). However, records are too sparse from someareas, and collection sites reported are in somecases not sufficiently precise to link habitat tonematode intensity with more confidence.The significantly higher mean intensity of A.

antarctica in the presence of concurrent infectionswith one to four congeneric species reflects the lownumbers of A. antarctica in the more disturbedecosystems in the Southwest, from which otherspecies are absent (apart from one anomalousrecord from Two Peoples Bay east of Albany). A.antarctica itself is absent from the drier and hotterareas further north, beyond the range of V.rosenbergi. The factors affecting the populationdynamics and interspecific relations of these speciesare not yet understood, but the observationsreported here suggest that intensity of A. antarcticainfection is not adversely affected by competitionfrom other species in this environment. The absenceofA. hastaspicula, A. levicauda and A. tumidocapitis inthe cooler and more humid areas may be aconsequence of the scarcity or absence of suitableintermediate hosts, or by the viability of eggs in theexternal environment.

CONCLUSIONSV. rosenbergi is heavily infected with species of

Abbreviata throughout its range in southernAustralia. All but two of the lizards examined wereinfected, and 26.8% were concurrently infected withthree or more species. These results add to previouswork in confirming the dominant position ofnematodes in the genus Abbreviata in the gastricfauna of varanid lizards in arid Australia. The highprevalence across a range of habitat types suggestseither that the arthropod intermediate hosts areequally widespread, or that they have a low host-specificity and that many species are involved.However, the lower intensity of A. antarctica inthose areas where there has been extensive clearingof natural vegetation suggests diminishedtransmission, and indicates that the nematodeparasites are affected by these profound changes tothe ecosystem. The patterns of infection in thislizard would be clarified by knowledge of thearthropod intermediate hosts.

Gastric nematodes of Varanus rosenbergi

ACKNOWLEDGEMENTSI thank the late Dr. Dennis King for his

collaboration in recovering the specimens, and BradMaryan for assisting with access to material in theWestern Australian Museum. Dr. Dave Spratt,CSIRO Sustainable Ecosystems, and the Curator ofReptiles at the South Australian Museum allowedme access to specimens in their care. Peter Sanders 'from the Western Australian Department of LandInformation kindly made satellite images availablefor my use.

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263

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Manuscript received 9 February 2004; accepted 7 September2004