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Volume 85, No 10, October 2007 © 2007 The AuthorsJournal compilation © 2007 Australian Veterinary Association

420

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Blackwell Publishing Asia

Distributions of the paralysis ticks

Ixodes cornuatus

and

Ixodes

holocyclus

in south-eastern Australia

J JACKSON,

a,b

I BEVERIDGE,

a

NB CHILTON

a,c

and RH ANDREWS

d

Objective

To describe the actual and potential geographicdistributions of

Ixodes cornuatus

and

I holocyclus

in south-eastern Australia.

Procedure

Examination of ticks from museum collections andtrapped animals were made. (Bioclimatic analysis BIOCLIM)was used to predict potential distributions.

Results

I holocyclus

was collected from rodents (

Rattusfuscipes

,

R lutreolus

,

R rattus

), wombats (

Vombatus ursinus

),cats and dogs in Gippsland and

I cornuatus

was collected fromrodents (

R fuscipes

), wombats, cats and dogs in central Victo-ria. All life-cycle stages of both species were collected duringthe warmer months of the year. The known distribution ofthe two species was established from specimens in museumcollections and suggested that a boundary between the twomay exist in eastern Gippsland. BIOCLIM suggested thatthe area immediately to the east of Melbourne was climaticallysuitable for

I holocyclus

, although no endemic foci of infectionare currently known from this region. The potential distributionof

I cornuatus

included east Gippsland and the Otway Ranges,areas in which the tick is not currently known to occur.

Conclusions

I holocyclus

and

I cornuatus

have morerestricted distributions than current collections suggest andtherefore may have the possibility to extend their geographicalranges in the future.

Key words:

paralysis tick,

Ixodes cornuatus

,

Ixodes holocyclus

,tick habitat

Aust Vet J

2007;85:420–424 doi: 10.1111/j.1751-0813.2007.00183.x

T

wo species of ixodid tick,

Ixodes cornuatus

and

I holocyclus

,are capable of causing paralysis in domestic animals inAustralia.

I cornuatus

occurs in Tasmania and in centralVictoria

1,3

where it occasionally causes paralysis in domesticanimals.

4,5

Differentiation of the adult females of the two species,the stages most commonly causing paralysis, is difficult and mayrequire multivariate statistical analyses.

6

By contrast, the identi-fication of males and larvae is relatively straightforward.

6

Thenymph of

I cornuatus

has not been described.

Both species of tick occur in Victoria, but the limits of theirdistribution and their host preferences have not been well defined.

I holocyclus

is thought to occur east of the Tambo River,

1

whereas

Icornuatus

is reported to occur in central and eastern Victoria, althoughrecent studies found no evidence of the species in east Gippsland.

7

While the biology of

I holocyclus

has been studied extensively inNew South Wales and Queensland,

8,9

there are no studies of itsbiology and host distribution in Victoria. Information on thebiology of

I cornuatus

is also extremely limited. In the presentstudy, the hosts and seasonal occurrence of the two species wereexamined in Victoria. In addition, their potential geographicaldistributions were examined using bioclimatic analyses.

Materials and methods

Tick collection

Ticks were obtained by trapping small mammals (

Rattus

spp,

Antechinus

spp) using Elliot traps (46

×

11

×

15 cm) baited withpeanut butter, rolled oats and honey. Principal trapping siteswere at Bullengarook (37

°

30

′

S 144

°

50

′

E), central Victoria, a siteat which

I cornuatus

is known to occur, and at Nowa Nowa,Buchan, Lakes Entrance and Orbost in east Gippsland (37

°

30–53

′

S 148

°

00–28

′

E), sites at which

I holocyclus

is common. At theBullengarook trapping sites, closed eucalypt forest was dominatedby

Eucalyptus obliqua

and

E radiata

with an understorey of

Leptospermum continentale

and forest edges of heath dominatedby

Acacia verniciflua

and

Epacris

spp. In east Gippsland, trappingsites varied from rocky ridges covered with bracken,

Pteridiumesculentum

, to eucalypt forests dominated by

E bauerana

,

Ebosistoana, E botryoides, E bridgesiana, E cypellocarpa, E globoidea,E sieberi and E tricarpa

, and swamps dominated by

Melaleucaericifolia

. Trapping was carried out for 5 consecutive nights everymonth for 2.5 years at Bullengarook and fortnightly in EastGippsland between October and March for 2 successive yearsbetween 1995 and 1997. Trapped mammals were either lightlyanaesthestised with isoflurane and ticks removed with fine forceps,or were held over trays filled with water and the ticks werecollected as they detached. Animals killed on roads at both sitesprovided a source of additional ticks for study. In addition,veterinary practitioners and members of the public in Victoriaand Tasmania provided ticks collected from domestic animalsand some wild animals.

Identification

Ticks were identified using newly defined morphologicalcriteria

6

as well as by multilocus enzyme electrophoresis (MEE).

7

a

Department of Veterinary Science, University of Melbourne, Veterinary Clinical Centre, Werribee VIC 3030; ibeve@unimelb.edu.au

b

Current address: 57 Davies Road, Walmer VIC 3463

c

Current address: Department of Biology, University of Saskatchewan, Saskatoon, Canada

d

University of South Australia, Adelaide SA 5000

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Volume 85, No 10, October 2007Journal compilation © 2007 Australian Veterinary Association

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Known geographical distribution

The geographical distribution of the two species was establishedby re-examining and identifying, using current criteria,

6

allspecimens in the collections of the Australian National InsectCollection (Canberra), The Museum of Victoria (Melbourne),the South Australian Museum (Adelaide), the Queen VictoriaMuseum (Launceston), the Australian Museum (Sydney)and the collections of the Veterinary Clinical Centre, Universityof Melbourne, Werribee. The distributions of the ticks weremapped.

Seasonal occurrence

The numbers of larvae, nymphs and adults obtained in eachmonth from all collection methods were tabulated. Becauseadult ticks are the primary agents of paralysis, an index of adulttick activity in each month of the year was determined using theproportion of adults collected in each month, compared with thetotal numbers of adults of each species, collected throughoutthe study, expressed as a percentage. The index obtained wasplotted against the month of the year.

Potential geographical distribution

The potential geographical distribution of the two species wasexamined using the computer program BIOCLIM.

10,11

BIOCLIMuses climatic parameters including temperature, rainfall, radiationand moisture indices of known occurrences of a species topredict the potential distribution of a species. Core areas arethose in which the climatic parameters fall within the 90thpercentile of the climate profile. Marginal areas are identifiedwhere one or more parameters fall outside the 90th percentile butare within the total range of values for the climate profile. Twenty-five bioclimatic parameters were used

12

(Table 1). The locationsof 114 specimens of

I holocyclus

and 63 specimens of

I cornuatus

from all eastern states, which had been identified using currentmorphological or MEE criteria

6,7

were used in the analysis(locations shown in Figure 1). Coordinates for the locality recordswere based upon the Register of Place Names in Victoria and the

Australian 1:250,000 Map Series Gazeteer, and altitudes wereestimated using the 1:100,000 or 1:250,000 map series.

Results

Trapping

From a total of 1804 trap nights at Bullengarook, 10 agileantechinuses (

Antechinus agilis

) 14 dusky antechinuses (

Aswainsonii

) and 80 bush rats (

Rattus fuscipes

) were examined forticks. Eight nymphs of

I cornuatus

were obtained from

Rattusfuscipes

while

A agilis

was parasitised by

I antechini

(1 male, 3females, 6 nymphs, 12 larvae). From 3160 trap nights in eastGippsland, 9

A agilis

, 15

A swainsonii

, 86

R fuscipes

, 14 swamprats (

R lutreolus

) and 9 black rats (

R rattus

) were examined forticks. Twenty-three larvae and 109 nymphs of

I holocyclus

wererecovered from

R fuscipes

,

R lutreolus

and

R rattus

. Other tickspresent on the rats were

I fecialis

(2 nymphs, 6 females),

I tasmani

(1 nymph) and

Haemaphysalis longicornis

(1 larva, 2 nymphs).

From animals killed on roads, 9 female specimens of

I cornuatus

were obtained from 12 common wombats (

Vombatus ursinus

) aswell as 1 specimen of

I holocyclus

. Other species of ticks encounteredwere

I tasmani

and

Aponomma auruginans

. No ticks were foundon 20 kangaroos and wallabies (

Macropus giganteus

,

Wallabiabicolor

). Ticks submitted for identification by veterinary practi-tioners included 82 larvae and 5 female

I cornuatus

from dogsand a cat, 147 female

I holocyclus

from dogs and 25 female

I holocyclus

from cats.

Geographical distribution

Localities from which

I cornuatus

were collected in Victoria were:Cape Patterson, Lucyvale, Bullengarook, Pakenham, Blackwood,Monbulk, Emerald, Silvan, Gisborne, Kinglake, Toolangi,Tonimbuk, Yarra Junction, Buchan, Alexandra, Leongatha,Walkerville, Yarra Glen, Armadale, Eildon, Healesville, Daylesford,Marysville, Porepunkah and Moe. Specimens were also identifiedfrom Captain’s Flat and Wee Jasper in New South Wales andfrom Canberra in the Australian Capital Territory (Figure 1).

Table 1. Climate parameters used in bioclimatic analysis of the potential distributions of Ixodes cornuatus and I holocyclus in south-eastern Australia usingBIOCLIM.

Precipitation Temperature Moisture index

mean annual precipitation mean annual temperature mean annual moisture index

mean precipitation of wettest month mean diurnal temperature range highest mean monthly moisture index

mean precipitation of driest month maximum temperature of warmest month lowest mean monthly moisture index

precipitation seasonality (coefficient of variation) minimum temperature of coolest month moisture seasonality index (coefficient of variation)

mean precipitation of wettest quarter annual temperature range mean moisture index of wettest quarter

mean precipitation of driest quarter mean temperature of wettest quarter mean moisture index of driest quarter

mean precipitation of warmest quarter mean temperature of driest quarter mean moisture index of warmest quarter

mean precipitation of coldest quarter mean temperature of warmest quarter mean moisture index of coldest quarter

mean temperature of coolest quarter

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Virtually all specimens of

I holocyclus

were collected within theknown geographic limits of the species, subcoastal areas of eastGippsland (Figure 1). Extralimital specimens, collected beyondthe currently accepted boundary of the Tambo River, were fromdogs or cats in Moonee Ponds, Laverton, Cheltenham, Eltham,Doncaster, Wonga Park and Rye, all suburbs of Melbourne, andfrom Walwa, the Bellarine Peninsula and Maryborough. Specimenswere also collected from a wombat at Cape Patterson (Figure 1).

Seasonal occurrence

Using tick collections from all three sources including data fromTasmania, females of

I cornuatus

were found between October

and June, with peak occurrences between January and March(Figure 2), nymphs between July and December and larvae inMarch. Females of

I holocyclus

were collected between Augustand May, with peaks in August–September and February–March(Figure 2), nymphs were collected in all months with peaks inDecember, whereas larvae were collected between Decemberand March.

Bioclimatic analysis

The predicted core range of

I cornuatus

included easternTasmania, eastern Victoria, the Great Dividing Range east,north and west of Melbourne, the Otway Ranges south-west ofMelbourne and parts of the southern tablelands of New SouthWales (Figure 3). The predicted core range of

I holocyclus

wasto the east of Melbourne, and included coastal east Gippsland andextended along the New South Wales and Queensland coasts tothe latitude of Maryborough. Isolated occurrences were predictedin northern Queensland (Figure 4). Areas where the range ofthe two species was predicted to overlap were the areas immediatelyto the east of Melbourne and in coastal east Gippsland.

Discussion

Trapping of small mammals showed that rodents (

R fuscipes

,

Rlutreolus

and

R rattus

) could act as hosts for the larvae and nymphsof both

I cornuatus

and

I holocyclus

in Victoria.

I holocyclus

hasbeen reported occasionally from rodents,

3

but in this studyrodents appeared to be significant hosts in the life historiesof both species of ticks. Neither tick species was found onany of the antechinuses trapped, but the role of possums, koalasand bandicoots as potential hosts cannot be excluded asinsufficient numbers of these species were available for exam-ination.

I holocyclus

is known to occur on common brushtailpossums (

Trichosurus vulpecula

) and the mountain brushtailpossum (T caninus)9 whereas I cornuatus has been found on Tvulpecula in Tasmania.13 Both species of tick have been collectedfrom koalas.3 Neither tick species was found on any of theexamined carcases of kangaroos or wallabies killed on the roads,although both species of ticks have been collected previouslyon macropodids.3 It is possible that, in this study, ticks mayhave detached from carcases before examination. Females of

Figure 1. Distribution of Ixodes cornuatus and I holocyclus in south-eastern Australia based on museum specimens reclassified using currentmorphological criteria or new collections using allozyme (MEE) and morpho-logical criteria. Single points may represent more than one collection.Circles represent collections of I cornuatus; triangles represent collectionsof I holocyclus; squares represent collections of I holocyclus beyond theknown gepgraphical range for this species.

Figure 2. Index of activity of female Ixodes cornuatus and I holocyclus inVictoria and Tasmania from 1995 to 1997 as indicated by the proportion (%)of female ticks obtained from all collection sources. Solid circles: Ixodesholocyclus; open squares: Ixodes cornuatus.

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both species of ticks were found on wombats. Bandicoots area common host of I holocyclus in New South Wales andQueensland,3 but there are no published data on the occurrenceof these ticks on bandicoots in Victoria. The data presented arefragmentary, but suggest that rodent hosts may be significant inthe life cycle of paralysis ticks in Victoria.

The seasonal occurrence of the ticks as indicated by the collectiondata presented here suggests that the ticks are most frequentlyencountered in the warmer months of the year, as documented inNew South Wales and Queensland.8,9 In the case of I holocyclus,the occurrence of females, the principal stage causing paralysis,was bimodal, with peak numbers occurring between Septemberand December and again in March. By contrast, I cornuatusfemales were found between December and February in eachyear of the study.

Distributions based on collections of ticks identified using currentmorphological and MEE methods indicated that I holocyclus wasessentially restricted to coastal east Gippsland whereas I cornuatusoccurred in the Great Dividing Range east, north, north-east andnorth-west of Melbourne, in south Gippsland and as far east

as Buchan. The latter species was also represented by a fewspecimens from southern New South Wales and the AustralianCapital Territory. Although there are obvious limitations toinferring distributions of animals based on museum collections,there was limited overlap in the distributions of the two species,with the approximate division between their ranges being theTambo River in southern Australia. One specimen of I cornuatuswas recorded from Buchan, just east of the Tambo River, and onespecimen of I holocyclus was found at Bairnsdale, just west of theTambo River although clinical cases of paralysis are not normally

Figure 3. Distribution of Ixodes cornuatus in eastern Australia predictedby BIOCLIM. Black areas represent core habitat; grey areas representmarginal habitat.

Figure 4. Distribution of Ixodes holocyclus in eastern Australia predictedby BIOCLIM. Black areas represent core habitat; grey areas represent mar-ginal habitat.

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seen in this area. In addition, a specimen of I holocyclus was foundon a wombat at Cape Patterson, well to the west of the TamboRiver. The region of the Tambo River therefore approximates theboundary between the two species, but intensive collections inthe area would be required to establish the precise distributionsof the two species of tick.

The distribution predicted by bioclimatic indices included theknown distributions of the two species of tick although the lackof museum specimens from central and northern Queenslandmay have impaired the predictions of potential distributionsin these regions. However, there were significant differencesbetween predicted and known distributions. Predictions for thedistribution of I cornuatus included the Otway Ranges andcoastal east Gippsland in Victoria. The few ticks that have beencollected in the Otway Ranges prevents conclusions being drawnon the likely occurrence of I cornuatus in this region, whereasextensive collecting in coastal east Gippsland has failed to reveal anyspecimens of I cornuatus.6,7 Similarly, the predicted distributionof I holocyclus includes the area immediately to the east ofMelbourne, which has not previously been considered an endemicarea for the tick. The single specimen of I holocyclus recoveredfrom a wombat at Cape Patterson,7 well to the west of theaccepted distribution of the species, is of particular interest inthis regard. Other so-called extralimital occurrences are invariablyassociated with domestic pets and there may have been movementof animals or owners into endemic areas, although it hasnot always been possible to establish relevant movements.2 Suchexplanations do not account for the finding of I holocyclus on awombat at Cape Patterson and it may be that small populations ofthe tick exist well to the west of its recognised geographical range.

The apparent discrepancies between known and predicteddistributions suggest the existence of geographical barriers, aconsideration not included in bioclimatic analyses. The resultsalso suggest that a barrier may have limited the extension of Icornuatus into climatically suitable zones in coastal east Gippsland,while the same hypothesis may explain the relative absence ofI holocyclus from the suitable climatic zone to the north and eastof Melbourne. The precise nature of the geographical barrierremains speculative, however, the collection of both I cornuatusand I holocyclus on a single wombat from Cape Patterson indicatethat the two species can occur in sympathy.

The apparent climatic suitability of the area surroundingMelbourne for I holocyclus suggests that, were introductions to

be made to this area, the tick species may be able to persist.Introductions appear to occur either through movements ofdogs or their owners,2,7 but there is little evidence to date of thepersistence of the tick in this climatically suitable area. It ispossible however, that I holocyclus could become established inthe outer Melbourne metropolitan area and could persist on suitablenative mammals present in these areas.

AcknowledgmentsWe wish to thank John Ward, Maisie Byrne, John Appleby, FredAlbrecht, the Catron family, Katrina Florence, Val York, TimHutton, Terri Larkin, Bill and Barbara Callow, Anthea Rooney,Judy Barnes, Hanya Stoward, Jeff Parsons and Sue Woinarski forassistance in collecting ticks and Dave Spratt for comments on adraft of this manuscript.

References1. Arundel JH, Sutherland AK. Ectoparasitic diseases of sheep, cattle, goats andhorses. Animal Health in Australia. Vol. 10. Australian Government PublishingService, Canberra, 1988:1–178.2. Beveridge I. Ixodes holocyclus in the Melbourne metropolitan area. AustVet J 1991;68:214.3. Roberts FHS. Australian Ticks. CSIRO, Melbourne, 1970:1–267.4. Mason RW, Kemp DH, King SJ. Ixodes cornuatus and tick paralysis. Aust VetJ 1974:50:580.5. Beveridge I, Coleman G, Gartrell W, Hitchman A, Whitnall V. Tick paralysis indogs in Victoria due to I cornuatus. Aust Vet J 2004;82:642–643.6. Jackson J, Beveridge I, Chilton NB, Andrews RH, Dixon B. Morphological com-parison of the adult and larval stages of the Australian ticks Ixodes holocyclusNeumann, 1899 and I cornuatus Roberts, 1960 (Acari: Ixodoidea). Syst ApplAcarol 2002;7:91–108.7. Jackson J, Chilton NB, Beveridge I, Morris M, Andrews RH. Genetic variationwithin the ticks Ixodes holocyclus and Ixodes cornuatus from south easternAustralia. Int J Parasitol 2000;30:1159–1166.8. Clunies-Ross I. The bionomics of Ixodes holocyclus Neumann, with aredescription of the adult and nymphal stages and a description of the larva.Parasitology 1924;16:356–381.9. Doube BM. Seasonal patterns of abundance and host relationships of theAustralian paralysis tick, Ixodes holocyclus Neumann (Acarina: Ixodidae), insoutheastern Queensland. Aust J Ecol 1974;4:345–360.10. Busby JR. Bioclimatic prediction system (BIOCLIM), User’s manual Version2.0. Bureau of Flora and Fauna, Canberra, 1986.11. Hutchinson MF, Houlder D, Nix HA, McMahon JP. ANUCLIM Version 1.5.Publication of the Centre for Resource and Environmental Studies. The AustralianNational University, Canberra.12. Jackson J. A comparison of the paralysis ticks Ixodes holocyclus and Icornuatus (Acari: Ixodidae) in southeastern Australia. PhD Thesis, Universityof Melbourne, 1999.13. Viggers KL, Spratt DM. The parasites recorded from Trichosurus species(Marsupialia: Phalangeridae). Wildl Res 1995;22:311–332.

(Accepted for publication 30 September 2006)

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