echinococcus granulosus in northern queensland : 2. ecological determinants of infection in beef...

Australian Veterinary Journal

Volume 84, No 9, September 2006 © 2006 The AuthorsJournal compilation © 2006 Australian Veterinary Association

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Blackwell Publishing, Ltd.

Echinococcus granulosus

in northern Queensland. 2. Ecological determinants of infection in beef cattle

DJD BANKS,

a

DB COPEMAN

a

and LF SKERRATT

b

Objective

To provide information on possible ecologicaldeterminants of infection with


in abeef pastoral area of northern Queensland.

Procedure

An ecological study was carried out on the preval-ence and viability of infection with


indefinitive and potential intermediate hosts, and their predatorprey relationships.

Seven adjacent extensive beef properties 100 km south ofTownsville, that included areas of savannah, open woodlandand dense closed scrub, were selected for the study. Infectionwith

E granulosus

in dingoes was determined at post mortem,and in domestic dogs by examining duodenal mucus afterpurging with arecoline hydrobromide. Cattle, wild pigs andmacropods were examined at post mortem for viable hydatidcysts. The diet of dingoes was investigated by identifying thehair of prey species found in their stomach and colon, and thatof domestic dogs by questioning their owners.

Results

Prevalence of hydatidosis in adult cattle ranged from41% in animals from properties with large areas of dense closedscrub, to 3% on properties with little or no scrub. Hydatid cystswere found in 21.8% of black-striped wallabies (

Macropusdorsalis

), 9.4% of feral pigs, 1.5% of wallaroos (

Macropusrobustus

), and 1.4% of eastern grey kangaroos (

Macropus gigan-teus

). No rufous rat kangaroos (

Aepyprymnus rufescens

) orswamp wallabies (

Wallabia bicolor

) were infected. Most cystsin macropods were viable, whereas in pigs about half wereviable and in cattle only 0.7% contained viable protoscoleces.Infection with

E granulosus

was detected in 76% of dingoes,whereas no infection was detected in domestic dogs in thestudy area.

Conclusions

It was concluded that the sylvatic cycle of

E granulosus

in the study area was maintained mainly throughpredation of black-striped wallabies by dingoes, and that theverges of dense scrub were the main nidus of infection.

Aust Vet J

2006;84:308–311

T

he adult and larval stages of the hydatid tapeworm


have been reported in a widerange of domestic, feral and wild mammals.

1

Cycles ofthis parasite between domestic dogs and various species oflivestock have been well documented, but less attention has beengiven to the so-called sylvatic cycles among wild or feral animals.This is unfortunate, because they may be of lesser importance asa source of human infection but may make a major contributionto the prevalence in domestic animals, and are generallyintractable to conventional methods of control. For example,cattle in northern Queensland may have high prevalence ofinfection but are not important in maintaining the life-cycle.and infection relies on a sylvatic cycle.

2

In Australia only the sheep/G1 strain of


is known to occur.

1

A sylvatic cycle between dingoes and speciesof Macropodidae was first proposed in 1952 in Queensland byDurie and Riek.

3

A similar cycle has since been confirmed inNew South Wales,

4

in eastern Victoria,

5

in Western Australia,

6

and in south-eastern Australia.

7

The relatively high numbers ofhydatid cysts found in cattle at abattoirs in Queensland, northernNew South Wales and northern Western Australia

3,8–10

wereattributed to the presence of sylvatic cycles through contact withinfected dingoes. In contrast, transfer of the parasite from wild todomestic animals was not considered important in the sheep-raising areas of Victoria where both sylvatic and domestic cyclesoccur.

11,12

The first report on the sylvatic cycle of echinococcosis inQueensland

3

relied on the opportunistic examination of animalsfrom widely dispersed areas of the state, so no conclusions couldbe drawn about details of the lifecycle. A more detailed examinationwas made in the area south of the Tropic of Capricorn,

9,13

butthere is no detailed information on the ecological determinantsof

E granulosus

infection for pastoral areas of northern Queenslandnorth of the Tropic of Capricorn. The distribution of infectionin cattle in northern Queensland closely matches the distributionof the smaller species of Macropodidae. These appear to be themajor intermediate hosts in the region and the source of infectionin cattle.

2

Therefore, the present study was designed to test thishypothesis through an investigation of the interrelationshipsbetween dogs, dingoes, beef cattle and native fauna and theirhabitats in the lifecycle of

E granulosus

in a beef pastoral area ofnorthern Queensland.

Materials and methods

Study area

In 1981, a group of 7 adjoining properties situated about100 km south of Townsville in northern Queensland and knownto have cattle infected with hydatid cysts were selected for study(Figure 1). The area was approximately 3000 sq km and containeda variety of types of vegetation including areas of savannah, openwoodland and dense closed scrub. The annual rainfall wasapproximately 600 mm, most of which was received duringsummer.

Definitive hosts

Residents of the study area were questioned about the presenceof carnivores in the region and their relative abundance.Domestic dogs, dingoes and feral cats were common and onesighting of a fox had been made several years previously, but thisspecies was considered to be rare. All domestic dogs belonged topeople in the study area. Feral dogs were not seen. Dogs used tohunt feral pigs also entered the area from time to time, especiallyalong the rivers, but no information was available on thenumber, or frequency of their visits.

School of Veterinary and Biomedical Sciences, James Cook University, Townsville, Queensland 4811

a

Deceased

b

Corresponding author

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Arecoline hydrobromide was administered orally at 2 mg/kg toall of the domestic dogs over 4 months of age in the study area toinduce purging. The method of administration and detection ofworms described by Gemmell

14

were followed, with the excep-tion that if a dog failed to purge within 2 h of administration itwas given another dose the next day. Property owners were askedto save any dingoes they trapped or killed and these were sub-jected to post-mortem examination. The small intestines wereopened using the method described by Thompson

15

and the con-tents examined microscopically for the presence of

E granulosus

.Some dingo carcases were too decomposed to permit the detec-tion of worms. In these cases the liquefied mucosa and intestinalcontents were forced through a sieve with 150

µ

m diameterholes to break up any intact segments and release the eggs. Theresidue was then mixed with a saturated solution of zinc sulphateand examined for the presence of taeniid eggs using a standardflotation technique. Because no other species of taeniid tapewormoccur in dingoes or dogs in north Queensland,

16,17

the presenceof eggs was assumed to indicate infection with

E granulosus

. Cats

were not examined due to their low susceptibility to infectionwith this parasite.

4,18

Dog and dingo diets

Owners of the domestic dogs were questioned about the diet oftheir dogs. Answers were grouped into 3 categories: meat andoffal from home-killed livestock, meat and offal from nativefauna and commercially prepared dog food.

The diet of dingoes in the area was investigated by identifyingthe hair of prey species found in the stomach and colon of thedingoes at necropsy. The hair was washed and photographs takenof cross-sections, scale imprints and medullary patterns using themethod described by Brunner and Coman.

19

Comparisons weremade with photographs of hairs from known species in the region.

Intermediate hosts

Permits were obtained to collect common mammalian speciesfound in the area. These included various species of macropod andferal pigs. Rabbits and rodents were considered to be unlikely naturalintermediate hosts for

E granulosus

20,21

and were not included inthe survey. The site, diameter and viability of hydatid cysts wererecorded. Records were also kept of the species, sex and weight ofeach mammalian specimen and, in the case of macropods, anestimate of age was made by measuring the molar index.

22

Cattle from the properties in the study area were traced forwardthrough saleyards to the abattoir. The proportion of cattle foundto be infected was recorded for each property and cysts wereexamined for the presence of live protoscolices. Apart fromstock horses, no other livestock were produced in the area.

Results

Dogs

At the time of survey there were 22 domestic dogs over the age of4 months on the 7 properties in the study area. Samples of duodenalmucus were obtained from 17 of these at the first attempt andfrom another 4 on the second. None of these samples contained

E granulosus

.

The majority of dogs (18) were fed on home-slaughtered beefand beef offal, one received a commercial canned dog food andthree were fed on wallaby meat. In the latter cases, the ownerreported that only meat and bone were offered. All dogs in the areahad the opportunity to scavenge carrion from dead native animalsalthough owners did not believe that this happened frequentlybecause most dogs were under observation during the day andconfined at night.

No feral dogs were seen during 2 years of observation in the area,confirming the claim by local inhabitants that dingoes were theonly wild dogs in the area.

Dingoes

Post-mortem examinations were carried out on 21 dingoes, ofwhich 14 were male and 7 female. Estimates of age were attemptedby examining the teeth, but wear on the incisors did not appearto follow the same pattern as in domestic dogs, possibly due todifferences in diet. Dingoes were therefore classified as juvenilesor adults according to their degree of maturity, based on bodysize and sexual development.

Carcases of dingoes were presented in varying states of decompo-sition and, although it was possible in most cases to determine

Figure 1. Map of the Townsville district showing the study area.



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whether an animal was infected without resorting to the detectionof eggs, it was not possible to estimate worm numbers. However,it was clear that infections were high in many of the specimens.The prevalence of

E granulosus

in dingoes was 76% (16/21). Fiveof nine adult males and five of six adult females were infected. Alljuveniles, five males and one female were infected.

Hairs from prey species were found in the alimentary tracts of 13of the 21 dingoes and 6 had hairs from more than one species(Table 1).

Intermediate hosts

The two significant intermediate hosts were black-stripedwallabies (

Macropus dorsalis

) and feral pigs (

Sus domesticus

) withprevalence proportions of 21.8% and 9.4% respectively (Table 2).The other small wallabies suspected to be major intermediatehosts,

M parryi

(whiptail wallaby) and

M rufogriseus

(red-neckedwallaby),

2

were not present at the study site. All of the hydatidcysts found in macropods were in the thoracic cavity. Most werein the lungs but occasional cysts were found in the pleural cavityattached to the lungs by a thin peduncle. In macropodsprotoscoleces were present in 83% of cysts greater than 5 mmand in 100% of those over 20 mm in diameter. Chi-square analysisof the data for

M dorsalis

showed no significant difference inprevalence associated with age, sex or weight.

Of the 3 infected pigs, 2 harboured single cysts in the liver, oneof which was viable, and the third pig had a disseminated infec-tion with cysts in the liver (1, non-viable), lungs (4, non-viable),spleen (1, viable) and kidneys (2, viable).

The overall prevalence of hydatidosis in cattle from the studyarea was 21% (27/127). Cattle from properties which includedsubstantial areas of dense closed scrub had a prevalence of 41%

(25/61) compared with 3% (2/66) from properties with little orno areas of scrub. None of the bovine cysts were viable.

Discussion

A number of observations support a conclusion that the sylvaticcycle of

E granulosus

in the study area is maintained principallyby predation of

M dorsalis

(black stripe wallabies) by dingoes.Black stripe wallabies were the most common prey species ofdingoes. They also had the highest prevalence of infection withhydatids and the highest prevalence of viable cysts.

A single dingo might find difficulty in capturing an adult easterngrey kangaroo (

Macropus giganteus

) or wallaroo (

Macropus robustus

)because of its large size, but feet and ears found in the stomachsof some of the dingoes were clearly those of juveniles. During hisobservation of dingo predation on red kangaroos (

Macropusrufus

), Shepherd

23

noted that dingoes often ignored adults,preferring juveniles as prey, and it is possible that the same prefer-ence is shown for the young of other large macropods. The black-striped wallaby, on the other hand, is a relatively small species withaverage adult body weights of 14 kg for males and 6 kg forfemales. Analysis of stomach contents from dingoes indicatedthat all age groups of this species were subject to predation.

Macropods were the prey most commonly identified fromsamples of hair recovered from the alimentary tracts of dingoes.This is in agreement with surveys in other regions of Australia.

23–25

On the other hand, a survey

26

of the diet of dingoes in wet tropicalrainforests of northern Queensland found members of the Macro-podoidea were third after representatives of the families Muridaeand Peramelidae in order of predation. These authors concludedthat dingoes were opportunistic predators of a wide variety ofmammals, the most abundant forest-edge dwelling taxa beingthe most susceptible. This behaviour may explain the closeassociation between dingoes and black-striped wallabies requiredto maintain a viable sylvatic cycle. Black-striped wallabies wereinvariably found resting in areas of dense closed scrub duringthe day and emerged to feed on surrounding grasslands at dusk.From the frequency of tracks, it was noted that dingoes were alsoattracted to these areas, presumably in search of prey. As thewallabies did not move more than a few hundred metres fromthe protection of the scrub, even at night, the sylvatic cycle of

E granulosus

appeared to operate mainly within these limitedareas of dense scrub and their adjacent grasslands. It seems likely,therefore, that dense scrub acts as a nidus of infection for thesylvatic cycle of

E granulosus

in the study area. This conclusion issupported by the higher prevalence of infection in cattle fromareas with dense scrub (41%) compared with 3% from areaswith no or little scrub.

The results of this and other studies

27–30

confirm that hydatidcysts can develop in both the grey kangaroo and wallaroo. Thelow prevalence (<2%) found in those species may be due to theirpreference for feeding in areas of open woodland and savannah,rather than to an innate resistance to the parasite, as eggs of

E granulosus

are likely to be more concentrated on the verges ofdense scrub where dingoes hunt black-stripe wallabies than inopen woodland and savannah. A similar explanation may accountfor the absence of infection with hydatids in

W bicolour

in thepresent study, despite their high susceptibility to infection.

3,24

The low prevalence of hydatids in the grey kangaroo and wallaroo,the preference by dingoes for the young of these species as prey,

Table 1. Frequency and source of hairs from the alimentary tract of 13dingoes from the study area in northern Queensland.

Source of hairs Number of dingoes containing hairs

M dorsalis (Black-striped wallaby) 5

Bos indicus (domestic cattle) 5

Macropus giganteus (Eastern grey kangaroo)

4

Rodent (species not identified) 3

Not identified 4

Table 2. Proportion of animals infected with hydatid cysts in the study areain northern Queensland.

Species Number examined Percent infected

Macropus dorsalis (Black-striped wallaby)

78 21.8

Sus domesticus (Feral pig) 32 9.4

M giganteus (Eastern grey kangaroo)

73 1.4

M robustus (Wallaroo) 65 1.5

Aepyprymnus rufescens (Rufous bettong)

15 0.0

Wallabia bicolour (Swamp wallaby) 7 0.0

Bos indicus (Domestic cattle) 127 21.3

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the low density of

W bicolour

in the study area and their freedomfrom infection with hydatids, support a conclusion that thesethree species do not have a significant role in the sylvatic cycleof

E granulosus

in the study area.

Unlike other surveys, the present study revealed a high proportionof dingoes with bovine hairs in the alimentary tract. It is likelythat the source of the bovine hair was carrion rather than freshlykilled stock as most of the dingoes from which bovine specimenswere recovered were collected during the height of the 1983drought when dead cattle were a common sight at water holes.Although cattle from the study area had a comparatively highprevalence of hydatidosis (up to 41%) all of the cysts were viable,supporting a conclusion that cattle may be discounted as a significantsource of infection for dingoes, as shown previously.

2

Feral pigs potentially constitute a significant source of infectionfor canine predators when it is considered that 9.4% were infectedwith cysts of

E granulosus

, about half of which were non-viable,and pigs were common around rivers and swamps in the area.Presumably dingoes could readily catch and kill pigs, as trainedhunting dogs do. However, the role of wild pigs as intermediatehosts for dingoes may be limited by the apparent dietary preferenceof dingoes for macropods because there was no evidence fromexamination of the stomach contents of dingoes that they ate pigs.

Results support a conclusion that dingoes are the only residentdefinitive host of

E granulosus

in the area of northern Queenslandcovered by this study. Of particular note was the high prevalenceof infection in juveniles, demonstrating that dingoes becameinfected at an early age. Domestic dogs on properties in the areawere of no significance as definitive hosts, a conclusion supportedby absence of parasites in duodenal mucus and a diet thatprecluded infection. A similar conclusion was also reached insouthern Queensland.

13

Dogs which entered the area periodi-cally to hunt feral pigs were a possible source of infection because3% of such dogs were found to be infected with

E granulosus

.

16

However, the contribution to infection of intermediate hosts bypig-dogs is likely to be minor, due to the low prevalence of infectionin these dogs, the periodic nature of their visits and their habit ofrestricting their hunt to riparian areas.

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(Accepted for publication 27 June 2006)


echinococcus granulosus in northern queensland : 2. ecological determinants of infection in beef...

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