The geographic distribution and host range of Capillaria hepatica (Bancroft) (Nematoda) in Australia

Internarional Jmunalfor Parasitology Vol. 21, No. 8, pp. 945-957, Printed in Great Britain

1991 0

THE GEOGRAPHIC CAPZLLARZA HEPATZCA

DISTRIBUTION AND HOST RANGE OF (BANCROFT) (NEMATODA) IN AUSTRALIA SPRATT,S.C.

G.R.SINGLETON,*D.M. Division

002&7519/91 $3.00 + 0.00 Pergamon Press p/c 1991 Austrrrlim Society/or Parosifology

of Wildlife and Ecology,

CSIRO,

(Received 19 December

BARKER~~~~P.F.HODGSON

P.O. Box 84, Lyneham,

A.C.T.

2602, Australia

1990; accepted 30 June 1991)

AbStTPCt-SINGLETON G. R., SPRATT D. M., BARKER S. C. and HOD~SON P. F. 1991. The geographic distribution and host range of Capilluriu hepatica (Bancroft) (Nematoda) in Australia. International Journal for Parasitology 21: 945-957. The geographic distribution, host range and prevalence of Capillaria hepatica were recorded in 4629 house mice, A4us domesticus, 263 black rats, Rattus mttus, and 58 Norway rats, R. norvegicus. The parasite was found at five localities, all in or near large towns along the coast. The two Rattus species appeared to be the primary hosts of C. hepatica in Australia. Published and unpublished data on helminth infections of Australian native mammals from 1162 murids (26 species), 3018 marsupials (67 species) and 99 monotremes (two species) were compiled. Only seven animals from three murid species were infected with C. hepatica; all were from the same rainforest in northern Queensland. C. hepatica was distributed widely, occurring in the house mouse, black rat and Norway rat on a 10,850 ha farm but there was no infection in cattle, sheep or goats (abattoir records). Also, 52 rabbits, four cats and one fox (shot samples) and 27 marsupial mice, Sminthopsis crassicauduta (museum specimens), had no sign of C. hepnticu infection. Overall, the results indicate that transmission of C. hepatica to native, domestic and feral mammals is rare, presumably because of ecological constraints on egg embryonation and survival. In the light of these findings, the potential use of C. hepatica as a biological agent to control mouse plagues in Australia is discussed.

INDEX KEY WORDS: control; mouse plagues.

Geographic

distribution;

host range;

INTRODUCTION hepatica

was

* To whom all correspondence should be addressed. t Present address: Department of Parasitology, University of Queensland, Queensland 4072, Australia.

Capillaria hepatica; biological

details) requires host death, ingestion and digestion of infected liver (through cannibalism or necrophagy), and then deposition of unembryonated eggs in an environment which will allow eggs to survive and embryonate. Eggs deposited on the soil surface quickly die because they are susceptible to desiccation and U.V. light (Johnston, 1918). Mice are thought to become infected through embryonated eggs adhering to their fur or feet and then being ingested during preening (Spratt & Singleton, 1986). Eggs of C. hepatica are not infective until embryonation has occurred; thus predators that eat infected hosts will not become infected. C. hepatica has been reported in 34 species of mammals in North America but with one exception, no exclusively vegetarian species was infected (Solomon & Handley, 1971; Barrett & Chalmers, 1972). Therefore, transmission of C. hepatica should occur predominantly in small fossorial mammals, but persist only in populations of species that are carnivorous or omnivorous. The aims of the current study were: (i) to investigate the geographic distribution and prevalence of infection of C. hepatica in the house mouse, Mus domesticus, black rat, Rattus rattus, and Norway rat, R. norvegicus (hereafter referred to as the ‘introduced rodents’) in Australia; (ii) to compile from published and some unpublished records the geographic distribution, host range and prevalence of infection of C.

first described from rats in Brisbane by Thomas Bancroft (1893) nearly 100 years ago. It was reported also in Sydney (Johnston, 1918) and Townsville early this century (Fielding, 1927), yet little is known about the geographic distribution, host range, prevalence and epizootiology of this nematode infection in Australia. Previous results from the laboratory and the field indicate that C. hepatica could be used tactically as a biological agent to prevent mouse plagues (see Spratt, 1990; Singleton & McCallum, 1990 for reviews). The parasite is not known to occur in the cerealgrowing regions of Australia (e.g. Singleton, 1985) which are highly prone to mouse plagues. Before a release of the parasite into these regions can be undertaken, more information on its present geographic distribution, host range and prevalence of infection is required. Also, the likelihood of native and domestic animals becoming infected needs to be assessed. The life-cycle of C. hepatica (see Bancroft, 1893; Luttermoser, 1938; Spratt & Singleton, 1986, for Capillaria

mammals;

The

945

946

G. R. SINGLETON, D. M. SPRATT, S. C. BARKER and P. F.

TABLE I-DETAILS BLACK RATS

OF LOCALITIES ON

(Rattus

FIG. 1: YEAR OF COLLECTION, LOCATION. HABITAT TYPE, NUMBER OF HOUSE MICE (Mw domes&us), RATS (Rattus norvegicus) TRAPPED, AND THE NUMBER OF EACH SPECIES INFECTED WITH Capillaria hepatica

rutm) AND NORWAY

Site

Year

Location

1 2 3 4 5 6 I 8 9 10 11 12 13 14 15 16

1986 1986 and 1990 1986 1986 1986 1986 1986 1986 1984 1982-1990 1983 1986 1986 1986 1986 19861990

Port Lincoln Cowell Nelshaby Lower Light Adelaide Murray Bridge Keith Kangaroo Is Big Desert Walpeup and Ouyen Woomelang Horsham Hamilton Portland Warnambool Werribee

17 18 19

1987 1986 1988

Melbourne Healesville Sommerville

20 21 22 23 24 25 26

1988 1988 1988 1989 1986 1990 1981-1990

Koo-wee-rup Moe Sale Flinders Is Launceston Hobart Nadgee

21 28 29 30 31 32 33 34 35

1987 1983-1990 1984 1986 1982-1986 1986 1989 1989 1986andl989

Mogo Canberra Jerilderie Coleambally Griffith Woodstock Trangie/Dubbo Narrabri Moree

36 37

1988 1983andl988

Jervis Bay Sydney

38 39 40 41 42 43 44 45 46 41 48 49 50 51

1986 1986 1986 1987 1986 1986 1986 and 1989 1986andl989 1979andl981 1986 1986 1990 1987 1987

Newcastle Taree Kempsey Arid zone Currumbin Tamborine Mt Brisbane Darling Downs Townsville Atherton Alice Springs Penong Boullanger Is Thevenard Is

*Inf = number

HODGSON

of animals

Habitat

Cereal Cereal Cereal Cereal City Cereal Cereal Buildings Heathland Cereal Cereal Cereal Cereal Pasture Pasture Pasture and sewage lagoons City zoo Pasture store and poultry Aviaries and poultry Dairy/pigs Swamp/town Pasture City Uni campus Dry sclerophyll forest Dry scler City/forest R&/cereal Rice/cereal Rice/cereal Cereal Cereal/zoo Cereal/soybean Cereal/cotton Forest City/zoo/animal house Industrial Seed store Dairy Sand dunes Animal park Showground City/farms Cereal Town Farm bldg Town Cereal Native veg. Native veg.

infected with C. hepatica.

M. domesticus Inr n 0

0 0

100 39 82 63 51 16 15 8 16 1137 57 2 14 11 4

16 0 0

371 48 22

0 0 0 0 0

36 79 7 18 15

0

8

0 0 0 0 0 0 0 0 0

197 7 475 51 60 35 17 39 100

0

142

0 0 0 0 0 0 0 0 0

0 0 0

145 0 1 0 0 0 0 0 0

258 12 29 30 5 26 20 48 201

0 0 0 0 0

12 11 10 16 3

R. rattus Inf n

10

25

0 0 0

13 2

0 0 0

R. norvegicus Inf n

15

28

4

5

11

15

4

10

6 31

0

0

14

59 0

126

0

3

0

4

1 0 0

12 15

Distribution

941

and host range of C. hepafica

I i

i

I

4,8

i

: \-,

!

i i.-.-.-.-.-._.L._.~ !

i

1Taree

Perth

q .

Wheat Growing Areas Trapping Sites

*

Confirmed Infections

*

Likely Sites

FIG. 1. Localities where house mice, black rats and Norway rats were trapped and examined for occurrence of Capillaria hepatica. The numbers of each species trapped, the percentage of hosts infected with C. hepatica at each locality and the habitat type are given in Table 1. Likely sites (open star): Townsville, infection reported in R. norvegicus and R. rams (Fielding, 1927); Melbourne and Perth, infection in zoo animals communicated verbally to one of us (D. M. Spratt).

17

Unirrigated pasture

H

Sedimentation bays

0 SCALE

1

Zkm

-

FIG. 2. The distinction of habitat types on the Melbourne and Metropolitan Board of Works (MMBW) farm at Werribee and location of sites where rabbits, cats and a red fox were shot. At some sites two animals were shot. Shot samples were taken in February and March 1990.

948

G. R. SINGLETON, D. M. SPRAT~, S. C. BARKER and P. F. HODGSON

PmPhillip Bay PREVALENCE OF CHEPATICA SAMPLE SIZE

IN RODENTS

>40 SCALE

0 I

1

2km

FIG. 3. The distribution of trapping sites on the MMBW farm and the prevalence of Cupillariu hepatica infection in the three species of introduced rodents at these sites. This figure represents a compilation of trapping data from April 1986 to March 1990.

in species of native rodents, monotremes and marsupials; (iii) to examine the habitat distribution and prevalence of infection of C. hepatica on a large farm near Melbourne where the parasite occurs in the three species of introduced rodents; and (iv) to determine whether domestic, feral and native mammals sympatric with these three species on the farm have become infected with C. hepatica. hepatica

METHODS Distribution of C. hepatica in introduced rodents. The distribution of C. hepaticu infection was investigated by trapping house mice, black rats and Norway rats at more than 150 sites in Australia. To simplify presentation, results were pooled from sites within close vicinity of each other or in similar habitat within a region (Fig. 1). For example, the locality given as Sydney is a compilation of five different sampling sites from the metropolitan area. Data are presented for 51 localities (Table 1). Many different habitats were trapped, ranging from backyard aviaries to zoos, small shops to large supermarket warehouses, arid desert habitats to coastal forests, and across a diverse range of crops-winter cereals, oilseeds, rice, coarse grains and cotton. Mouse populations in the Mallee (Victoria) and the Darling Downs (Queensland) cereal-growing regions were sampled in nonplague and plague years. Each animal was measured ( f 1.O mm) from tip of snout to distal end of anus. Mice were assigned to one of three size classes 172 mm (sub-adults), 72-78 mm (small adults) and > 78 mm (large adults) (after

Singleton, 1989). Rats were assigned to two size classes: ~200 or >200 mm. The livers of animals were examined grossly. If there was any sign of lesions or spots on the liver surface these were examined further under a binocular microscope (x 250). Confirmation of infection required recovery of identifiable worm fragments or of eggs of C. hepatica with characteristic shell morphology and ornamentation. Distribution of C. hepatica in native rodents, monotremes and marsupials. Records of the presence or absence of C. hepatica infection in species of native rodents, monotremes and marsupials were compiled from published papers on the helminth fauna of these species and from data collected between 1967 and 1990. The bulk of the latter were from studies by D. M. Spratt (mainly from eastern Queensland and south-eastern N.S.W) and P. J. A. Presidente (Mitchell Plateau, Western Australia). The records are of animals collected from numerous locations. To simplify presentation, records were divided broadly into the six states and the Northern Territory. Records from the Australian Capital Territory were combined with those from New South Wales. Distribution andprevalence of C. hepatica at Werribee. The study was located at the Melbourne and Metropolitan Board of Works (MMBW) farm at Werribee, Victoria. The 10,850 ha farm is located on the edge of metropolitan Melbourne along the western side of Port Philip Bay. The region has a Mediterranean climate and the farm has an average annual rainfall of 5 12 mm. The main soils are fine red-brown to greybrown sandy and sandy clay loams, and those derived from basaltic parent materials. Much of the habitat has been

Distribution

TABLE 2-PERCENTAGEOFANIMALSINFECTEDWITH Capillariahepatica

Qld

Species

N.S.W.* (% ii)

(% n) Rattus colletti R. sordidus R. tunneyi R. lutreolus R. leucopus R. fuscipes R. villosissimus Rattus sp. R. norvegicusf R. rat&s $ Mus domesticus $ Mastacomys fuscus Pseudomys nanus P. delicatulus P. gracilicaudatus P. hermannsburgensis P. higginsi Zyzomys argurus Z. woodwardi Conilurus penicillatus Mesembriomys gouldii Notomys mitchelli Uromys caudimoculatus Melomys burtoni M. cervinipes M. sp. 1 M. sp.2 Hydromys chrysogaster Pogonomys mollipilosus

949

and host range of C. hepaticu

Vie (% n)

Sth A. (% n)

INRODENTSPECIESINAUSTRALIA Tas (% n)

W.A. (% n)

N.T. (% n) 0 22

0

48

0 0 17 0

5 8 80 8

0 1 0 186

0

0 426

0 47

0 28 5 0

857 1253 28

0 0

1 4

2

0

8

0

5

0 12

1

3 219 3 73 0 8

0 12 0 12 0 18 0 8 0 2 0 0 24t 0 1t 0 0 0 0

4 4 21 18 86 7 4 26 2

0 0

1 7 0 23 0

0

2

0 32

* Includes ACT. t All infected animals were captured in Danbulla Forest Reserve in northern Queensland. $ Records prior to 1976; see text for details. Note: Records were obtained from the following-Johnson (1918); Fielding (1927); Waddell (1975); Glazebrook et al. (1978); Obendorf (1979); Obendorf L Smales (1985); Spratt (1987).

modified to function as a land filtration system of industrial and human waste (Fig. 2). Some waste is treated also in lagoons through settlement and bacterial action. The main habitats are permanent pastures (summer and winter irrigated areas), lagoons, unirrigated pastures, banks of rivers and streams, coastal heath, sedimentation bays (where sewage sludge is decomposed) and various buildings (including houses, stables, haysheds and recreation and administration buildings) (Fig. 2). Cattle (19,000 grazed per year), sheep (30,000) and goats (~500) are produced for human consumption. Two native species of small mammal are common on the farm; the water rat, Hydromys chrysoguster, along the banks of streams and artificial channels, and the fat-tailed dunnart, Sminthopsis crassicaudata, under basaltic rocks in fields. The house mouse, black rat and Norway rat were trapped in a range of habitats on the farm on six occasions, at various times of year, from April 1986 to March 1990. Mice were caught using Longworth and Elliott live-capture traps, and rats using wire cage traps (585 x 215 x 215 mm). All captured animals were measured, sexed, killed humanely by cervical dislocation, and examined for C. hepatica infection. Females were examined also for breeding condition (presence of embryos and/or uterine scars; size of uterus; evidence of lactogenesis). An abundance index of each species was estimated by determining the number

1

(1969); Peisley & Howell

caught per 100 trap nights. In addition to the routine trapping, the Victorian Field Naturalist’s mammal survey group collected specimens of the three introduced rodent species at various times. The exact locality of capture and demographic data were not always available for these animals. Host range of C. hepatica at Werribee. Information on the occurrence of C. hepatica infection in other host species was acquired as follows: (i) cattle, sheep and goats via abattoir records (eight livers of cattle were examined thoroughly); (ii) rabbits (n = 52), feral cats (n = 4) and one fox were shot and examined; (iii) 27 fat tailed dunnarts from museum specimens that were caught on the Werribee farm from 1973 to 1976 were examined (there were no museum specimens of the native water rat, Hydromys chrysogaster); and (iv) fresh road kills of native animals were examined. The shot samples of rabbits and cats included sites on the farm where infected rodents occurred (Figs. 2 and 3). Statistical analysts. Prevalence of infection with C. hepatica and the relative abundance of host species at Werribee were analysed separately by considering probability of infection and probability of capture as binomial variates using generalized linear models with binomial error and a logit link function (see McCullagh & Nelder, 1983). In this analysis the abundance index (number of mice caught per 100

950

G. R. SINGLETON, D. M.

hepatica

TABLET---PERCENTAGEOFANIMALSINFECTEDW~THC~~~N~~~~

Qld

Species

(% n) Ornithorhynchus anatinus Tachyglossus aculeatus Planigale gilesi P. maculata Antechinus leo A.Jlavipes A. minimus A. stuartii A. swainsonii Phascogale tapoatafa Dasyurus hallucatus D. maculatus D. viverrinus Sarcophilus harrisii Sminthopsis leucopus S. crassicaudata S. virginiae Perameles gunnii P. nasuta Isoodon macrourus I. obesulus Trichosurus caninus T. vulpecula johnstonii T. vulpecula vulpecula T. arnhemensis T. squamicaudata Cercartetus nanus C. lepidus Acrobates pygmaeus Petaurus australis P. breviceps Pseudocheirus herbertensis P. peregrinus Pseudochirops archeri Hemibelideus lemuroides Petauroides volans Dactylopsila trivigata Hypsiprymnodon moschatus Potorous trithtctylus Bettongia gaimardi Aepyprymnw rufescens Thylogale thetis T. billardierii T. stigmatica Petrogale brachyotis P. godmani P. inornata P. assimilis P.a. “Mareeba” P.a. “‘Mt Clara” P. lateralis purpureicollis P. penicihata P. herberti P. persephone Lagorchestes conspicillatus Macropw fuhginosus M. giganteus M. agilis M. eugenii M. parryi M. rujogriseus

0 0 0 0 0

5 1 1 1 2

0

4

0 0 0

1 2

0 0

3 I

N.S.W. (% n) 0 0

0 57 0 6 0 8

5 9

INNATIVEMONOTREMEANDMARSUPIALSPEC~ES~NAUSTRALIA

vie (% n)

Sth A. (% n)

Tas (% n)

0

0

0

7s

2

W.A. (% n)

0

0

1

0 0 0 0

5 9 8 3

0

5

0

6

0 183

0 10 0

1

0 0

11 27

0 41 19 7

0 109

0 124

0

2

0

31

1 2 2 1 2 1 2 4

0

5

0 0 0

3 2 10

0

17

0

30

0

0 11

7

0 I2

0

2

0

3

0 21 0 0

0 0 0 0 0 0 0 0

1

1

0 545 0 160

0 0 0

N.T. (% n)

3 0

1

0 12 0 21

S. C. BARKER and P. F. HODGSON

SPRATT,

0

2

0 0

3 4

0

5

1 1

10

0 18 0 3 0 13 0 0 0 0 0 0 0 0 0 0 0 0

13 15 36 3 4 3 2 11 2 8 13 7

0 0

24 56

0 3 0 119

0

5 0 65

0 105 0 0

6 1

0

46

0

4 Continued

Distribution Table 3 Continued M. robustus M. rufus Wallapia bicolor Onychogalea fraenata 0. unguifera Dendrolagus lumholtzi Phascolarctos cinereus Vombatus ursinus

0 3 0 59 0 9 0 2 0 13 0 7 0 13

and host range of C. hepntica

0 1 0 552 0 27

0

33

0

0

62

57

951

0

4

Note: Records were obtained from the following-Mykytowycz (1964); Beveridge & Barker (1975, 1976); Peisley & Howell (1975): Smales & Mawson (1978); Arundel, Beveridge & Presidente (1979); Beveridge & Arundel (1979); Presidente (1982a,b,c); Presidente, Barnett, How & Humphrey (1982); Speare, Beveridge, Johnson & Comer (1983); Beveridge, Presidentek Speare (1985); McOrist & Smales (1986); O’Callaghan & Moore (1986); Smales (1987); Spratt (1987); Beveridge, Spratt, Close, Barker & Sharman (1989); Arundel, Dempster, Harrigan & Black (1990).

TABLE &PREVALENCE

hepatica INFECTION IN HOUSE norvegicus) ANDBLACK RATS (R~~~~~~~~~~~)INRELATIONTOSEASONANDSIZECLASS (mm) ONTHE MMBW

MICE (MIS

domesticus),

(%)

OF

NORWAY

Capillaria

RATS (Rattus

FARM AT WERRIBEE

Class Summer* Males FemZes Comnbined Autumi+ Males FemZes Comnbined

House mouse <72 72-78 >78

0

19 0 19 0 38 0

10 0 8 0 18

Winter; Males n Females Comnbined

0 38 9.1 11 2.0 49

2.9 70 8.6 35 4.8 105

0 1

0 25 0 8 0 33

12.5 48 5.6 18 10.6 66

75.0 4 0

8.0 12 0 8 5.0 20

4.0 25 0 6 3.2 31

Spring; Males Femiles n Other (combined Feb 1988 n

Norway rat <200 >200

0 0 50.0 2 50.0 2

Black rat <200 >200

4.0 5

0 2 0 0 0 2

42.9 7 33.3 6 38.5 13

66.6 9 33.3 6 53.3 15

0 2 0 1 0 3

75.0 4 0 0 75.0 4

100.0 3

100.0 1 100.0 1

0 3

100.0 1

sex and class)

* Two trap sessions-February t Three trap sessions-April $ One trap session-August 0 One trap session-October

0 6

1987; December 1989. 1986; May 1988; March 1990. 1987. 1989.

trap nights) was expressed as a percentage. The parameters fitted in themodel were species of rodent (n = 3), habitat type (n = 7) and time (n = 4; 1986,1987,1988,1989-1990). The time

interaction terms were treated as residual deviance. Significance values (P < 0.05) were determined for each model from analysis of deviance which asymptotically follow an F-distribution.

952

G.

R.

SINGLETON,

D. M. SPRAIT, S. C.

BARKER and P. F. HODGSON

TABLE ~-THE HABITATOF CAPTUREOF HOUSEMICE, NORWAYRATSAND BLACKRATS,THEABUNDANCEOF HOSTS,AND THEIR RESPECTIVE PREVALENCESOF INFECTIONWKTHCupilluria hepaticu ON THE WERRIBEE MMBW FARM; THE DATA WERE COLLECTEDBETWEEN APRIL 1986 AND MARCH 1990

Habitat

Species

Lagoons

Mouse Norway rat Black rat

52

Number captured*

Species abundancet

Prevalence (%) C. heparical

10

17.2 2.7 27.2

0.0 0.0 30.0

Mouse Norway rat Black rat

58 8 5

9.7 5.6 2.2

5.2 62.5 60.0

Mouse Norway rat Black rat

67 0 0

13.6 0.0 0.0

0.0 0.0 0.0

Banks of rivers and creeks

Mouse Norway rat Black rat

69 1 4

15.4 2.2 4.3

1.4 100.0 50.0

Foreshore

Mouse Norway rat Black rat

71 6 5

17.8 11.3 9.4

8.5 83.3 40.0

Mouse Norway rat Black rat

34 2 0

17.4 22.2 0.0

14.7 0.0 0.0

Mouse Norway rat Black rat

24 2 1

11.8 14.3 7.1

0.0 50.0 0.0

Irrigated

pasture

Unirrigated

pasture

of bay

Buildings

Sedimentation

area

1

* There were no details on habitat of capture for eight Norway rats and one black rat (all caught t Host abundance was estimated from the number of animals caught per 100 trap nights.

in August

1987).

$ Prevalence values include one trapping session where site of capture of animals was available but not the trap success.

RESULTS Distribution of C. hepatica in introduced rodents C. hepatica was found at five localities, all near or in large towns along the coast (Fig. 1). None of the 2764 mice and four black rats sampled from 19 localities in the cereal-growing regions were infected (Table 1). In the localities where C. hepatica occurred, the prevalence of infection was highest in Norway rats (26 out of 43) but not significantly higher than black rats (70 out of 152) (x’, = 2.8, P>O.O5). Both rat species had prevalences significantly higher than house mice (162 out of 658) (house mice vs black rats, x2, = 27.8, P
examined for hehninth infections, only seven rodents from three species were infected with C. hepatica (Tables 2, 3). Eggs believed to be those of C. hepatica (on the basis of egg shell ornamentation) were observed in histological sections of liver of the bush rat, Rattus fuscipes, the while-tailed rat, Uromys caudimaculatus, and the fawn-footed Melomys, Melomys cervimpes. Adult worms of this species were not observed at post mortem examination although adults of Hepatojarakis pycnofasciatus, larvae of Ophidascaris robertsi and calcified larvae of an undetermined species of acanthocephalan were found in livers of these hosts. All infected animals occurred in the Severin logging area of Danbulla Forest Reserve (17” 11‘S; 145’4O’E) in northern Queensland, an area of complex notophyll vine forest (wet uplands) on basaltic red earths (Tracey, 1982) which had been logged 10 years previously. Distribution andprevalence of C. hepatica at Werribee Capillaria hepatica infections occurred in 4.3% (n = 371) of house mice (M. domesticus), 35% (n = 26) of black rats (R. rattus) and 54% (n = 28) of Norway rats (R. norvegicus) (Table 4).

953

Distribution and host range of C. hepatica TABLE ~INDEXOPPO~ULAT~ONABUNDANCEOFHOUSEMICE(NUMBEROFMICECAUGHTPER I@, T-NIGHTS) ANDPERCENTAGEOFADULTFEMALES (HEAmBODYLENGTH > 71 BREEDINGATTHEWERRIBEEMMBWFARMAPR~L I~~~TOMARCH 1990

Month

Year

Abundance index

April February August May December March

1986 1987 1987 1988 1989 1990

13.5 22.9 8.9 14.7 17.4 9.6

Generalized linear modelling revealed significant differences in prevalence of C. hepaticu between species (corrected for habitat; F2,,6 = 6.25, P = O.Ol), but no significant habitat differences (corrected for species; = 1.45 P > 0.1) or species by habitat interaction $i:, = 3.46 P> 0.1). The mean prevalences adjusted for’habitat and time ( f S.E.)were 6% ( f 1.7) for mice, 44% (f 9.1) for black rats and 43% (f 8.4) for Norway rats. Some rats were not included in this analysis because their habitat of capture was unknown. No significant differences in estimates of population abundance occurred between species (F2,29 =OSO, P>O.l), habitats (Fez9 = 1.31, P>O.l) or the interaction between species and habitat (F,0,29 = 1.46, P>O.l). Infected rodents were widely distributed on the farm and were found in habitats ranging from banks of rivers and coastal heath, to an indoor feed preparation and storage room in horse stables (Fig. 3). In unirrigated areas of the farm (see Fig. 2) where only mice were caught, no animals were infected (Table 5). The highest prevalence of C. hepatica infection was in the largest size class; 6.9% of mice > 78 mm (n = 203) 47.4% of black rats 2 200 mm (n = 19) and 60.9% of Norway rats 2200 mm (n = 23). No subadult mice ( < 72 mm, n = 60) or black rats < 200 mm long (n = 5) and only one Norway rat < 200 mm (n = 2) were infected with C. hepatica. Prevalence of infection with C. hepatica was too low overall to test for seasonal differences (Table 4). Prevalence of infection was the same in males and females for mice (4.4%) and black rats (37.5%). In Norway rats, more males (75%, n = 16) than females (33.3% n = 9) were infected but the sample sizes were too small for meaningful statistical analyses (Table 4). The index of population abundance of house mice during the 4 years ranged from 8.9 in August 1987 to 22.9 in February 1987. Adult females were breeding on every occasion. Breeding performance was highest in summer and lowest in late autumn and winter. No data were available for spring (Table 6). Host range of C. hepatica at Werribee None of the rabbits, cats, the fox or native animals were infected with C. hepatica (Table 7). The stomach

mm)

Adult females breeding n W) 10 28 14 5 18 11

20.0 17.9 7.1 40.0 66.6 54.5

contents of each cat was examined. Each stomach had remains of at least three mice. The museum specimens of S. crassicaudata had no signs of C. hepatica infection. On average 6500 steers at 18-22 months of age are sold from this farm to abattoirs each year, and some 24,000 sheep are fattened and sold each year. There have been no reports of C. hepatica infection from abattoir records of cattle or sheep. There are few recent abattoir records for sheep because during our study most were sold for live export. DISCUSSION C. hepatica was found principally in populations of rodents located in or near coastal towns (Fig. 1). The exception was in rainforest in Danbulla Forest Reserve where three native rodent species were infected (Table 2). This forest was approximately 12 km from Atherton and 45 km from the coast. Capillaria hepaticu has not been reported from birds or reptiles in Australia or elsewhere. Knowing the habitat distribution of C. hepatica in Australia is important in assessing the potential of the parasite as a biological agent to prevent mouse plagues (Singleton & McCallum, 1990). Absence of C. hepaticu in the cereal-growing regions supports its potential because if it was present and widespread, we would not expect plagues to occur. Eggs of C. hepatica are susceptible to WV. light and to desiccation (Johnston, 1918). In the majority of habitats in Australia, which is a “dry” continent, survival of eggs requires their release from the liver and subsequent deposition below ground, a scenario most consistent with eggs being released in burrows after cannibalism or intraspecific necrophagy. A formidable ecological barrier to interspecific transmission of the parasite is apparent over much of Australia, especially in drier areas such as the cerealgrowing regions (Spratt & Singleton, 1986; Singleton & McCallum, 1990). This barrier would not be as stringent in the damp litter of a rainforest, exposed only to strongly filtered U.V. light, where survival and subsequent embryonation of eggs of C. hepatica may occur. Thus, the occurrence of infection in three native murid species in a rainforest in northern Queensland is

G. R. SINGLETON, D. M. SPRATT,S. C. BARKER and P. F. HODGSON

954

TABLE~-THE PREVALENCE (%) OF Capiiiaria hepatica INFECTION IN ANIMALS, THENUMBER OFSITESSAMPLED ANDTHE NUMBER OF SITESWITHINFECTED RODENTS ON THE WERRIBEEMMBW FARM; DATAON THERODENTS WERECOLLECTED BETWEEN APRIL 1986 ANDMARCH 1990, DATAONTHEOTHER ANIMALS WERECOLLECTED IN FEBRUARY ANDMARCH1990

Animal host

Rodents House mouse Black rat Norway rat Others Rabbit Domestic cat Red fox Cattle Tiger snake Whistling kite

Prevalence of C. hepatica No. of sites sampled No. of sites with C. n hepatica (%) 371 26 28

4.3 34.6 53.6

33 12 6

Sites which had infected rodents

6 6 3

52 4 1 8 1

36 3 1 n/a 1

7 2 0 n/a 1

1

1

1

consistent with our knowledge of the life-cycle of C. heputicu and the environmental constraints on egg embryonation and survival. The strength of these environmental barriers is best indicated by the absence of the parasite in commensal populations of native species (Tables 2 and 3), supporting the contention that they rarely come into contact with infective eggs. This is highlighted by the absence of infection in native mammals living in or around coastal towns where C. hepatica occurs in introduced rodents. Indicator species include the brushtail possum (over 290 records from the five eastern and southern states), ringtail possum, bush rat, water rat, swamp rat, bandicoots, marsupial mice (Antechinus spp. and Sminthopsis spp.) and the grey kangaroo. This contrasts with the catholic host range of C. hepaticu among carnivores and omnivores in North America (Solomon & Handley, 1971) and the successful establishment of C. heputicu experimentally in the brushtail possum, Trichosurus vulpeculu (Spratt & Singleton, 1986) and the bush rat, Rattus jiicipes. These two species are well-adapted to living alongside humans over a broad geographic range in Australia. Four possible reasons why C. heputica has not been reported in the cereal-belt of Australia have been proposed (Spratt & Singleton, 1987). The two most likely explanations are: (i) for several years after plagues, mouse densities are generally very low; the population dynamics of C. heputicu (especially mode of transmission) may prevent it from surviving these prolonged host population bottlenecks (McCallum & Singleton, 1989); and (ii) maintenance of the parasite in mouse populations may be dependent on the presence of one or both species of introduced rats. Both the black rat and the Norway rat are less common in the cereal-growing regions than in urban environments along the coast. How do these explanations compare with our understanding of the host dynamics and host-parasite

associations on the Werribee farm? Firstly, from 1986 to 1990, the Werribee farm had a moderate abundance of mice irrespective of season or year of study. From other field studies in Australia their abundance should be lowest in late winter and early spring and highest around late autumn (Newsome, 1969; Singleton, 1989, Singleton & Redhead, 1990). Compared to these population studies, the lowest abundance at Werribee was relatively high but the peaks in abundance were relatively low. There has been no record of a mouse plague on the Werribee farm (Singleton & Redhead, 1989). Thus, the mouse population there does not experience the boom-bust outbreaks that occur in the cereal-growing regions. Instead, the population density appears to be maintained above the threshold required for persistence of the parasite in mouse populations (see McCallum & Singleton, 1989, for discussion of this threshold). Second, the two Rattus species were the principal hosts of C. heputicu and infected mice were living sympatrically with both species of rats. Thus, the Werribee farm provides an environment well suited to the persistence of C. heputica in a mouse population either because rats are the principal hosts of the parasite or because mouse population density is high. The likely role of the two Ruttus species in the geographic distribution and prevalence of C. heputicu infection in mice in Australia was further supported by the survey study; at each locality where mice were infected, one, and most often both species of rats were present. These results reinforce the suggestion that the Rattus species are the primary reservoirs of C. heputicu infection and that mice and other small mammals are secondary hosts (Farhang-Azad, 1977; Childs, Glass & Korch, 1988). C. heputicu occurred in all three species of rodents only at Werribee and in the Sydney metropolitan area. At both locations the prevalence of infection of C. heputica was many times higher in the Norway and

Distribution and host range of C. hepatica black rats than in mice. Bancroft (1893) indicated that most of the rats he examined in Brisbane in 1891 were infected with C. hepatica but he did not state the species. Waddell (1969) reported infection in 79% of Norway rats (n = 240) trapped close to the central business district of Brisbane in the late 1960s. Johnston (1918) recorded infection in 3% of both black rats (n =219) and mice (n = 73) examined in Sydney in 1909 and 1910, and Fielding (1927) in 8% of Norway rats and 5% of black rats examined in Townsville (n > 1700) in 1925 and 1926; none of the three mice examined were infected. Fielding also examined five H. chrysogaster which were uninfected. Unfortunately no other epidemiological data were reported in these early studies. More recently, C. hepatica infection was not recorded in 96 black rats, three Norway rats and 25 mice in coastal and subcoastal locations, and on the Atherton Tableland in northern Queensland (Glazebrook, Campbell, Hutchinson & Stallman, 1978). Childs et al. (1988) reported a prevalence of 87.4% in Norway rats compared with 5.4% in house mice and 0% in meadow voles and white-footed mice in urban Baltimore. As in our Werribee study, larger animals had a higher prevalence of infection. These authors noted that house mice only rarely have been reported to be infected with C. hepatica in natural settings. In reality, surprisingly few surveys of the parasite communities in wild house mice have been reported throughout the world. Luttermoser (1936) found C. hepatica in 85.6% of 2500 R. norvegicus examined in a survey in Baltimore. However, only 5% of these had infections in which one-half or more of the liver was involved. This author subsequently conducted a series of experiments with laboratory rats and mice (Luttermoser, 1938). He demonstrated that the rat possesses a natural resistance against infections of a certain size, becomes more resistant with age and is able to develop an active, acquired resistance to infection. In contrast, C. hepatica developed slightly faster in the mouse than in the rat as a consequence of a slower and less intense host reaction to the presence of the parasite. Mice did not exhibit nor acquire a resistance to infections although they did demonstrate a partial age resistance. Luttermoser concluded that rats have a much greater tolerance and control of C. hepatica infection than do mice. These results are consistent with the suggestion that rats are the primary host for the parasite and mice are secondary hosts. Results of the present study indicate that commercial livestock, rabbits and mammalian predators of mice were not infected with C. hepatica on a farm where the parasite has been extant for at least 4 years and probably decades. As noted earlier, the brushtail possum potentially is a key indicator species for C. hepatica infection in native animals living in association with humans. Although no possums were collected in the current study, none of 10 examined at nearby Werribee Park estate in 1976 and 1977 were infected (Presidente, 1982a).

955

S. crassicaudata are carnivorous and on the farm they occasionally share winter nests under rocks with house mice (Morton, 1978). No other species of native mammal is known to share nests with house mice. Thus, the potential exists for transmission of C. hepatica from mice to S. crassicauduta. There is no evidence, however, that this occurs nor that the marsupial mouse population is threatened with extinction-the S. crassicaudata population at Werribee is one of only two substantial populations within a 75 km radius of metropolitan Melbourne (D. Williams, personal communication). Of 24 mammal species recorded on the farm in a survey in 1987, only the S. crassicaudata population was considered to be of State (of Victoria) significance (Schulz, 1987). The survey was conducted over 6 weeks in late summer when 133 individuals were detected (Schulz, 1987). The main sampling method was turning over rocks (119 animals caught); a method which returns the highest capture in winter (Morton, 1978). Thus, the S. crassicaudata population on the Werribee farm was appreciable during the current study. The apparent restriction of C. hepatica to the introduced rodents at the Werribee farm is surprising. Flush irrigation provides a damp environment with lush growth of grasses, conditions considered favourable to the embryonation and survival of C. hepatica eggs (e.g. Johnston, 1918; Freeman & Wright, 1960). In one study in North America, however, the parasite was confined almost entirely to hosts living in relatively dry scrub habitat (Layne, 1968). CONCLUDING REMARKS The persistence of C. hepatica at Werribee was consistent with the relatively stable population dynamics of house mice on the farm. Indices of mouse population abundance were well below the levels that cause significant economic damage in the cerealgrowing regions. Whether this was due to limitations of resources or to C. hepatica infection playing an important role in the regulation of the population could not be determined from this study. A longitudinal population study on the Werribee farm with more frequent trapping sessions, a non-destructive method for monitoring the prevalence of C. hepaticu infection and an emphasis on how mice share resources with the two Rattus spp. (especially food and burrows), would provide an excellent basis for understanding the dynamics of this host-parasite interaction. The broad spatial distribution of the parasite on the Werribee farm and the lack of significant habitat differences in the prevalence of infection of C. hepatica in the three rodent species, augurs well for the tactical use of the parasite to control mouse plagues. The success of a field release program will rely on the establishment and then persistence of the parasite over a wide area and in a variety of habitats. C. hepatica infection was absent from over 4000 native mammals. Only seven animals were infected, all in the same rainforest area of northern Queensland. At

956

G. R. SINGLETON, D. M. SPRATT, S. C. BARKER and P. F. HODGSON

Werribee, only the three introduced rodent species were infected despite the widespread occurrence of the parasite in these rodent populations for at least the previous 4 years and environmental conditions suitable for egg embryonation and survival. Overall, the results of the present study strongly suggest an ecological barrier to interspecific transmission of C. hepaticu in mammalian species in many regions of Australia and the likelihood of this barrier existing in the cereal-growing regions. Acknowledgements-We thank Colin Tann, Glenn Schipp and Michelle Leishman for their expert and enthusiastic technical assistance, Monica van Wensveen for drawing the figures and Warren Miiller for his advice on analysing the data. We are indebted to David Obendorf, Paul Presidente and Rick Speare for access to their unpublished data. Many people assisted in collecting rodents during our survey of C. hepatica. We thank them all but in particular Greg Mutze, Francis Crome, Mary Bomford, Chris Dickman, Hamish McCalIum and Michael Stoddart. At Werribee we were generously assisted by David Williams and other staff of the MMBW farm, and by Julian Grusovin and the Victorian Field Naturalists Club. We thank Joan Dixon of the Museum of Victoria for allowing us to examine the livers of S. crassicaudata in the museum’s collection. Our appreciation is extended also to Roger Pech, Hamish McCallum and Hugh Tyndale-Biscoe for their critical comments on a draft of this manuscript. This research was funded partially by Rural Credits Development Fund grants 8714 and 8926 and Wheat Research Council of Australia grant CSV4. REFERENCES ARUNDEL J. H., BEVERIDGEI. & PRESIDENTEP. J. A. 1979. Parasites and pathological findings in enclosed and freeranging populations of Macropus rufus (Desmarest) (Marsupialia) at Menindee, New South Wales. Australian Wildlife Research 6: 36 l-37 1. ARUNDELJ. H., DEMP~TERK. J., HARRIGAN K. E. & BLACK R. 1990. Epidemiological observations on the helminth parasites of Macropus giganteus Shaw in Victoria. Australian Wildrife Research 17: 39-5 1 BANCROFTT. L. 1893. On the whipworm of the rat’s liver. Journal and Proceedings of the Royal Society of New South Wales 27: 8690. BARRETTM. W. & CHALMERSG. A. 1972. Capillaria hepatica (Nematoda: Trichuridae) in pronghorn antelope (Antilocapra americana Ord) in Alberta. Journal of Wild@ Diseases 8: 332-334. BEVERIDGEI. & BARKER K. 1975. Acuariid, capillariid and hymenolepidid parasites of the dasyurid marsupial Antechinus stuartii Macleay, 1841, from southeastern Australia. Journal of Helminthology 49: 21 l-227. BEVERIDGEI. & BARKER K. 1976. The parasites of Antechinus stuartii Macleay from Powelltown, Victoria, with observations on seasonal and sex-related variations in numbers of helminths. Australian Journal of Zoology 24: 265-272. BEVERIDGEI. & ARUNDEL J. H. 1979. Helminth parasites of grey kangaroos, Macropus giganteus Shaw and M. jiiliginosus (Desmarest), in eastern Australia. Australian Wildlife Research 6: 69-77. BEVERIDGEI., PRE~~DENTE P. J. A. & SPEARER. 1985. Parasites and associated pathology of the swamp wallaby, WaNabia bicolor (Marsupialia). Journatoj~Witdtije DiseasesZl: 377-3X5.

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