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Review

Implications of wild dog ecology on the sylvatic and domestic life cycleof Neospora caninum in Australia

Jessica S. King a,e, David J. Jenkins b, John T. Ellis c, Peter Fleming d, Peter A. Windsor a, Jan Šlapeta a,*

a Faculty of Veterinary Science, University of Sydney, NSW 2006, Australiab School of Animal and Veterinary Science, Charles Sturt University, Wagga Wagga, NSW 2678, Australiac Department of Medical and Molecular Biosciences, University of Technology, Sydney, NSW 2007, Australiad Vertebrate Pest Research Unit, Industry & Investment NSW, Orange Agricultural Institute, NSW 2800, Australiae Invasive Animals Cooperative Research Centre, University of Canberra, Canberra, ACT 2601, Australia

a r t i c l e i n f o

Article history:Accepted 2 March 2010

Keywords:NeosporosisHorizontal transmissionEpidemiologyDingoFarm dogCattle

a b s t r a c t

Neospora caninum is transmitted either transplacentally or horizontally by ingestion of tissue cysts pres-ent in tissues or oocysts shed by dogs. Neosporosis is a significant disease, causing cattle abortion at 5–7 months of pregnancy. Infected cows may remain infective for life transmitting the infection in severalconsecutive or non-consecutive pregnancies. A great deal is known about the epidemiology of neospor-osis, although only limited information is available on the main routes of horizontal transmission. In Aus-tralia, the presence of the dingo as the top-order predator suggests a potential sylvatic route oftransmission between dingoes and as yet unknown native wildlife in addition to the domestic routevia dogs with access to infected tissue on farms.

This review article critically evaluates the overlap between the domestic and sylvatic routes, takinginto account canine ecology, and summarises current understanding of the transmission of N. caninumto provide a foundation for epidemiologists, farmers and conservation biologists dealing with neosporosisand wild dog control programs.

� 2010 Elsevier Ltd. All rights reserved.

Introduction

Bovine reproductive failure causes considerable economic lossto both the beef and dairy cattle industries in Australia. Incurredproduction losses include low conception rates, abortions, de-creased milk production, falls in the calving rate, weaner and calfloss, as well as increased involuntary culling of diseased animals(Fourichon et al., 2000; Maizon et al., 2004). Despite the eradica-tion of brucellosis from Australia in 1989 (Lehane, 1996), bothinfectious and non-infectious causes of bovine reproductive lossare still widespread. Common infectious diseases that causereproductive failure include campylobacteriosis (or vibriosis), tric-homonosis, leptospirosis, pestivirus, akabane and neosporosis(McGowan and Holroyd, 2008).

Surveys from several countries, including Australia, have identi-fied neosporosis caused by Neospora caninum as the leading causeof bovine reproductive failure worldwide, with up to 50% of abor-tions on farms caused by N. caninum (Anderson et al., 1995, 2000;Boulton et al., 1995; Davison et al., 1999; Trees et al., 1999; Reicheland Ellis, 2006). It has been estimated that neosporosis costs the

Australian beef and dairy industries in excess of Aus$110 million1

per annum (Reichel and Ellis, 2009).This article reviews the horizontal transmission of N. caninum

with a special focus on Australia and the potential hosts of Neos-pora in that country, both wild and domestic. There are three ques-tions that remain to be addressed experimentally: (1) What are thetransmission routes of N. caninum in Australia? (2) If a sylvatic cy-cle involving wild dogs is identified, will wild dog populationreduction programs reduce cases of cattle neosporosis? (3) If thedomestic cycle demonstrated elsewhere applies in Australia, willrefraining from feeding offal to farm dogs reduce transmission ofN. caninum to livestock? We examine the ecosystem functions ofwild dogs as top-order predators and identify their potential rolein the maintenance of cattle neosporosis in Australia.

Cattle neosporosis

A Toxoplasma-like parasite was first recognised in Norway caus-ing neurological disorders in dogs (Bjerkas et al., 1984), and in1988 it was described as a new protozoan species distinct fromToxoplasma gondii and named Neospora caninum (Dubey et al.,

1090-0233/$ - see front matter � 2010 Elsevier Ltd. All rights reserved.doi:10.1016/j.tvjl.2010.03.002

* Corresponding author. Tel.: +61 2 9351 2025; fax: +61 2 9351 7348.E-mail address: jan.slapeta@sydney.edu.au (J. Šlapeta). 1 Aus$1 = approx. £0.60, US$0.9, €0.66, at 1 March 2010.

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1988). The disease can cause clinical signs in dogs, includingascending paresis or paralysis of the hind limbs, muscle and pelviclimb atrophy, rigid hyperextension of the limb, as well as myocar-ditis, pneumonia and dermatitis (Barber and Trees, 1998; Reichelet al., 2007).

The disease in cattle was first demonstrated on a dairy farm inthe US in 1989 (Thilsted and Dubey, 1989). It has since been recog-nised as a critically important disease with a significant economicimpact worldwide, causing both epidemic and endemic abortion aswell as stillbirth in both beef and dairy cattle (Dubey et al., 2007).The complete facultative heteroxenous life cycle has been experi-mentally elucidated with the dog as the definitive host (Dubeyet al., 2002).

Once infected, cows may remain infective for life, transmittingthe infection in several consecutive or non-consecutive pregnan-cies (Trees et al., 1999; Guy et al., 2001). The primary clinical man-ifestation of infection in cattle is abortion. This is most common at5–7 months of gestation, but can happen anywhere from 3 monthsof gestation to term. Although there are no clinical signs in the in-fected dam, the outcome depends on fetal age. If the fetus dies inearly gestation it may be resorbed or mummified. However, the

most commonly observed manifestation is expulsion of a fetusshowing no gross lesions or only moderate autolysis.

If the calf is carried to term there are several potential out-comes. Most commonly it will be born clinically normal but con-genitally infected (Williams et al., 2009). Such calves willmaintain the infection in the herd, although they have an increasedrisk of abortion; Thurmond et al. (1997) reported that congenitallyinfected heifers were 7.4 times more likely to abort in their firstpregnancy than age-matched, non-infected controls. Additionally,anecdotal evidence suggests that congenitally infected calvesmay not always be clinically normal but present with varying de-grees of ataxia or other birth defects (Dubey et al., 1996). Finally,an infected dam can also give birth to a non-infected calf, thusbreaking the N. caninum life cycle (Anderson et al., 2000; Dijkstraet al., 2003; Romero and Frankena, 2003; Dubey et al., 2006).

So, the dominant transmission route of the N. caninum faculta-tive and heteroxenous life cycle is from the dam to its fetus (Wil-liams et al., 2009). However, although congenital transmissionrates can be high, the rate of transmission decreases with increas-ing parity (Wouda et al., 1998; Dijkstra et al., 2001a; Romero et al.,2002; Fioretti et al., 2003). Vertical transmission alone has been

Fig. 1. Histological presentation of neosporosis in calf. Histological tissue sections from the posterior cervical spinal cord of a neonatal calf presenting with arthrogryposisassociated with congenital neosporosis. The case was originally reported as toxoplasmosis by Hartley and Bridge (1975) but this was later revised to neosporosis by Dubeyet al. (1990). (A) Asymmetrical cord due to unilateral reduction of ventral grey and white matter (LFB-PAS, X10). (B) Intracytoplasmic location of an apicomplexan tissue cystin a neuron in the ventral grey matter (HE, X100). (C) Confirmation of a neuronal tissue cyst as N caninum by positive immunohistochemistry (Immunoperoxidase, X200).Images taken from ‘OLIVER’ database at the University of Sydney and contributed by Dr. W.J. Hartley.

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shown to be insufficient to sustain the infection in a herd, withmathematical models indicating a range of vertical transmissionprobabilities within herds of 41–95% (Davison et al., 1999; Frenchet al., 1999; Pan et al., 2004). Because vertical transmission cannotsustain N. caninum in cattle, a point source exposure of cattle to N.caninum oocysts (i.e. horizontal transmission) has been implicatedin the production of abortion storms because of acute synchronoustransplacental transmission (McAllister et al., 2000; Dijkstra et al.,2001a).

The disease has been identified in both dairy and beef cattle butit is most commonly diagnosed in the dairy industry. This is mostlikely due to sampling bias, as it is routine practice within a dairyherd to pregnancy test the herd and therefore disease and abortionmay be more readily diagnosed in contrast to beef cattle wherepregnancy may not be monitored. Although N. caninum is a rela-tively newly recognised disease, it is quite clear that it was previ-ously misdiagnosed in Australia as sarcocystosis in cattle (Boultonet al., 1995). Retrospectively, the earliest identification of neospor-osis was in a stillborn lamb and calf from New South Wales in 1974(Fig. 1; Hartley and Bridge, 1975; Dubey et al., 1990).

Life cycle and epidemiology

Neosporosis consists of three principle infectious stages ofdevelopment (tachyzoites, bradyzoites within tissue cysts and oo-

cysts containing sporozoites). Asexual development occurs withinan intermediate host, such as cattle, whereas sexual reproductionoccurs within a definitive host (a canid such as a dingo). The asex-ual stages of N. caninum consist of fast replicating tachyzoites andslowly dividing bradyzoites. During an acute phase of neosporosis,the tachyzoites may be found in virtually all host tissues and fluids,including the blood of the dam and the fetus as well as the placentaand amniotic fluids of pregnant cows (Davison et al., 1999; Buxtonet al., 2002; Larson and Hardin, 2003; McInnes et al., 2006b). In theneural cells, tachyzoites may differentiate into bradyzoites follow-ing the onset of a strong immune response against the protozoan,resulting in the formation of tissue cysts (Peters et al., 2001). Thebradyzoites remain within the tissue cysts until reactivation occursas a result of changes to the immune system of the intermediatehost, most often as a result of pregnancy or the presence of otherinfectious agents, such as bovine viral diarrhoea virus (Buxtonet al., 2002; Quinn et al., 2004; Ortega-Mora et al., 2006). Verticaltransmission occurs when an infected dam of the intermediatehost transfers tachyzoites through the blood stream to its fetus(Dubey et al., 2007).

In Australia, vertical transmission was found to be the majorsource of infection (74%) in a herd, with postnatal horizontal trans-mission (seropositive calf from seronegative dam) accounting foronly 15% of seropositive calves (Atkinson et al., 2000; Landmannet al., 2002; Hall et al., 2005). Horizontal transmission occurs after

Fig. 2. Hypothetical transmission routes of Neospora caninum in Australia. The proposed life cycle of N. caninum shows the domestic route (blue circle) and the proposedsylvatic route (green circle). The domestic route involves vertical transmission in which the main route of infection (red arrows) from the intermediate host (cow) to itsoffspring results in the birth of congenitally infected calves. Alternatively the intermediate host can give birth to a non-infected calf which breaks the cycle or it can abort itscalf. Infected fetal material can be eaten by the domestic dog (domestic route) or dingo (sylvatic route) and result in horizontal transmission. Both animals have been definedas definitive hosts of N. caninum and are capable of shedding oocysts which may contaminate food and water of the intermediate host. The proposed sylvatic route involvesdingoes or wild dogs either defecating on wildlife pasture and subsequently infecting wildlife or consuming potentially-infected wildlife tissue. The overlap between the twocycles could occur when domestic dogs are fed potentially-infected wildlife tissue or the dingo excretes in faeces infective oocysts onto feed or water of livestock. However,the extent of the overlap between the domestic and the sylvatic routes is yet to be investigated in Australia.

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a definitive host consumes infected host tissue such as fetal mem-branes. Environmentally resistant oocysts are subsequently ex-pelled in the faeces and sporulate to form infective N. caninumoocysts (Dijkstra et al., 2001a; Dubey et al., 2002). It is unclearhow long these sporulated oocysts can survive within the environ-ment, but oocysts of the closely related T. gondii can remain viablefor 200 days at 25 �C (Dubey, 1998). Horizontal transmissionthrough accidental ingestion of feed or water contaminated withcanid faeces is thought to be the principal way in which interme-diate hosts become infected (Fig. 2). After ingestion, the oocysts re-lease sporozoites into the intestinal tract of the intermediate host,and initiate an acute neosporosis, potentially resulting in abortion(Barling et al., 2000; Gondim et al., 2004a; Williams and Trees,2006; Williams et al., 2009).

Domestic dogs (Canis lupus familiaris) and coyotes (Canis latrans)are known to be definitive hosts for N. caninum through the exper-imental demonstration of a transient period of oocyst productionfollowing ingestion of infected mouse or calf tissue (McAllisteret al., 1998; Lindsay et al., 1999; Gondim et al., 2004c). Impor-tantly, dogs are known to shed only low numbers of oocysts, withexcretion commencing 5 days or more after ingestion of infectedmaterial. This oocyst shedding has been shown to last from 1 to27 days (McAllister et al., 1998; Lindsay et al., 1999; Dijkstraet al., 2001b). However, on one occasion oocysts of N. caninumwere found in dog faeces 4 months apart (McGarry et al., 2003).This foxhound was presumed to have been fed carcases of animalsthat died or were unfit for human consumption and it is unknownif it had been continually shedding oocysts, started to shed afterreactivation of the existing infection or re-shed the oocysts dueto re-infection (McGarry et al., 2003).

Re-shedding of oocysts may be more important than previouslythought in the epidemiology of neosporosis through increasingcontamination of the environment with oocysts (McGarry et al.,2003; Dubey et al., 2007; Reichel et al., 2007). We are unawareof any other reports of prolonged or repeated shedding of N. cani-num oocysts but in the very closely related parasite, T. gondii, re-shedding of oocysts has been experimentally documented. Dubey(1976, 1978) showed that super-infection of chronically infectedcats with Cystoisospora spp. led to re-shedding of T. gondii oocysts,but that infection with the Mycobacterium tuberculosis BCG straindid not. Nevertheless, this phenomenon of re-shedding of T. gondiihas not attracted further experimental attention and cats are con-sidered to shed oocysts only once in their lifetime (Dubey, 1986).

Farm dogs as a potential risk factor for cattle neosporosis

Domestic dogs are known to be a definitive host of N. caninumand the presence of farm dogs has been suggested to impact onN. caninum prevalence (McAllister et al., 1998). Numerous epide-miological studies from around the world support this claim sincethere is an association between the presence of domestic dogs andthe incidence of neosporosis on cattle farms (Sawada et al., 1998;Wouda et al., 1999; Basso et al., 2001; Moore et al., 2002; Otrantoet al., 2003; Schares et al., 2004; Hobson et al., 2005; Wanha et al.,2005; Bartels et al., 2007; Malmasi et al., 2007; Collantes-Fernan-dez et al., 2008). Other workers have not found such a correlation(Barling et al., 2000; Rodriguez et al., 2002; Fischer et al., 2003).

The role of dogs in the epidemiology of neosporosis is stronglysupported by studies including those from The Netherlands, whereit was found that a significantly greater population of seropositivedogs were present in rural populations (36/152; 23.6%), comparedto those tested in urban areas (19/344; 5.5%) (Wouda et al., 1999).The presence of N. caninum-seropositive rural dogs also stronglycorrelated with a high prevalence of N. caninum antibodies in cattleon their respective farms (Wouda et al., 1999). Studies have re-ported N. caninum-seroprevalence in rural dogs on beef and dairy

farms to be as high as 51% (51/100) (Collantes-Fernandez et al.,2008). In urban dogs, the highest seroprevalence of N. caninumwas 26.2% (42/160) (Basso et al., 2001).

Another risk factor attributed to N. caninum infection in cattle isthe number of dogs present on or around a property. A Dutch studyshowed that the probability of herds being seropositive was 5.5%higher on farms with dogs than that of herds with no farm dogs(2.3%) (Bartels et al., 2007). Furthermore, herds on farms withtwo or more dogs were found to have higher seroprevalence thanherds on farms with no or one dog (Otranto et al., 2003). In Ger-many, Schares et al. (2004) found that not only the number of dogson a farm, but also the density of dogs in the municipality of thefarm were significant risk factors for N. caninum infection.

The higher prevalence of seropositive dogs in rural areas com-pared to urban populations could be related to increased accessto potentially infected tissues from cattle (including offal) and toother possible intermediate hosts, such as small mammals andbirds. This and the fact that it is possible to identify seropositivecattle on farms where no domestic dogs are present, suggests thatthere may be sources of infection other than the dog, indicatingthat a sylvatic life cycle may be involved in disease transmission(Wouda et al., 1999).

However not all studies have shown this link with dogs. Rodri-guez et al. (2002) used a questionnaire to assess the abortion his-tory of dairy and beef herds and exposure to N. caninum from 4907cows from 98 herds across 20 US States and Puerto Rico. Evaluationof N. caninum cattle prevalence data against the number of dogs on

Fig. 3. Cattle and wild dog distribution on mainland Australia. (A) Distribution ofbeef cattle (light grey), and dairy and beef cattle (dark grey) on mainland Australia.(B) Distribution of wild dogs (grey). Maps of Australia are shown without Tasmania.The distribution of cattle and dogs is based on Australian Bureau of Statistics (2006)and West (2008).

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Table 1Neospora caninum seroprevalence and molecular identification studies in Australia.

Location Host N. caninum prevalence (percentage),technique(s)

Comments and references

New South WalesAborted calf fetuses 152/729 (21%), histology/IHC Review of abortion cases in north-eastern New South

Wales from 1982 to 1994 (Boulton et al., 1995)Affected herdsDairy 74/126 (59%), histology/IHCBeef 52/126 (41%), histology/IHC

Domestic dogs 18/150 (12%), serology (IFAT) Australia - wide seroprevalence study (Barber et al.,1997)Dingoes 1/117 (0.9%), serology (IFAT)

Dairy cows Seroprevalence investigation 1 month after an abortionoutbreak in dairy herd in New South Wales (Atkinsonet al., 2000)

Whole herd 83/266 (31%), serology (IFAT/immunoblot)Aborting 59/63 (86%), serology (IFAT/immunoblot)Non-aborting 50/164 (30%), serology (IFAT/immunoblot)

Dairy calf Single calf, histology, culture and PCR Isolation of N. caninum Nc Nowra strain from brain andspinal cord of congenitally infected dairy calf in NewSouth Wales (Miller et al., 2002)

Dairy herd Investigation into an abortion outbreak on a dairy farmwith 40/170 (24%) abortions over 20 months (Quinnet al., 2004).

Cattle 20/183 (11%), serology (IDEXX ELISA)Aborting 11/39 (28%), serology (IDEXX ELISA)

Dairy cows Association study using two bleeds 12 months apart of asingle dairy herd and four dogs on the property in NewSouth Wales (Hall et al., 2005); 25/27 cattle wereselectively culled, 12 months later only one newseroconversion occurred.

First bleed 27/266 (10%), serology (ELISA, Institut Pourquier)Second bleed 16/207 (8%), serology (ELISA, Institut Pourquier)

Farm dogs 1/4 (25%), serology (IFAT)

Dairy cows 84/398 (21%), milk (ELISA, Institut Pourquier) Seroprevalence on 203 dairy farms across New SouthWales (Hall et al., 2006)69/198 (35%), serology (ELISA IDEXX)

Beef cattle Seroprevalence study from beef cattle across New SouthWales (Moloney and Kirkland, 2006)Cattle 136/3111 (5.4%), serology

Herd 36/59 (60.4%), serology (in-house ELISA by EMAI)

Brushtail Possums 0/142 (0%), serology (MAT) Seroprevalence into an urban population of the BrushtailPossum in New South Wales (Eymann et al., 2006)

Feral mice 28/104 (27%), PCR Prevalence in farm mice using nested PCR (Barratt et al.,2008)

Sheep Investigation into a suspected neurological neosporosisand seroprevalence survey in New South Wales (Bishopet al., 2010)

Dead sheep Single sheep, PCR, histology, IHCSheep 0/184 (0%), serology (ELISA IDEXX)

5/232 (2.2%), serology (ELISA VMRD)

White rhinocerosfetus

Aborted fetus, histology, IHC, PCR Investigation into an abortion of a fetus of the SouthernWhite Rhinoceros at the Taronga Western Plains Zoo(Sangster et al., submitted for publication)

Queensland

Dingoes 14/52 (27%), serology (IFAT) Australia wide seroprevalence study (Barber et al., 1997)

Dairy cows herd 45/186 (24%), serology (IFAT) Seroprevalence study in south east Queensland dairyherd with 100% rate of vertical transmission (Landmannet al., 2002)

Beef cattle and herds Seroprevalence study in central Queensland showingincreasing seroprevalence with age (Stoessel et al., 2003)Cattle 249/1673 (14.9%), serology (IFAT)

Individualproperty

38/40 (95%)

Beef cattle Seroprevalence study across beef cattle in Queensland(Taylor and Landmann, 2003), results include previousdata (Stoessel et al., 2003)

Cattle 858/5785 (14.8%), serology (IFAT)Individual

property139/154 (90.3%)

Western Australia

Domestic dogs 13/94 (14%), serology (IFAT) Isolation of N. caninum WA-K9 strain from a skin lesionof a dog and seroprevalence from urban dogs in WesternAustralia (McInnes et al., 2006a)

Single dog, culture and PCR

Pregnant beef cows Abattoir study of dams and their fetuses and two beefherds from Western Australia (McInnes et al., 2006b)Dam 1/79 (4%), PCR on serum

1/79 (0%), serology (IFAT)Fetus 11/79 (14%), PCR on tissue

0/79 (0%), serology (IFAT)Two beef herds 1/30 (3%), serology (IFAT)

0/30 (0%), PCR on sera (PCR)Dams that aborted 23/23 (100%), serology (IFAT)

12/23 (52%), PCR on serum

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the farm suggested that presence of dogs did not increase the riskof exposure of cows to N. caninum. Barling et al. (2001), based onthe results of an epidemiological study of 760 calves from 76 Texasranches, suggested that the presence of cattle-working dogs pre-vented other canids from entering the property and contaminatingfeed and water sources. In that study, calves had a lower preva-lence of N. caninum antibodies on farms where cattle-working dogswere used.

Neospora caninum and cattle neosporosis in Australia

The cattle industry is one of Australia’s major agriculturalindustries, with a total of 28.8 million dairy and beef cows re-corded in Australia in 2006 (Australian Bureau of Statistics,2008). Dairy cattle are restricted mainly to southern and coastaldistricts of Australia, with 83% of Australia’s dairy herds distributedalong the east coast of Australia (Fig. 3A). Similarly nearly 70% ofthe beef cattle herd are concentrated in eastern Australia. Cattleneosporosis research in Australia has been particularly focussedon the cattle industries in New South Wales and Queensland de-spite 61% of the dairy industry being located in Victoria (Table 1).

State-wide seroprevalence studies of N. caninum have found asmany as 21% of dairy cattle from 198 farms and 5.4% of beef cattlefrom 59 farms across New South Wales to be seropositive (Hallet al., 2006; Moloney and Kirkland, 2006). Queensland data arelimited to beef cattle with an estimated 15% of animals found tobe seropositive (Stoessel et al., 2003). These studies also found ahigh herd level prevalence with 35% of tested dairy herds and60% of beef herds containing at least one seropositive animal inNew South Wales, and 95% of beef herds in Queensland (Stoesselet al., 2003; Hall et al., 2006; Moloney and Kirkland, 2006).

The only known Australian cattle-associated strain of N. cani-num (Nc Nowra) was isolated from the brain and spinal cord of acongenitally infected calf from the south-east coast of New SouthWales (Miller et al., 2002). The only other isolate (WA-K9) fromAustralia was isolated from a naturally infected dog in WesternAustralia, which is genetically distinct at multiple DNA loci to NcNowra and its infectivity to cattle is unknown (McInnes et al.,2006a; Al-Qassab et al., 2009).

Australian dingoes and wild dogs as a likely component of theNeospora caninum life cycle

Serology data revealed that 0.9% (1/117) of dingoes in NewSouth Wales and 27% (14/52) of dingoes in Queensland had N. cani-num antibodies in their serum (Barber et al., 1997). This finding,coupled with the existing knowledge that domestic dogs are defin-

itive hosts of N. caninum and reports that presence of dogs on farmscorrelated with high N. caninum seroprevalence in cattle, fuelledthe argument as to the necessity of controlling wild dogs, includingdingoes, because of their assumed role in disease transmission.However, no existing scientific evidence suggests that control ofdingoes will control neosporosis.

Recently, we experimentally addressed the ability of dingoes toserve as a definitive host of N. caninum (Fig. 4, King et al., 2010).These data represent the first step towards a comprehensiveunderstanding of the role of dingoes in the epidemiology of neo-sporosis in Australia. To further evaluate and resolve the assump-tion that dingoes are a key factor in cattle neosporosis one needsto consider the ecology of the dingo which is distinct in many waysfrom domestic dogs.

The Australian dingo, Canis lupus dingo, is the top-order preda-tor in Australia (Glen et al., 2007). In legislation, the dingo is con-sidered an Australian native animal, despite it being brought toAustralia from South-East Asia 3500–5000 years ago (Corbett,1995; Savolainen et al., 2004). However, today, dingoes are oftenincorporated under the term ‘wild dog’, which refers to the dingo,domestic dogs and their hybrids and reflects the difficulty of deter-mining pure dingoes from phenotypes in the field. The interbreed-ing of dingoes with domestic dogs threatens the dingo gene pool tothe extent that pure Australian dingoes are almost non-existent insouth-eastern Australia (Claridge and Hunt, 2008). Wild dogs areestimated to inhabit around 82.8% of Australia (6.3 million km2),being dispersed over most of mainland Australia, excluding thesheep-wheat belt in south-eastern Australia (Fleming et al., 2006;West, 2008) (Fig. 3B).

Wild dogs are declared a pest on agricultural lands in NewSouth Wales (under the Rural Lands Protection Act 1998) and inmost other states in Australia because of their impact on livestock,with wild canids estimated to cost livestock industries approxi-mately Aus$66 million per annum in production losses andassociated control expenses (McLeod, 2004). A recent report by‘Blueprint for the Bush’ and AGFORCE in Queensland indicates thatwild dogs cost Aus$67 million per annum, including an assumedAus$3.14 million due to N. caninum in cattle (Hewitt, 2009).However, management of wild dogs is a controversial topicbecause the dingo is considered by many in Australia as a nativeand iconic species.

Are dingoes and other wild dogs increasing the risk of cattleneosporosis?

Outside Australia, N. caninum has been identified in a variety ofwild animals. In North America white-tailed deer (Odocoileus

Table 1 (continued)

Location Host N. caninum prevalence (percentage),technique(s)

Comments and references

Victoria

Domestic dogs 11/207 (5%), serology (IFAT) Australia - wide seroprevalence study (Barber et al.,1997)

Tasmania

Dairy herd abortion Report of an outbreak of abortion over three consecutiveyears in a dairy herd in Tasmania with further review ofdairy and beef abortions during 1987–1995 (Obendorfet al., 1995).

Fetuses 3/11 (27%), IHCDairy and beefabortedFetuses from herds(1987–1995)

6/9 (33%), IHC

IFAT, immunofluorescence antibody test; ELISA, enzyme-linked immunosorbent assay; MAT, modified agglutination test; IHC, immunohistochemistry; PCR, polymerase chainreaction; EMAI, Elizabeth Macarthur Agricultural Institute, Menangle, New South Wales.

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virginianus) has been identified as an intermediate host and thecoyote (Canis latrans) as a definitive host, suggesting that a sylvaticcycle may play a role in the epidemiology of N. caninum (Gondimet al., 2004b; Vianna et al., 2005). The existence of this life cyclesuggests that the natural prey (white-tailed deer) of the predator(coyote) is the most likely source of infection for the wild definitivehost rather than domestic animals or livestock.

In Australia, wild dogs, including dingoes, have flexible behav-iours that enable them to survive well either commensally withhumans or completely remote from them (Corbett, 1995). Thebehavioural ecology of the dingo is in many ways similar tothe coyote and less similar to the wolf (Canis lupus), from whichthe dingo is descended (Savolainen et al., 2004). Wild dogs are gen-eralist carnivores that can change their hunting strategy to enablepredation on a wide range of prey (Corbett, 1995; Fleming et al.,2006). Whereas a single wild dog can easily prey on rabbits (Oryc-tolagus cunniculus), wallabies (Macropodoididae), sheep and new-born calves, groups are formed to attack larger prey such askangaroos (Macropus spp.) and older cattle (Thomson, 1992; Cor-bett, 1995; Allen and Fleming, 2004). Thus, when assessingwhether wild dogs play a substantial role in the transmission ofN. caninum to livestock, the existence of a sylvatic life cycle needsto be considered and conditions that may promote the overlap ofthe sylvatic and domestic life cycles investigated (Fig. 2).

Both livestock and wild dogs are free-ranging and their distribu-tions overlap with each other and with native and feral herbivores(Strahan, 1995; Allen and Sparkes, 2001; West, 2008). However,the use of habitats by wild dogs is heterogeneous, with huntingand travelling routes favoured (Meek, 1999; Claridge et al.,2009). Wild dogs defaecate in areas where they hunt and eat bothnative herbivores and livestock, and areas of common use couldprovide the route of N. caninum infection. However, this partiallysylvatic cycle requires continued interactions between cattle andpasture contaminated by infectious wild dog faeces to instigateinfection of clean herds. An entirely sylvatic cycle would requirethe involvement of Australian native herbivores to ensure cyclingof N. caninum in wild dog populations (Fig. 2).

Where wild dogs occur, medium- and large-sized macropodsand possums are their preferred prey, with known regional differ-ences influenced by the availability and the abundance of prey spe-cies (Thomson, 1992; Corbett, 1995). A plausible sylvatic life cyclecould be occurring between wild dogs (including dingoes) andtheir macropod prey. However, we currently do not know whichspecies of macropod are likely to be intermediate hosts. Seroprev-alence and DNA analysis for N. caninum would have to be con-ducted on these animals before any firm conclusions could bedrawn. Feral mice around farms in eastern Australia have been

shown to be a plausible intermediate host of N. caninum throughthe demonstration of N. caninum DNA in tissue (Barratt et al.,2008). However, the importance of small rodents in wild dog dietsvaries with season and region (Newsome et al., 1983; Robertshawand Harden, 1985), leading to the conclusion that feral mice on thefarm may be contributing to the domestic route sustained by farmdogs.

Because wild dogs can prey on livestock, they are persecutedover much of the continent (McLeod, 2004; Fleming et al., 2006).Wild dog control programs are aimed at reducing or locally elimi-nating the dog populations to reduce livestock losses and to im-prove livestock welfare (Allen and Sparkes, 2001; Fleming et al.,2006; Hewitt, 2009). It is yet unknown, if in areas where control ef-forts have substantially reduced wild dog abundance (e.g. Thom-son, 1984), there is a correlation with reduced horizontaltransmission of N. caninum to domestic cattle, and reduced overlapof the domestic and sylvatic cycles (Fig. 2).

However, wild dog control is not always successful (e.g. El-dridge et al., 2000) and it has been suggested that under certainconditions these control attempts might lead to increased numbersof wild dogs (Allen, 2005) and disruption of the natural sylvatic lifecycle of N. caninum, increasing the overlap between the domesticand sylvatic routes of N. caninum transmission (Fig. 2).

Australian dingoes often belong to highly structured packs,essentially extended families in which there is a hierarchy (Cor-bett, 1995; Fleming et al., 2006). Partial control of dingo popula-tions has been linked to increased calf losses in centralQueensland (Allen and Fleming, 2004). Allen (2005) postulatedthat a breakdown of pack structure facilitated increased calf preda-tion by younger subordinate dogs. When comparing an area wheredingo control occurred compared to an area where no control waspracticed, the annual predation losses in calves increased in boththe frequency of killings and the percentage of calves killed by wilddogs in the controlled area (Allen, 2005). If this is true, then ineffec-tive wild dog control programs may foster undesirable impacts onlivestock by predation and consequently promote mixing of thesylvatic and domestic sides of the N. caninum life cycle.

The domestic route of parasite life cycles maintained byAustralian farm dogs

Within Australia, we suggest that a sylvatic and a domesticroute of transmission are involved in the life cycle of N. caninum.This predator and prey interaction is paralleled in Australia bythe parasite Echinococcus granulosus, the causative agent of hydatiddisease (Jenkins, 2006). Similar to N. caninum, the definitive hostfor E. granulosus are canids (both wild and domestic dogs) and a

offalCOW1 COW2 COW3

COW4 COW5 COW6

N. caninum (Nc Nowra) control

DINGO1 DINGO2 DINGO3 CONTROL

DOG1 DOG2 DOG3 CONTROL

COW1 COW2 COW4/5 COW3/6

Fig. 4. Experimental transmission trial identifying dingoes as definitive hosts of N. caninum. Four dairy bull calves and two control calves were intravenously infected withtachyzoites from the Australian isolate of N. caninum (Nc Nowra). Calves were deemed infected through detection of N. caninum antibodies in their serum (ELISA) and N.caninum DNA in their blood (PCR). Thirteen weeks post infection, calves were euthanised and their offal was fed to three dingo pups and a control and three domestic dogpups and a control. Faecal samples of all dingoes and dogs were collected daily and examined microscopically for the presence of N. caninum-like oocysts by a standardflotation technique using saturated sodium chloride. Twelve days post infection, dingo 3 started excreting N. caninum-like oocysts which were confirmed to be N. caninumoocysts through PCR and sequencing (King et al., 2010).

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domestic route is maintained through dogs consuming tissue frominfected farm animals, while a sylvatic route is maintained by wilddogs preying on native marsupials. The dogs defaecate infectivestages of E. granulosus onto pasture and feed of farm animals,and in turn transmit the disease to livestock (Jenkins, 2006). Thisis largely facilitated by the ease of access farm dogs have to poten-tially infected material.

Farm dogs are commonly fed offal and raw animal tissue in Aus-tralia. A hydatid survey presented to rural dog owners in NewSouth Wales revealed that 64% of farmers interviewed fed theirdogs on raw animal carcasses of home slaughtered animals(including sheep and cattle) and wild animal meat (including kan-garoo, feral pig, rabbits and feral goats) which are all potentialsources of both E. granulosus and N. caninum (Jenkins, 2006). Thesame survey in Victoria indicated that 95% of farmers fed theirdomestic dogs raw meat and 21% admitted to feeding offal (Jen-kins, 2006). A study conducted in Hungary observed that farm dogsthat were seropositive to N. caninum often ate aborted or deadcalves or consumed raw offal of game animals including deer(Hornok et al., 2006). Thus it is likely that, in Australia, offal feedingof farm dogs is the pendulum that maintains N. caninum on farmsvia the domestic route.

The recent findings that birds, specifically chickens, can be nat-ural intermediate hosts of neosporosis has prompted questions asto whether birds may be another reservoir host for wild dogs(Costa et al., 2008). However, birds are known to only make up asmall proportion of wild dogs diets in eastern Australia (Newsomeet al., 1983; Robertshaw and Harden, 1985). The prevalence of N.caninum in birds is unknown in Australia. Genotyping using micro-satellite markers is an emerging field that has the potential to mapthe epidemiology of N. caninum genotypes (Al-Qassab et al., 2009;Sangster et al., submitted for publication). Moreover, this technol-ogy has the ability to discern if any biological differences can belinked to these markers, including the sylvatic and domestic originof N. caninum isolates or clinical samples.

Conclusions

Intermediate hosts infected with N. caninum remain infectiousfor life. The parasite is transmitted to a new host either transpla-centally in utero or the intermediate host falls victim to a predator– the definitive host. Consumption of infective tissue by the defin-itive host is followed by a short period of oocyst shedding but so farit remains unknown whether that same host is then refractory tonew infection or production of N. caninum oocysts.

Undeniably, horizontal transmission plays an essential role inthe maintenance of N. caninum on a farm. We predict that thedomestic route, where the farm dog is the source of horizontalinfection to livestock, predominates as farm dogs are likely to bemore efficient vectors than wild dogs because of greater probabil-ity of infectious contact on farm (Fig. 2). We also predict the pres-ence of a sylvatic route, very similar to that of E. granulosus, wherewild canids are the source of infection to their natural prey, whichis important for disease maintenance, and where infection of cattleis secondary.

It is unethical to shoot wild dogs based on a scientificallyunsubstantiated argument that dingoes may be associated withtransmission of cattle neosporosis. Their ability to produce the par-asite does not directly lead to a conclusion that they are an impor-tant route in the transmission of N. caninum to livestock inAustralia. We need to know whether undisturbed wild dogs or dis-turbed wild dogs pose a greater risk than the presence of domesticdogs on farms in Australia. Only then will development of effectivefarm-management practices for the control of N. caninum on cattlefarms be possible, taking into account the importance of thedomestic and sylvatic routes of the parasite transmission.

Conflict of interest statement

None of the authors of this paper has a financial or personalrelationship with other people or organisations that could inappro-priately influence or bias the content of the paper.

Acknowledgements

The authors would like to thank the Invasive Animals Coopera-tive Research Centre, the Dr. William Richards Award in VeterinaryPathology (University of Sydney), The University of Sydney and TheUniversity of Technology, Sydney for support.

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