A review of viral and parasitic infections in wild deer in Australia with relevance to livestock and human health

Introduction

Multiple infectious diseases, including avian influenza virus, African swine fever virus and coronaviruses have emerged or re-emerged in recent decades, raising questions about their pathogenesis and epidemiology (Rhyan and Spraker 2010; Barroso et al. 2021; McClymont et al. 2022). Wildlife populations are the most significant source of emergent infectious diseases that impact human health, biodiversity, and agriculture (Morner et al. 2002). As a result, pathogen transmission between wildlife and livestock is a global concern (Rhyan and Spraker 2010). Of particular importance in wildlife health are pathogens that do not exhibit host specificity or can infect host species across different taxa. In this context, it is estimated that 77% of pathogens detected in livestock can infect multiple wild and domestic species (Woolhouse et al. 2001), and can therefore be acquired by other species. Wild animals typically carry more pathogens than are present in domestic animals (Walker et al. 2017), and some of these pathogens do not need to persist for an extended period within a wildlife population for transmission to livestock to occur (Morgan et al. 2006).

Due to altered landscapes or the introduction of non-native species, changes in wildlife density and habitat use lead to new interfaces between livestock and wildlife, potentially exacerbating processes that promote pathogen transmission (Rhyan and Spraker 2010; Miller et al. 2013). Because cervids (Family Cervidae) are ruminants and closely related to economically important livestock species such as cattle, sheep, and goats, it is not surprising that they share many pathogens, including several of major agricultural significance. Here, we focus on the role of wild deer as wildlife hosts of viral and parasitic pathogens in Australia. The role of wild deer as a source of infection for livestock has been widely studied in Europe and North America, where wildlife–livestock interactions have increased (Böhm et al. 2007; Conner et al. 2008; Martin et al. 2011; Ruiz-Fons et al. 2014).

Deer are not native to Australia and were first introduced in the early 19th century from Europe and Asia (Bentley 1998; Hall and Gill 2005). Six species – chital (Axis axis), fallow (Dama dama), hog (Axis porcinus), red (Cervus elaphus), rusa (Cervus timorensis), and sambar (Cervus unicolor) deer – have established self-sustaining wild herds in Australian habitats (Bentley 1998; Moriarty 2004a). Wild deer are present in all Australian states and territories, but are most widespread and abundant in Tasmania, Victoria, New South Wales, and the Australian Capital Territory (Forsyth et al. 2015; Davis et al. 2016; Forsyth et al. 2016; Crittle and Millynn 2020). For approximate current and potential distributions of the six species of wild deer in Australia, see fig. 2 in Davis et al. (2016). Wild deer populations continue to increase in size and distribution in mainland Australia and Tasmania (Moriarty 2004a; Davis et al. 2016; Cunningham et al. 2022). Wild deer are particularly widespread and abundant in south-eastern Australia, where population densities of up to 39 per km² occur in agricultural landscapes (Bengsen et al. 2022). Bioclimatic modelling, which matches animal species’ requirements to suitable environments, suggests that deer currently occupy a small proportion of their potential distribution in Australia (Moriarty 2004a; Davis et al. 2016).

Australia is currently free of many animal pathogens detected elsewhere in the world, such as those causing Foot and Mouth Disease or Lumpy Skin Disease, and exotic diseases remain a major threat to Australia’s livestock industry as well as to human and wildlife health. Therefore, ongoing monitoring to determine the presence of pathogens in wildlife is crucial to identifying potential reservoirs of infectious diseases and preventing future disease outbreaks. Wild deer populations currently pose a disease risk (Fig. 1), and further increases in size and distribution could increase that risk. However, data about the infection status of Australian wild deer populations are sparse, with only six studies reported before 2014, all of them identified in localised surveys conducted 41–56 years ago (Munday 1966; Munday 1972; Presidente and Westbury 1979; Slee and Presidente 1981; English 1982; McKenzie et al. 1985). More recently, however, at least 11 further surveys have been reported, many of them our own work (Davies 2014; Koehler et al. 2016; Panozzo 2018; Huaman et al. 2020, 2021a, 2021b, 2021c, 2022a, 2022b; Jenkins et al. 2020; Lamb et al. 2021).

Fig. 1.

A farm paddock in Victoria, Australia. Note the presence of deer scats in the foreground and domestic animals (horses) in the background.

Here, we provide an updated assessment of the prevalence of both viral and parasitic infections in wild deer in Australia. We conducted this assessment by searching the PubMed database using the keywords ‘Deer’, ‘Australia’ and ‘Disease’; ‘Deer’, ‘Australia’ and ‘Pathogen’, or ‘Deer’, ‘Australia’, and ‘Parasite’ (in the title and abstract) and inspecting the references in the publications identified in this literature search. Our search was conducted on 02 December 2022. We also highlight how advanced genomic techniques have increased our understanding of wild deer diseases. In this present review we aimed to: (1) review current knowledge of deer infection in Australia; (2) examine how this compares to deer overseas; and (3) assess the implications for wild and domestic animal populations and humans.

Viral diseases in deer

Viral infections of deer have been examined across multiple decades in Australia. All six deer species have been assessed for various viral infections; however, most data are available for fallow deer. The first study of diseases in Australia’s wild deer was published in 1966 (Munday 1966) and assessed fallow deer in Tasmania for the presence of Bovine Herpesvirus (BoHV-1) and Pestivirus. BoHV-1 causes two clinical diseases in cattle: infectious bovine rhinotracheitis and infectious pustular vulvovaginitis. The prevalence of antibodies to BoHV-1 in adult cattle in Australia is typically 25–40%, with the virus occurring across the continent but being particularly associated with feedlots (Gu and Kirkland 2008). No BoHV-1 was detected in the survey of Munday (1966), or in other surveys of small areas and a more recent study across large areas of eastern Australia (Table 1). These findings suggest that Australian deer are not carriers of BoHV-1, despite the moderate prevalence levels in livestock and the extensive sharing of pastoral habitats by cattle and wild deer across Australia (Gu and Kirkland 2008). Multiple deer species have been experimentally infected with BoHV-1 (Chow and Davis 1964; Mollema et al. 2005). Bovine Herpesvirus has also been detected serologically in deer in Poland (<5% prevalence) and Hungary (12–47% prevalence via PCR detection and subsequent sequencing) (Kalman and Egyed 2005; Fabisiak et al. 2018). All studies involving Australian deer were conducted using serological tests, and it may be that this detection method is less sensitive than PCR, but further work is needed to confirm this.

Pestivirus infection is widespread in Australian cattle, causing the clinical disease Bovine Viral Diarrhoea (Reichel 2000; Scharnbock et al. 2018). Studies of Pestivirus exposure in deer species in Australia have been conducted across small geographical areas, with more recent studies encompassing larger land areas (Table 1). All these studies have found variable but low prevalence. Seropositive fallow deer were first reported in a small study in Tasmania with a prevalence of 14.5% (11/76 deer) (Munday 1966), and a decade later in another small study in NSW with a prevalence of 1.2% (1/86) (English 1982).

A larger study assessing Pestivirus prevalence in red deer sourced from 20 localities in eastern Australia in 1985 reported 4% prevalence (McKenzie et al. 1985). Recently, a study sourcing five deer species from locations in eastern Australia reported a similar prevalence of 3% (13/432) for Pestivirus antibodies (Huaman et al. 2020). These findings are consistent with the low seroprevalence of deer species globally for Pestivirus (reviewed in Passler et al. 2016). In addition, Australian cattle exhibit high seropositive rates (53%) (Scharnbock et al. 2018), but deer experimentally infected with Pestivirus have a low ability to shed the virus or display clinical symptoms (reviewed in (Passler et al. 2016)). Therefore, deer seem to be a spill-over end-host for Pestivirus and seldom able to transmit the virus to cattle.

Many significant viral infections of Australian livestock are carried by mosquitoes, termed arboviruses. Because arboviruses are vector-borne viruses, their occurrence is mainly driven by the effects of temperature and rainfall. There are distinct seasonal geographical changes in the incidence of important livestock-associated arboviruses (Geoghegan et al. 2014). Four agriculturally significant arboviruses have been detected in Australian deer: Bluetongue virus; Akabane virus; BEFV (Bovine Ephemeral Fever Virus); and EHDV (Epizoootic Hemorrhagic Disease Virus) (Table 1). Most of these observations have come from one large study of wild deer conducted across Queensland in 1985, in which 43% of deer were seropositive for BEFV, 19−50% seropositive for one of five strains of EHDV, and 13% seropositive for Akabane virus (McKenzie et al. 1985). Similar results were reported in a small study conducted in NSW in 2004, with rusa deer seropositive for Akabane virus and EHDV. More recently, a large-scale PCR-based screening study of deer blood samples collected from eastern Australia revealed no infection for a range of vector-borne diseases including BEFV, EHDV and Akabane (Huaman et al. 2020, 2021a). However, considering (1) endemicity of these pathogens in eastern Australia, (2) the presence of suitable vectors, and (3) expected increases in the distribution and abundance of deer (in the absence of substantial control efforts) (Davis et al. 2016; Cunningham et al. 2022), the possibility that deer species could be a future source of infection of these pathogens cannot be ruled out.

Using next-generation sequencing (NGS), three recent studies identified and characterised novel viruses in deer serum, plasma, and faecal samples (Huaman et al. 2021b, 2021c, 2022a). These studies illustrate how novel molecular techniques can change our understanding of viral epidemiology and evolution. Picobirnaviruses (PBVs) were detected in serum and plasma from fallow, rusa, and sambar deer (Huaman et al. 2021c), with subsequent molecular screening of a range of specimens collected from wild deer and of faecal samples from farmed cattle. PBVs have been detected in several animal species worldwide, mostly in faecal samples but also in blood and respiratory tract samples (Smits et al. 2011; Malik et al. 2014). High prevalence of PBVs were recorded in deer and cattle sampled in south-eastern Australia (Huaman et al. 2021c), with a predominance of genogroup I and simultaneous genogroups I and II detection in these host species. Moreover, the detection of identical sequences in the trachea and nasal swabs of the same animal, with no amplification in the lung, suggests active replication and infection of PBVs in the upper respiratory tract, expanding our knowledge of picobirnavirus tropism.

Genomic and phylogenetic analyses of NGS data revealed the presence of a new member of the genus Bopivirus, proposed as ‘Bopivirus C’ (Huaman et al. 2021b), in samples from south-eastern Australia. Further epidemiological investigation showed a prevalence of 8.5% in fallow deer, 16.7% in red deer and 0% in sambar deer and cattle. Phylogenetic and sequence analyses of the positive samples indicated that the same genotype is circulating. To our knowledge, this study reports for the first time a deer-origin bopivirus and the presence of a member of the genus Bopivirus in Australia.

A nearly complete genome of an endogenous betaretrovirus was characterised for the first time in fallow deer (Huaman et al. 2022a). Further genomic analysis showed that this provirus, tentatively named cervid endogenous betaretrovirus 1 (CERV β1), has typical betaretroviral genome features (gag-pro-pol-env). In addition, CERV β1 pol sequences were detected by PCR in wild populations of all the six non-native deer species in Australia. Phylogenetic analyses suggested that CERV β1 endogenisation occurred between 3.3 and 5 million years ago (Huaman et al. 2022a). Although this provirus does not appear to constitute a current risk for livestock, these results provide important insights into the evolution of betaretroviruses in cervids.

Parasitic diseases in deer

Unlike viral infections, research into parasitic infections on Australian deer populations was mostly conducted in the last 20 years, the majority of which was reviewed in Cripps et al. (2019). The research has focused on detecting gastrointestinal parasites and helminths. However, exposure to Sarcocystis, Entamoeba, and Neospora caninum and four vector-borne parasites (Babesia, Theileria, Trypanosoma, and Plasmodium) was recently assessed in PCR-based assays in wild deer from eastern Australia (Table 2).

PCR-based screening of deer serum and blood samples detected no active infection (i.e. where the pathogen replicates) of Sarcocystis and a range of vector-borne infections relevant for the livestock industry (Huaman et al. 2020, 2021a). Despite this non-detection, it remains possible that deer could become infected with these parasites (and act as a source of spill-back infection) in the future, given their endemicity in livestock, the presence of suitable vectors, and the ongoing spread of deer (Davis et al. 2016). This survey represents the first large-scale molecular study of its type in Australian deer and provides important baseline information about the infection status of wild deer in eastern Australia.

Following a similar research project detecting N. caninum parasites in wild dogs (Canis familiaris) (Davidson et al. 2022), and given the current gaps in knowledge about the sylvatic life cycle of this parasite, the seroprevalence of N. caninum was investigated in wild deer (unpublished data). Using a competitive ELISA (cELISA) test, a seroprevalence of 4% was detected in deer serum samples from fallow, red, and sambar deer collected in south-eastern Australia. These results suggest that wild deer contribute to the sylvatic cycle of this parasite in Australia. To our knowledge, this is the first reported detection of N. caninum antibodies in Australian wild deer and highlights the usefulness of cELISA for assessing serological assays in wildlife populations.

The intestinal parasite Entamoeba bovis has been previously detected in farm and wild ruminants worldwide, but its epidemiology and distribution in wild ruminants remain largely unexplored (Stensvold et al. 2010). E. bovis has also been detected in Australia, including in feral goats (Capra hircus) from Western Australia (Al-Habsi et al. 2017) and wild deer from eastern Australia (Huaman et al. 2022b). The cross-species infection between deer and livestock species was evaluated by estimating the time to a most recent common ancestor (TMCRA) of E. bovis sequences of wild deer and cattle origin (Huaman et al. 2022b). The TMCRA in this study was estimated to be >200 years ago (i.e. before cattle and deer were introduced to Australia), providing no evidence of E. bovis transmission between wild deer and cattle in Australia. This finding is surprising, but it is possible that wild deer populations have until recently been at a too-low density to play an important role in the transmission of these parasites.

Panozzo (2018) focused on interspecific transmission of gastro-intestinal parasites between livestock and wild deer (C. unicolor, D. dama and A. porcinus). She showed that the prevalence of parasites typically associated with cattle (e.g. Monieza spp.) was significantly higher in deer samples collected close to farmland, suggesting (but not proving) inter-species transmission. This study reported a high number of parasite species from deer samples that are relevant to the livestock industry and established that about a quarter of deer samples were positive for Fasciola hepatica and gastro-intestinal parasites, including O. ostertagi, O. leptospicularis, Haemonchus spp., O. radiatum, Trichostrongylus spp., and C. oncophora. The high prevalence of F. hepatica is consistent with the findings of Jenkins et al. (2020) and Lamb et al. (2021). Both studies focused on identifying the risk that deer pose to maintaining the infection of F. hepatica in livestock and established that approximately 50% of the samples were positive for this important parasite. These results led Jenkins et al. (2020) to conclude that deer are likely to represent a major source of environmental contamination. The presence of these parasites reduces livestock growth rates, which delays animals reaching slaughter weight (Roeber et al. 2013; Mazeri et al. 2017).

Current and future directions

This review suggests a low risk of transmission from wild deer to livestock in Australia. However, in Europe and North America wild deer were considered an important source of infection for livestock, and several publications focused on their local consequences and implications (Böhm et al. 2007; Conner et al. 2008; Martin et al. 2011; Ruiz-Fons et al. 2014). This discrepancy likely reflects differences between Australia and Europe/North America in climate, farming practices, and potential wildlife hosts. Changes in weather patterns in Australia due to climate change can alter the distributions, movements, and dispersal rates of invertebrate vectors (Bryan et al. 1996). Climate change could also influence the distributions and abundances of wildlife hosts. Thus, climate patterns can significantly impact pathogen transmission and interactions between wildlife hosts, vectors, and humans. Indeed, climate change is increasingly recognised as playing a major role in the emergence of vector-borne diseases in humans and wildlife (Fouque and Reeder 2019; Rocklov and Dubrow 2020). Therefore, long-term changes, especially warming temperatures, could significantly alter the distribution and prevalence of vector-borne diseases in wildlife populations (Fouque and Reeder 2019).

Climate change may pose a similar risk when considering the distribution of deer, and the potential for the spread of wild deer to new parts of Australia could result in new epidemiological challenges. The social behaviour of hosts is also likely to be an important factor influencing the epidemiology of some pathogens. Each of the six deer species in Australia congregates at preferred feeding areas, increasing the probability of disease spread among individuals. Male deer may further contribute to the risk of disease transmission through contact with multiple females during the breeding season.

Advances in high-throughput sequencing and bioinformatics have greatly increased our understanding and capacity to identify novel microorganisms. For example, in the last decade, a novel virus (Schmallenberg virus – SBV) was described in European cattle, constituting an emerging threat to the livestock industry in Europe and worldwide (Hoffmann et al. 2012; Endalew et al. 2019). Since its description in 2011, high seroprevalence of SBV has been detected in wild deer in Europe, indicating that deer could act as a source of this virus for livestock (Mouchantat et al. 2015; Garcia-Bocanegra et al. 2017; Jimenez-Ruiz et al. 2021). As mentioned above, next-generation sequencing was instrumental in identifying a novel Bopivirus in fallow and rusa deer from south-eastern Australia (Huaman et al. 2021b). The authors hypothesised that this virus, like other enteric picornaviruses, is transmitted via the faecal–oral route. However, further work is required to determine its distribution in other deer species (e.g. chital, rusa and hog deer), and livestock species other than cattle, to increase our understanding of the potential for cross-transmission between wild deer and livestock.

As discussed above, deer are infected by and susceptible to many diseases, some of which are zoonotic, meaning that they can also affect humans. Increasing the focus on wildlife disease surveillance to detect emerging infectious diseases and integrate wildlife and environmental health into One Health policies (Cunningham et al. 2017) is crucial to prepare Australia to better recognise and manage the adverse impacts of zoonotic diseases. Indeed, high wild deer densities (e.g. 39 per km²; Bengsen et al. 2022) may cause concern for human health via the transmission of infectious agents through direct contact, the consumption of venison, or contamination of the environment (particularly water) with faeces or urine.

Several zoonotic diseases occur in wild deer in Australia, including Q fever, leptospirosis, fasciolosis, cryptosporidiosis, and giardiasis. Recently, attention has turned to the potential role of deer as reservoirs of the SARS-CoV-2 virus, which causes COVID-19 in humans. There was high seroprevalence of SARS-CoV-2 in free-ranging white-tailed deer (Odocoileus virginianus) in the USA, revealing high susceptibility to infection of this deer species and active deer-to-deer transmission (Murphy and Ly 2021; Palmer et al. 2021; Hale et al. 2022). Moreover, the identification of SARS-CoV-2 variants suggests human-to-deer infections and that wild deer can sustain transmission (Hale et al. 2022). In contrast, no evidence of SARS-CoV-2 infection was found in common European deer species (Holding et al. 2022; Moreira-Soto et al. 2022). These studies indicate that deer should be considered when identifying potential reservoirs and intermediate hosts of emerging zoonotic diseases.

Finally, we recommend developing a passive surveillance system through the Australian deer hunter community. Deer hunters harvest large numbers of deer (Moloney et al. 2022). Training in identifying, recording macroscopic lesions, and collecting specimens could be provided to hunters as part of the licensing process, and hunters could help monitor the presence and distribution of infectious diseases. The investigations conducted in the last 5 years provide vital baseline data for future research. Monitoring changes in the disease status would offer a more comprehensive view of the dynamics of infectious diseases, which is important if the risks of those disease to humans, livestock, and wildlife are to be minimised. These findings extended our knowledge of known and novel viruses and parasites associated with Australian deer.

Data availability

This manuscript reviewed published literature; as such, no new data were generated in this study.

Conflicts of interest

David Forsyth and Anthony Pople were guest Associate Editors for this special issue. Despite this relationship, they did not at any stage have editor-level access to this manuscript while in peer review, as is the standard practice when handling manuscripts submitted by an editor to this journal. Wildlife Research encourages its editors to publish in the journal, and they are kept separate from their manuscripts’ decision-making process. The authors have no further conflicts of interest to declare.

Declaration of funding

This study was funded by the Centre for Invasive Species Solutions (PO1-L-002). The funding body had no role in the preparation or review of the manuscript.