Invasive wild deer exhibit environmental niche shifts in Australia: Where to from here?

Invasive species have established populations around the world and, in the process, characteristics of their realized environmental niches have changed. Because of their popularity as a source of game, deer have been introduced to, and become invasive in, many different environments around the world. As such, deer should provide a good model system in which to test environmental niche shifts. Using the current distributions of the six deer species present in Australia, we quantified shifts in their environmental niches that occurred since introduction; we determined the differences in suitable habitat between their international (native and invaded) and their Australian ranges. Given knowledge of their Australian habitat use, we then modeled the present distribution of deer in Australia to assess habitat suitability, in an attempt to predict future deer distributions. We show that the Australian niches of hog (Axis porcinus), fallow (Dama dama), red (Cervus elaphus), rusa (C. timorensis), and sambar deer (C. unicolor), but not chital deer (A. axis), were different to their international ranges. When we quantified the potential range of these six species in Australia, chital, hog, and rusa deer had the largest areas of suitable habitat outside their presently occupied habitat. The other three species had already expanded outside the ranges that we predicted as suitable. Here, we demonstrate that deer have undergone significant environmental niche shifts following introduction into Australia, and these shifts are important for predicting the future spread of these invasive species. It is important to note that current Australian and international environmental niches did not necessarily predict range expansions, thus wildlife managers should treat these analyses as conservative estimates.

Dancing to a different tune: changing reproductive seasonality in an introduced chital deer population.

Male and female reproductive behaviour is typically synchronised. In species such as those in the family Cervidae, reproductive timing is often cued by photoperiod, although in females, it can be dependent on body condition. When a species is introduced to a novel environment, the environment changes, or responses of the sexes to such cues differ, asynchronous reproductive behaviour between males and females may occur. We investigated the seasonality of reproductive behaviour in introduced chital deer in northern Queensland by examining male antler phase in relation to female conception rates. We then analysed the influence of different variables likely to affect the timing of male and female reproductive physiology. The lowest percentage of chital in hard antler in any 1 month in this study was 35% (Fig. 1), but the average value was closer to 50%, thus there was a seasonal peak in antler phase linked with photoperiod. Females conceived at any time of year, but were strongly influenced by the amount of rainfall 3 months prior to conception. This resulted in varying conception peaks year-to-year that often did not correspond to the male's peak in hard antler. In this system, a proportion of males and females were physiologically and behaviourally ready to mate at any time of the year. We predict that differences in the timing of the peaks between the males and females will lead to increased reproductive skew (variation in reproductive success among individual males). This pattern may select for different mating strategies or physiological mechanisms to increase reproductive success. Fig. 1 The average percentage of male chital deer in hard antler by month from 2014 to 2019 in north Queensland. Values above the bars indicate the total number of males that were sampled in each month and the error bars indicate the standard error. In the month with the lowest % males in hard antler in the entire study (November, 2017), 35% of males were in hard antler.

Estimating deer density and abundance using spatial mark-resight models with camera trap data.

Globally, many wild deer populations are actively studied or managed for conservation, hunting, or damage mitigation purposes. These studies require reliable estimates of population state parameters, such as density or abundance, with a level of precision that is fit for purpose. Such estimates can be difficult to attain for many populations that occur in situations that are poorly suited to common survey methods. We evaluated the utility of combining camera trap survey data, in which a small proportion of the sample is individually recognizable using natural markings, with spatial mark-resight (SMR) models to estimate deer density in a variety of situations. We surveyed 13 deer populations comprising four deer species (Cervus unicolor, C. timorensis, C. elaphus, Dama dama) at nine widely separated sites, and used Bayesian SMR models to estimate population densities and abundances. Twelve surveys provided sufficient data for analysis and seven produced density estimates with coefficients of variation (CVs) ≤ 0.25. Estimated densities ranged from 0.3 to 24.6 deer km-2. Camera trap surveys and SMR models provided a powerful and flexible approach for estimating deer densities in populations in which many detections were not individually identifiable, and they should provide useful density estimates under a wide range of conditions that are not amenable to more widely used methods. In the absence of specific local information on deer detectability and movement patterns, we recommend that at least 30 cameras be spaced at 500-1,000 m and set for 90 days. This approach could also be applied to large mammals other than deer.

Detection and Characterisation of an Endogenous Betaretrovirus in Australian Wild Deer.

Endogenous retroviruses (ERVs) are the remnants of past retroviral infections that once invaded the host's germline and were vertically transmitted. ERV sequences have been reported in mammals, but their distribution and diversity in cervids are unclear. Using next-generation sequencing, we identified a nearly complete genome of an endogenous betaretrovirus in fallow deer (Dama dama). Further genomic analysis showed that this provirus, tentatively named cervid endogenous betaretrovirus 1 (CERV ß1), has typical betaretroviral genome features (gag-pro-pol-env) and the betaretrovirus-specific dUTPase domain. In addition, CERV ß1 pol sequences were detected by PCR in the six non-native deer species with wild populations in Australia. Phylogenetic analyses demonstrated that CERV ß1 sequences from subfamily Cervinae clustered as sister taxa to ERV-like sequences in species of subfamily Muntiacinae. These findings, therefore, suggest that CERV ß1 endogenisation occurred after the split of these two subfamilies (between 3.3 and 5 million years ago). Our results provide important insights into the evolution of betaretroviruses in cervids.

Novel Picornavirus Detected in Wild Deer: Identification, Genomic Characterisation, and Prevalence in Australia.

The use of high-throughput sequencing has facilitated virus discovery in wild animals and helped determine their potential threat to humans and other animals. We report the complete genome sequence of a novel picornavirus identified by next-generation sequencing in faeces from Australian fallow deer. Genomic analysis revealed that this virus possesses a typical picornavirus-like genomic organisation of 7554 nt with a single open reading frame (ORF) encoding a polyprotein of 2225 amino acids. Based on the amino acid identity comparison and phylogenetic analysis of the P1, 2C, 3CD, and VP1 regions, this novel picornavirus was closely related to but distinct from known bopiviruses detected to date. This finding suggests that deer/bopivirus could belong to a novel species within the genus Bopivirus, tentatively designated as "Bopivirus C". Epidemiological investigation of 91 deer (71 fallow, 14 sambar and 6 red deer) and 23 cattle faecal samples showed that six fallow deer and one red deer (overall prevalence 7.7%, 95% confidence interval [CI] 3.8-15.0%) tested positive, but deer/bopivirus was undetectable in sambar deer and cattle. In addition, phylogenetic and sequence analyses indicate that the same genotype is circulating in south-eastern Australia. To our knowledge, this study reports for the first time a deer-origin bopivirus and the presence of a member of genus Bopivirus in Australia. Further epidemiological and molecular studies are needed to investigate the geographic distribution and pathogenic potential of this novel Bopivirus species in other domestic and wild animal species.

Molecular Epidemiology and Characterization of Picobirnavirus in Wild Deer and Cattle from Australia: Evidence of Genogroup I and II in the Upper Respiratory Tract.

Picobirnaviruses (PBVs) have been detected in several species of animals worldwide; however, data pertaining to their presence in Australian wild and domestic animals are limited. Although PBVs are mostly found in faecal samples, their detection in blood and respiratory tract samples raises questions concerning their tropism and pathogenicity. We report here PBV detection in wild deer and cattle from southeastern Australia. Through metagenomics, the presence of PBV genogroups I (GI) and II (GII) were detected in deer serum and plasma. Molecular epidemiology studies targeting the partial RNA-dependent RNA polymerase gene were performed in a wide range of specimens (serum, faeces, spleen, lung, nasal swabs, and trachea) collected from wild deer and cattle, with PCR amplification obtained in all specimen types except lung and spleen. Our results reveal the predominance of GI and concomitant detection of both genogroups in wild deer and cattle. In concordance with other studies, the detected GI sequences displayed high genetic diversity, however in contrast, GII sequences clustered into three distinct clades. Detection of both genogroups in the upper respiratory tract (trachea and nasal swab) of deer in the present study gives more evidence about the respiratory tract tropism of PBV. Although much remains unknown about the epidemiology and tropism of PBVs, our study suggests a wide distribution of these viruses in southeastern Australia.

Evaluation of haemoparasite and Sarcocystis infections in Australian wild deer.

Wild animals are natural reservoir hosts for a variety of pathogens that can be transmitted to other wildlife, livestock, other domestic animals, and humans. Wild deer (family Cervidae) in Europe, Asia, and North and South America have been reported to be infected with gastrointestinal and vector-borne parasites. In Australia, wild deer populations have expanded considerably in recent years, yet there is little information regarding which pathogens are present and whether these pathogens pose biosecurity threats to humans, wildlife, livestock, or other domestic animals. To address this knowledge gap, PCR-based screening for five parasitic genera was conducted in blood samples (n = 243) sourced from chital deer (Axis axis), fallow deer (Dama dama), rusa deer (Rusa timorensis) and sambar deer (Rusa unicolor) sampled in eastern Australia. These blood samples were tested for the presence of DNA from Plasmodium spp., Trypanosoma spp., Babesia spp., Theileria spp. and Sarcocystis spp. Further, the presence of antibodies against Babesia bovis was investigated in serum samples (n = 105) by immunofluorescence. In this study, neither parasite DNA nor antibodies were detected for any of the five genera investigated. These results indicate that wild deer are not currently host reservoirs for Plasmodium, Trypanosoma, Babesia, Theileria or Sarcocystis parasites in eastern Australia. We conclude that in eastern Australia, wild deer do not currently play a significant role in the transmission of these parasites. This survey represents the first large-scale molecular study of its type in Australian wild deer and provides important baseline information about the parasitic infection status of these animals. The expanding populations of wild deer throughout Australia warrant similar surveys in other parts of the country and surveillance efforts to continually assess the level of threat wild deer could pose to humans, wildlife, livestock and other domestic animals.

Serosurveillance and Molecular Investigation of Wild Deer in Australia Reveals Seroprevalence of Pestivirus Infection.

Since deer were introduced into Australia in the mid-1800s, their wild populations have increased in size and distribution, posing a potential risk to the livestock industry, through their role in pathogen transmission cycles. In comparison to livestock, there are limited data on viral infections in all wildlife, including deer. The aim of this study was to assess blood samples from wild Australian deer for serological evidence of exposure to relevant viral livestock diseases. Blood samples collected across eastern Australia were tested by ELISA to detect antigens and antibodies against Pestivirus and antibodies against bovine herpesvirus 1. A subset of samples was also assessed by RT-PCR for Pestivirus, Simbu serogroup, epizootic hemorrhagic disease virus and bovine ephemeral fever virus. Our findings demonstrated a very low seroprevalence (3%) for ruminant Pestivirus, and none of the other viruses tested were detected. These results suggest that wild deer may currently be an incidental spill-over host (rather than a reservoir host) for Pestivirus. However, deer could be a future source of viral infections for domestic animals in Australia. Further investigations are needed to monitor pathogen activity and quantify possible future infectious disease impacts of wild deer on the Australian livestock industry.

Should managed populations be monitored every year?

We often need to estimate the size of wild populations to determine the appropriate management action, for example, to set a harvest quota. Monitoring is usually planned under the assumption that it must be carried out at fixed intervals in time, typically annually, before the harvest quota is set. However, monitoring can be very expensive, and we should weigh the cost of monitoring against the improvement that it makes in decision making. A less costly alternative to monitoring annually is to predict the population size using a population model and information from previous surveys. In this paper, the problem of monitoring frequency is posed within a decision-theory framework. We discover that a monitoring regime that varies according to the state of the system can outperform fixed-interval monitoring. This idea is illustrated using data for a red kangaroo (Macropus rufus) population in South Australia. Whether or not one should monitor in a given year is dependent on the estimated population density in the previous year, the uncertainty in that population estimate, and past rainfall. We discover that monitoring is important when a model-based prediction of population density is very uncertain. This may occur if monitoring has not taken place for several years, or if rainfall has been above average. Monitoring is also important when prior information suggests that the population is near a critical threshold in population abundance. However, monitoring is less important when the optimal management action would not be altered by new information.