Ecology of free-ranging axis deer (Axis axis) in the Edwards Plateau ecoregion of Central Texas: Population density, genetics, and impacts of an invasive deer species

Axis deer (Axis axis) initially were introduced to Texas in 1932 for additional hunting opportunities. These introductions were conducted with minimal consideration of the ecology of axis deer and how they may impact native species and ecosystems. Furthermore, despite being present in Texas for nearly a century, there is a still a paucity of available information on the ecology of axis deer in Texas, as only a few studies have been conducted during the last 90 years, many of which would benefit from additional basic ecological data and updated techniques and technologies. Therefore, the goal of this dissertation was to answer pressing questions regarding axis deer ecology to aid in management of free-ranging axis deer in Texas. Axis deer have been widely introduced to new geographic ranges and in the United States, free-ranging axis deer have become well established in the Edwards Plateau ecoregion as well as other portions of Texas. However, no formalized nor reliable estimates of axis deer population density or size have been conducted since 1994. It is hypothesized that axis deer on the Edwards Plateau are potentially competing with native white-tailed deer (Odocoileus virginianus) for food, space, and habitat resources, and causing damage to important riparian habitats. My goal was to assess if the density of axis deer and white-tailed deer in Texas could provide information about potential negative impacts of axis deer on native wildlife and habitats. Estimated using distance sampling techniques in 2018 and 2019, axis deer density was 19.7 (95% CI: 14.1 – 25.6) axis deer/km2 compared to 23.0 (95% CI: 18.2 – 27.5) white-tailed deer/km2. Axis deer densities ranged from 16.9 – 171.0 /km2 among eight different habitat types in Kimble County, TX, with a county wide estimate of 61,078 (95% CI: 30,407 – 100,369). Axis deer densities among the different habitat types imply that axis deer have habituated to the ecoregion, are demonstrating habitat selection, and may be having profound ecological impacts in riparian habitats. Finally, axis deer population estimates suggest their population has grown substantially since introduction. Axis deer apparently have completed a successful invasion in this portion of Texas and have successfully emerged from the colonization, establishment, and lag periods of invasion. My findings suggest population management of axis deer is warranted to limit impacts to native wildlife from potential disease transmission or habitat usurpation or damage to riparian vegetation communities, soil, and water quality. Free-ranging axis deer exist throughout central Texas, and three Hawaiian Islands, with numerous captive populations throughout North America. Currently, there is no dentition-based technique specifically developed to age axis deer, subsequently resulting in the use of tooth replacement and wear criteria established for white-tailed deer to age axis deer, which may be inappropriate and result in incorrect age estimates. Given the lack of a species-specific aging protocol for axis deer, I developed a tooth replacement and wear aging technique for free-ranging axis deer. My objectives were to (1) assess potential error and bias associated with white-tailed deer aging criteria for axis deer, (2) characterize patterns of tooth eruption and wear of age axis deer using cementum annuli (CA) analysis, (3) describe tooth replacement and wear criteria and develop a guide to age axis deer, and (4) assess the accuracy and precision of the age guide. I collected 88 mandibles from axis deer and used CA protocols developed for elk on the primary incisor to obtain an age estimate for each individual mandible. I then asked 11 biologists, in two groups of five and six, to age 51 and 37 axis mandibles, respectively, using their experience and prior knowledge of the white-tailed deer aging guide. I then used these CA-aged axis deer mandibles (ranging from 0 – 15 years old) and developed a tooth replacement and wear guide. This resulted in eight separate axis deer age classes, ranging from fawn to 13+ years old, where I used similar verbiage and approaches commonly used for white-tailed deer. I then validated the guide by testing the accuracy of three biologists and 34 naïve students to use the guide to age axis deer. Biologists tended to underestimate the age of axis deer by up to several years when using criteria established for white-tailed deer. However, both professional biologists and students accurately (81.8% of estimates within ± one year) aged axis deer when using the tooth replacement and wear guide I developed. This guide shows promise for both professional biologists and land managers involved in axis deer harvest, harvest management, and other management activities, where more accurate age-related data are required for axis deer management. Human-mediated introductions and subsequent establishment and spread of nonnative species has the potential to create a founder effect in such populations, which typically results in low genetic diversity and inbreeding. However, several exotic invasive species exhibit a ‘genetic paradox’ in which they thrive, despite inbreeding and low genetic diversity patterns in their introduced range. Axis deer were introduced into Texas, Hawaii, Australia, and Croatia during the 19th and 20th centuries and subsequently successfully established large populations from a few founding individuals. Mitochondrial (Cytochrome-b, Cytb; Displacement loop, D-loop) and nuclear (10 microsatellites) markers were used to assess genetic diversity within and between axis deer populations in Texas and Hawaii and then compared to other introduced and native populations. Overall, mtDNA divergence was 0.54% (Cytb) and 1.55% (D-loop) indicating high mitochondrial similarity. Further, each invasive population was composed of only one or two mtDNA haplotypes. Microsatellite allele diversity also was low within and between populations in Texas and Hawaii resulting in monomorphic loci and multiple violations of Hardy-Weinberg equilibrium in both populations. The low genetic diversity in native (i.e., Indian) axis deer as well as within and between invasive populations suggests that the introduced populations experienced founder effects following introduction, and then underwent successful establishment and expansion. Axis deer appear to be another invasive species exhibiting the genetic paradox where they exhibit genetic profiles that suggest inbreeding effects are imminent yet display no signs of inbreeding and are wildly successful adapting to novel environments. Chronic wasting disease (CWD) is a fatal, transmissible spongiform encephalopathy that affects both native and non-native North American cervid species. The expanding geographic distribution of CWD and list of affected species is concerning, especially for those who manage wildlife populations or harvest wild animals. In areas where native and non-native species are sympatric, the potential for interspecific transmission of CWD is concerning when the CWD susceptibility of the non-native species is unknown. Axis deer occur both in captivity and free-ranging populations in portions of North America, but to-date, no data exist pertaining to the species’ susceptibility to CWD. I sequenced the prion protein gene (PRNP) exon 3, the coding region of the prion protein (PrPC), from 133 axis deer to assess the species’ potential susceptibility to CWD. I then compared axis deer PrPC sequences and amino acid polymorphisms to those of CWD susceptible species. A single PRNP allele with no evidence of intraspecies variation was identified in axis deer that indicates axis deer PRNP is most similar to North American elk (Cervus canadensis) PRNP in both nucleic and amino acid composition. Based upon this evidence, axis deer may be susceptible to CWD infection. However, CWD surveillance of axis deer, in both captive and free-ranging populations is scarce at best. I recommend proactively increasing CWD surveillance for axis deer, with focus on areas where CWD has been detected and axis deer are sympatric with native North American CWD susceptible species. Introductions of axis deer to Texas were done with minimal knowledge of the ecology and potential impacts of axis deer. As the population has grown both in abundance and geographic distribution, questions have arisen on how axis deer may be impacting native habitats and wildlife. I used locations obtained during spotlight surveys to assess habitat selection and where axis deer may have the greatest impact. I also constructed deer exclosures to assess how herbivory by axis deer could be altering vegetation community composition and abundance. I found that axis deer selected riparian grasslands and mixed forests as well as upland grassland while selecting against other upland habitats that comprise most of the study area. While statistical significance was sparse, trends indicated that excluding axis deer and white-tailed deer resulted in increased ground coverage by grasses while also reducing the ground coverage by forbs and bare ground. The available biomass of grasses appeared to be influenced by excluding deer herbivory with exclosures having more estimated biomass whereas the biomass of forbs appeared to be cyclical with seasonal patterns. Although certain trends and changes to the vegetation community were identified, a major flooding event that occurred in the middle of this study may have confounded results. However, our results do indicate that axis deer select for highly sensitive and ecological important riparian habitats and may have impacts on vegetation community composition and abundance which in turn may affect ecological processes in those ecosystems. Continued monitoring of impacts of axis deer would be important to determine if management actions are necessary to preserve native ecosystems. The findings presented here have numerous management implications regarding the management of axis deer to preserve and protect native wildlife and ecosystems. Continuing research on the ecology of axis deer in Texas is needed to gain more understanding on the potential impacts of axis deer presence in Texas given that complete removal of the population is likely no longer feasible. Management of axis deer populations should be considered to maintain and preserve native ecosystems and wildlife populations.