https://orcid.org/0000-0002-6181-8469
Figures
Abstract
Introduction
Over recent decades, the abundance and geographic ranges of wild ungulate species have expanded in many parts of Europe, including the UK. Populations are managed to mitigate their ecological impacts using interventions, such as shooting, fencing and administering contraception. Predicting how target species will respond to interventions is critical for developing sustainable, effective and efficient management strategies. However, the quantity and quality of evidence of the effects of interventions on ungulate species is unclear. To address this, we systematically mapped research on the effects of population management on wild ungulate species resident in the UK.
Methods
We searched four bibliographic databases, Google Scholar and nine organisational websites using search terms tested with a library of 30 relevant articles. Worldwide published peer-reviewed articles were considered, supplemented by ‘grey’ literature from UK-based sources. Three reviewers identified and screened articles for eligibility at title, abstract and full-text levels, based on predefined criteria. Data and metadata were extracted and summarised in a narrative synthesis supported by structured graphical matrices.
Results
A total of 123 articles were included in the systematic map. Lethal interventions were better represented (85%, n = 105) than non-lethal interventions (25%, n = 25). Outcomes related to demography and behaviour were reported in 95% of articles (n = 117), whereas effects on health, physiology and morphology were studied in only 11% of articles (n = 14). Well-studied species included wild pigs (n = 58), red deer (n = 28) and roe deer (n = 23).
Conclusions
Evidence for the effects of population management on wild ungulate species is growing but currently limited and unevenly distributed across intervention types, outcomes and species. Priorities for primary research include: species responses to non-lethal interventions, the side-effects of shooting and studies on sika deer and Chinese muntjac. Shooting is the only intervention for which sufficient evidence exists for systematic review or meta-analysis.
Citation: Barton O, Gresham A, Healey JR, Cordes LS, Shannon G (2022) The effects of population management on wild ungulates: A systematic map of evidence for UK species. PLoS ONE 17(6): e0267385. https://doi.org/10.1371/journal.pone.0267385
Editor: Christopher A. Lepczyk, Auburn University, UNITED STATES
Received: July 5, 2021; Accepted: April 7, 2022; Published: June 10, 2022
Copyright: © 2022 Barton et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper and its Supporting Information files.
Funding: Our research was funded by KESS 2 (Knowledge Economy Skills Scholarship). KESS 2 is a pan-Wales higher level skills initiative led by Bangor University on behalf of the HE sector in Wales. It is part funded by the Welsh Governments European Social Fund (ESF) convergence programme for West Wales and the Valleys. The KESS 2 grant number is: c80815.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Wild ungulates are integral to the functioning of grassland and forest ecosystems [1–4]. As highly mobile and wide-ranging herbivore species, they have the capacity to influence ecological processes at multiple spatial scales [5–7]. In recent decades, the abundance and geographic ranges of many ungulate species have rapidly increased across Europe [8, 9]. Population growth has been attributed to translocations, the removal of natural predators, climate change and widespread alterations in land use [10]. These include the increased planting of trees to meet conservation targets, which has formed suitable habitat for a range of ungulates and agricultural intensification that provides a consistently available food-source throughout the year [11–13]. As their densities increase, a variety of interacting ecological and social factors must be considered in order to manage ungulate populations sustainably and satisfy the objectives of a range of stakeholders, including foresters, conservationists, farmers, landowners, recreational hunters and countryside visitors [10, 14, 15].
The effects of wild ungulates on ecosystems are species- and context-specific. Low-level herbivory by deer (Cervidae) and feral goats (Capra spp.) has been shown to suppress the growth of competitively dominant plant species and accelerate nitrogen and carbon cycling [6, 16]. However, more intense browsing pressure has been linked to declines in biodiversity [17], reductions in forest understorey foliage [18] and damage to agriculture [19]. In wetlands, rooting by wild pigs (Sus scrofa) can enhance microhabitat diversity and plant species richness [20], whereas the same behaviour in forests has been associated with decreased plant diversity [21] and the destruction of habitat for small mammals [22].
In human transformed landscapes, ungulates pose a threat to human health and well-being as a result of road traffic accidents [23, 24]. A recent assessment of the frequency of ungulate-vehicle collisions (UVCs) in Europe estimated that 30,000 incidents occur each year [25]. Additionally, ungulates are known to act as reservoirs of diseases, such as bovine tuberculosis [26] and salmonella [27], as well as vectors of diseases, such as Lyme disease [28], that are transmissible to humans and domestic livestock [29, 30]. In the past two decades, the need to better understand the role of ungulates as ecosystem engineers and to mitigate their negative ecological and socio-economic impacts has been increasingly recognised by scientists, wildlife managers and conservationists [8, 14].
Methods to mitigate ungulate impacts include control interventions, such as shooting, administering contraception, non-lethal deterrents and supplementary feeding [10, 31, 32]. Typically, the efficacy of each practice is measured by observing how key environmental variables respond or monitoring changes in the prevalence of disease [8, 10]. For example, in the UK the effectiveness of shooting deer is often estimated by observing the relationship between shooting effort and browsing damage to sensitive woodlands [8, 10, 33]. Monitoring environmental indicators of ecological change (IECs) is relatively inexpensive and provides convenient metrics for managers to compare the efficacy of different management strategies [8, 15, 34]. However, target species may respond to an intervention in a variety of ways that if not appropriately considered could lead to management strategies being ineffective or even counter-productive. For example, in the case of red deer (Cervus elaphus), shooting has been shown to reduce population densities and effectively mitigate the environmental impact of browsing [35]. However, there is evidence that shooting also has long-term effects on the morphology of red deer [36] and that the disturbance of shooting causes shifts in their home ranges, which may promote the spread of diseases [37]. Localised shooting of deer can lead to the development of source-sink dynamics in the population that neutralise efforts to reduce numbers at the scale of the landscape or region [33, 38]. Additionally, responses of target species may be taxon-specific, which is particularly important in scenarios where a single intervention is applied to manage multiple species. For instance, supplementary feeding can reduce levels of bark damage by red deer [39] but this intervention has also been shown to promote the population growth of wild pigs, leading to an increase in their disturbance on the environment [40].
A recent review [14] emphasised the importance of developing strategies for adaptive population management informed by robust empirical evidence. A total of ten measures were proposed to ensure the viability and long-term persistence of ungulate populations. These included long-term monitoring of habitat performance indicators (e.g., species richness), analysis of the indirect and unintended effects of supplementary feeding and a recognition for the impacts of hunting beyond reducing population densities [14]. Accurate assessment of the responses of ungulate species to interventions typically requires intensive sampling [e.g., 41] and specialist equipment, such as motion-activated cameras or global-positioning system (GPS) collars [e.g., 42]. These approaches are typically unfeasible for most practitioners and formal studies are usually constrained to observations of a narrow range of responses for a single species or intervention. Consequently, individual studies may be of limited benefit to decision-makers faced with the challenge of developing strategies to manage multiple species simultaneously in order to meet a range of objectives (e.g., environmental impact mitigation, sustainable exploitation, reducing disease transmission). Therefore, syntheses of the literature, that provide information on the quantity and quality of the available evidence are needed to provide appropriate support for wildlife and land managers as well as policymakers. However, systematic assessments of the available evidence are lacking. This is of particular importance for wild ungulate management because the strength of the evidence-base supporting practices is unclear.
In this review we systematically map the evidence for the effects of control interventions on the wild ungulate species resident in the UK. The purpose of the systematic map is to collate, catalogue and describe the extent and distribution of evidence in relation to key variables [e.g., species, intervention type, response etc., 43]. Additionally, the map is used to identify important topics for primary research and serves as a valuable resource for scholars to more easily locate relevant articles for further systematic review or meta-analyses. The aim of the study is to support the development of more efficient and effective management strategies by collecting and characterising the evidence for species responses to commonly-adopted practices.
Scope of study
The primary objective of this systematic map is to collate existing research on the effects of management practices on the nine wild ungulate (Artiodactyla) species resident in the UK. Searches were restricted to these species to provide an appropriate focus and to ensure that the volume of literature screened for eligibility would be manageable. The species included represent a range of body sizes and ecological characteristics (e.g., feeding behaviour, reproduction rates, average lifespan etc.). Several (notably wild pigs, red deer and roe deer) are also abundant across Europe and are globally important for wildlife management [8, 44]. Worldwide searches were conducted for peer-reviewed research articles but searches for ‘grey’ literature were restricted to UK-based sources only. It was beyond the scope of this review to critically appraise the evidence collected for each species. Instead, the synthesis provides a species-specific summary of the available evidence to identify important knowledge gaps and prioritise topics for future research and/or evidence synthesis. We did not preregister a protocol for this systematic map. In all other respects our procedure followed guidelines established by the Collaboration for Environmental Evidence [45] and complies with PRISMA and ROSES reporting standards [46, 47, S1 and S2 Files]
Methods
Eligibility criteria
Eligible articles included any primary research study that collected data by way of an experiment or quasi-experiment (control-intervention and/or before-after) to examine the effects of an intervention on one or several features of ungulate biology. Articles originating from any country were considered for inclusion. No explicit date restrictions were applied but the date of the earliest available records varied between literature sources. Articles were required to meet the eligibility criteria for the elements of the primary question described in the following sections.
Population.
All wild ungulate (Artiodactyla) species and subspecies currently resident in the UK, as described by Apollonio, Andersen and Putman [8] including:
Interventions.
Deliberate human practices intended to mitigate the environmental and socio-economic impacts of wild ungulates by manipulating one or more features of their biology. Included in the review are interventions that directly influence target species such as shooting, administering contraception, supplementary feeding and non-lethal deterrents, as well as actions that have indirect effects, such as fencing and landscape modification. All practices considered are hereafter referred to as ‘interventions’.
Comparator.
No intervention (a separate control site or population in a control/intervention (CI) study design, a time period of no intervention in a before/after (BA) study design or a combination of both in a before/after/control/intervention study design (BACI)) or an alternative level of intervention intensity (e.g., the effect of shooting may be inferred by comparing sites, populations or time periods that experienced different levels of shooting effort in an observational (Obs) study).
Outcomes.
Any responses of the target species to interventions were reported as they were stated in the relevant articles. Any effects on the biology of the target species were considered, including influences on population size and viability, morphology, physiology, movement behaviour, life history traits and habitat selection. The only outcomes included were effects on the target species and not secondary effects on other species, disease prevalence, plant and animal communities or habitat ecosystem components (e.g., evidence of the influence of an intervention on habitat selection by individuals of the target species from GPS location data or pellet counts was included as an outcome, but not inference from variation in tree growth or local species richness).
Searching for articles
An initial scoping search was conducted to identify suitable search terms, estimate the volume of relevant literature and validate the search methodology. Details of the search terms, number of hits and comments on the general quality of identified articles were recorded (S3 File). Terms describing the populations of interest were linked to intervention terms to form the following search string that was used to query Internet search engines and online bibliographic databases:
Population: ts = (muntjac OR "muntiacus reevesi" OR "chinese water deer" OR "hydropotes inermis" OR "roe deer" OR "capreolus capreolus" OR "red deer" OR "cervus elaphus" OR "sika deer" OR "cervus nippon" OR "fallow deer" OR "dama dama" OR "feral goat*" OR "capra aegagrus hircus " OR "wild goat*" OR "feral pig" OR "sus scrofa" OR "feral pigs" OR "feral hog*" OR "feral swine" OR "wild pig" OR "wild pigs" OR "wild hog*" OR "wild boar" OR "feral sheep")
AND
Intervention: ts = ("population control" OR "lethal control" OR hunt* OR cull* OR shoot* OR harvest* OR stalk* OR bait* OR poison* OR trapping OR (inhibit* AND reproduc*) OR immunocontracept* OR contracept* OR "fertility control" OR repel* OR deterrent* OR "diversionary feed*" OR (supplement* AND feed*) OR (supplement* AND food) OR "feed* station$" OR "forest management" OR "landscape structure" OR (manipulat* AND landscape) OR (manipulat* AND habitat) OR fenc*)
Sources of publications
A range of online sources were searched including four bibliographic databases (Clarivate Analytics Web of Science Core Collection and BIOSIS Citation Index, CAB Direct, Open Grey (www.opengrey.eu) and EThOS (www.ethos.bl.uk)), nine organisational websites and Google Scholar (S3 File). Where possible, search histories were saved in order to re-run the search if necessary. For each literature source, data were collected on: date accessed, search terms used, number of hits and a qualitative estimate of the relevance of identified articles (S3 File). Resource limitations constrained this study to an assessment of articles published in the English language.
Article screening and data coding
Articles identified by the search string were screened for eligibility using the online open-source platform of CADIMA (www.cadima.info/index.php). The CADIMA platform compiles records into a single reference library, automatically removes duplicates and facilitates the screening of articles at three levels; (1) Title, (2) Abstract and (3) Full text. The number of results from each literature source was recorded. A team of three reviewers screened articles for eligibility and reviewer consistency was checked at each stage (S3 File). Data were extracted for all articles that met the inclusion criteria and coded in an Excel spreadsheet to record the following information:
- Author(s)
- Study date
- Title
- Publication title
- Publication type (Journal article, report, thesis etc.)
- Country/countries of origin
- Total study area (km2)
- Study duration (years)
- Study species
- Species status (native or non-native)
- Intervention(s)
- Outcome(s)
- Response data type
- Study design (BA, CI, BACI or Obs)
Species status (native or non-native) was based on the species ranges described by the IUCN Red List of Threatened Species (www.iucnredlist.org) and CABI Invasive Species Compendium (www.cabi.org/ISC). As escaped domestic animals, feral sheep and feral goats were considered to be non-native irrespective of country.
Results
Number and types of articles
Fig 1 illustrates the results of the literature searches and stages of article screening. A total of 13,659 articles were retrieved from bibliographic databases and Google Scholar, of which 5,560 were identified as duplicates and automatically removed by the CADIMA software. Very few articles (n = 17) were obtained from ’grey’ literature sources. Only 3% of articles (n = 297) were retained after screening at the title and abstract level. The list of articles was further reduced following full-text assessment to a subset of 123 articles that were used for data extraction. Of the articles excluded at the full-text assessment stage (n = 174), 52% were excluded because they did not meet the eligibility criteria (n = 90) and the remaining 48% were either not accessible (n = 7), not in the English language (n = 26), could not be located (n = 22) or were identified as duplicates (n = 29, S4 File).
The duration of data-collection reported in articles ranged from less than 1 year to 27 years, excluding three studies that used multiple datasets [36, 49, 50]. The median duration of data collection was 3 years. Around 16% of articles used data collected over 10 or more years (n = 20). The earliest article included in the systematic map was published in 1980 (Fig 2A). We found a noticeable increase in the number of articles published in the past decade (2010 to 2020, n = 71), compared with the previous three decades (1980 to 2009, n = 52; Fig 2A). Studies designed to examine causal effects before and after an intervention were the most common and comprised 46% of the articles assessed (n = 57). Observational studies that quantified effects by observing sites or time periods exposed to different levels of intervention intensity accounted for around 28% of articles (n = 35). Approximately 15% of studies used designated control (non-treatment) and intervention (treatment) groups or sites (n = 19) and around 10% used a combined before-after-control-intervention study design (n = 12).
Number of articles by (a) publication year and (b) study design (BA = before-after, CI = control-intervention, BACI = before-after-control-intervention, and Obs = observation only). Totals are indicated by numerical values.
Geographical representativeness and coverage of articles
The geographic location of the studies reported in the articles included six regions (Fig 3). Europe was the most well-studied region with 69 articles. Oceania, North America and Asia were moderately well-studied with 25, 15 and 10 articles, respectively, while South America and Africa were the least-well studied regions with five articles between them. (Fig 3). The dataset used in the systematic map included articles from 28 countries (Fig 4). The most well-studied countries were Australia (n = 20), the UK (n = 16), USA (n = 13), France (n = 11) and Japan (n = 10, Fig 4). Study areas that covered more than one country were reported for five articles. The total area of land covered in each study ranged from less than 1 km2 to 175,000 km2. Articles most commonly covered study areas that were either 0–50 km2 or >600 km2 (Fig 5).
Totals are indicated by numerical values.
Colours indicate the frequency of article occurrences. The map was developed using the ’ggplot2’ and ’maps’ packages in R (www.R-project.org), which utilise public domain data from Natural Earth (www.naturalearthdata.com).
Species representativeness
The number of articles included in the systematic map for each of the ungulate species resident in the UK is presented (Fig 6, no relevant articles were identified for Chinese water deer). Multiple species were reported in 13 articles. Species were studied inside their native ranges in approximately 59% (n = 73) of articles and outside their native ranges in approximately 37% (n = 46) of articles. Around 3% (n = 4) of articles reported on multiple species, of which some were inside their native range and others were outside their native range. Wild pigs were the most well-studied species (n = 58), followed by red deer (n = 28) and roe deer (n = 23), whereas few studies reported on sika deer (n = 11), feral goats (n = 10), fallow deer (n = 5), feral sheep (n = 2) or Chinese muntjac (n = 2, Fig 6). Roughly equal numbers of articles reported on wild pigs inside (47%, n = 27) and outside (53%, n = 31) their native range. Articles that reported on roe deer (n = 23) and most of the articles that reported on red deer (93%, n = 26) and sika deer (91%, n = 10) were conducted inside their native ranges, while articles that reported on feral goats (n = 10), feral sheep (n = 2) and Chinese muntjac (n = 2), as well as the majority of articles for fallow deer (80%, n = 4), were conducted outside their native ranges.
Totals are indicated by numerical values. Patterns indicate the status of species studied in each article (native or non-native in relation to the geographic location of the study).
Types of interventions
Interventions were categorised and grouped into seven broader classes (Table 1). Multiple interventions were reported in 34 of the 123 included articles. Fig 7A presents the extent and distribution of articles in each intervention class. Shooting was the most well-studied intervention class and was examined in 78% of included articles (n = 96). The top three most frequently documented intervention classes (shooting, capture and poisoning) involved lethal interventions (Fig 7A). Supplementary feeding was the most well-studied non-lethal intervention class but was examined in less than 10% of articles (n = 12). The distribution of articles for native versus non-native species was roughly equal for shooting, supplementary feeding and contraception (Fig 7A). Articles that reported on the effects of poisoning (n = 13) and the majority of articles that reported on the effects of capture (88%, n = 14), focussed on non-native species. Whereas, articles that reported on the effects of deterrents (n = 5) and most of the articles that reported on the effects of barriers (80%, n = 4), examined native species. The most frequently documented interventions were ground-based shooting (n = 65), shooting with the assistance of dogs or human drivers (battues, n = 40), trapping (n = 16), shooting from an aerial vehicle (n = 13) and poisoning (n = 13, Fig 7B). The seven interventions that comprise the classes of barriers, contraception and deterrents (Table 1) were each reported in fewer than five articles (Fig 7B).
Number of articles by (a) intervention class and (b) intervention category. Totals are indicated by numerical values. Patterns indicate the status of species studied in each article (native, non-native or a mixture of native and non-native species), in relation to the geographic location of the study.
Interventions are categorised and assigned to a broad intervention class.
Types of outcome
The outcomes of interventions were categorised and grouped into five broad classes (Table 2). Multiple outcomes were reported in 39 of the 123 included articles. Fig 8A presents the number of articles for each outcome class. Demography and behaviour were the most well-studied outcome classes and were examined in 60% (n = 74) and 40% (n = 49) of included articles, respectively. Health, morphology and physiology were each reported in fewer than 5% of articles (Fig 8A). The most frequently documented outcomes were effects on population size (n = 49), spatial behaviour (n = 31), movement behaviour (n = 13), survival or mortality (n = 12) and habitat selection (n = 11, Fig 8B).
Number of articles by (a) outcome class and (b) outcome category. Totals are indicated by numerical values.
Outcomes are categorised and assigned to a broad outcome class.
Linkages between interventions and outcomes
Fig 9A displays the number of articles linking the interventions and outcomes (both grouped by class, Tables 1 and 2) identified in our systematic map. Well-studied linkages may be suitable areas of focus for more in-depth review and critical evaluation. Poorly studied linkages that are relevant to population management or policy and decision-making may be promising areas for further research or investigation by practitioners. Of the 35 possible linkages between interventions and outcomes, 15 were not identified in any article and a further 16 were reported in fewer than ten articles (Fig 9A). The most well-studied linkages were those of shooting and demography (n = 60), shooting and behaviour (n = 35), capture and demography (n = 14), and poisoning and demography (n = 13). The distribution of articles within each intervention and outcome class is presented for linkages between shooting and demography (Fig 9B) and shooting and behaviour (Fig 9C). Within the demography class the most frequently reported linkages were between population size and ground-based shooting (n = 28) or shooting with the assistance of drivers (n = 12, Fig 9B). No studies linking ground-based shooting with population genetics were identified. Within the behaviour class there was a more even distribution of articles amongst linkages (Fig 9C). The most frequently reported linkages were between spatial behaviour and ground-based shooting (n = 10) or shooting with the assistance of drivers (n = 14). The linkages between these interventions and habitat selection and movement were reported in 6 to 8 articles each (Fig 9C).
Structural matrices of the distribution and frequency of occurrence of studies reporting on the linkages between (a) intervention classes and outcome classes (b) shooting intervention categories and demography outcome categories and (c) shooting intervention categories and behaviour outcome categories for ungulate species resident in the UK. Matrix structure is adapted from McKinnon et al. [51].
Fig 10 maps the intersection of invention classes and outcome classes for each species. Shooting was the only intervention to be investigated across all eight reported species (Fig 10). Articles that examined species responses to contraception were identified for wild pigs, feral goats and fallow deer only. Evidence for the effects of deterrents was limited to studies of wild pigs, roe deer and sika deer, and the effects of poisoning were restricted to wild pigs and feral goats. For red deer and roe deer evidence was almost exclusively related to shooting. Wild pigs were the only species for which evidence was available on their responses to all seven of the intervention classes. Most of the articles found for sika deer examined behavioural responses. For feral goats, feral sheep and Chinese muntjac evidence was limited to the effects of interventions on demography only (Fig 10).
Discussion
Our review involved systematically mapping the existing worldwide research on the effects of population management interventions on the nine wild ungulate species that are resident in the UK. We collated peer-reviewed literature from 20 countries, supplemented by ’grey’ literature from UK-based sources to provide a species-specific summary of the evidence for commonly used interventions. The resulting map (S5 File) provides a resource for scholars, practitioners and decision-makers to more easily locate relevant articles, identify knowledge gaps and critically assess the state of the field.
General comments
The results from our review describe important characteristics of the evidence-base and reveal significant unevenness in the distribution of research across species, interventions and the types of outcomes examined. The literature search identified 123 relevant articles after screening for eligibility. There was an upward trend in papers published over time. More articles have been published in the last decade (2010 to 2020, n = 71) than in the preceding three decades (1980 to 2009, n = 52). Overall, the robustness of the evidence-base is low and dominated by comparatively short-term studies that collected data for a median duration of three years. Long-term studies using data collected over 10 or more years were rare and accounted for only 16% of articles (n = 20). The majority of studies were conducted over large areas > 50 km2 (n = 96), 27% of these involved areas > 600 km2. Most of the articles originated from Europe, Oceania and North America, which is consistent with the geographic ranges of the species examined [9, 52, 53].
Evidence extent
The relatively small number of articles included in our map (n = 123) most likely reflects a general trend towards studies evaluating the efficacy of management using only environmental-based indicators of ecological change [IEC, 15, 54]. A species is typically managed when its populations are negatively affecting human wellbeing, other species or ecosystem function [15]. Consequently, the outcomes reported by research are often environmental indicators, such as the frequency of ungulate-vehicle collisions, parasite loads and the growth rate/recruitment of plant species, and as such it often does not report metrics of the population of the wild ungulate species targeted by the intervention [14, 54]. Additionally, efforts to quantify ungulate species responses are constrained by limited human and financial resources. The notable scarcity of robust, long-term studies is likely due to the expense and logistical challenges associated with monitoring ungulate populations at the appropriate scale of the landscape or region [55, 56]. Technical advances and the decreasing cost of remote sensing technologies, such as motion-activated cameras and unmanned aerial vehicles, provide new opportunities for ungulate population monitoring, which can be used to overcome this deficit in the current evidence-base [57, 58].
Evidence distribution: Species
The top three most-studied species in our map, wild pigs, red deer and roe deer, are the most widely distributed ungulate species in Europe [9]. Wild pigs are invasive alien species throughout much of their range, which covers every continent except Antarctica [30, 59]. This was reflected in our results, which show that more than half (53%, n = 31) of the studies on wild pigs were conducted outside of their native range. They are generalist feeders that reproduce prolifically and are widely regarded as being one of the most destructive invasive species globally [32, 60, 61]. In contrast, almost all of the studies on red and roe deer were conducted within their native ranges (93% and 100% for red and roe deer, respectively). Both species are highly valued for recreational hunting and tourism [8], while overabundant populations can have a negative impact on woodland ecosystems, commercial forestry and agriculture, which makes them priority species for management [8, 9].
The top five countries with the highest frequency of articles were Australia, UK, USA, France and Japan. Feral goats and wild pigs are invasive alien species in Australia and USA and constitute a major threat to native biodiversity [62, 63]. Consequently, there is considerable interest in improving methods of population control and eradication [64–66]. With the exception of Chinese muntjac, all of the ungulate species resident in the UK are also present in France, so it is unsurprising that both countries make a large contribution to the existing evidence-base [9, 53]. The high frequency of studies in Japan is likely driven by the declining popularity of hunting in recent years, which has created a need to explore alternative interventions such as fencing and non-lethal deterrents [67–69].
Evidence distribution: Interventions
The distribution of evidence across different types of interventions is likely to be influenced by the effectiveness of the intervention, its availability and accessibility to practitioners as well as the range of legal restrictions and cultural views associated with its application. Our results show that a large majority of studies focus on various methods of shooting (78%), including shooting from the ground, from an aerial vehicle and shooting with the assistance of drivers (dogs or human battues). Shooting is popular for a variety of reasons. There is evidence supporting its effectiveness as a tool to mitigate ecological impacts [e.g., 70–72], it is relatively inexpensive [73] and hunting has an important significance in many cultures worldwide [74]. A key advantage of shooting is its specificity, which enables practitioners to target individuals or cohorts within the population (such as senescents, females or diseased individuals), that disproportionally contribute to ecological impacts or may be important for maintaining population health [10, 75]. In contrast, poisoning and capture (trapping and snaring) are less discriminate and so are typically only legally permitted for use on non-native invasive species. Our results show that poisoning and capture were studied for non-native species in 100% (n = 13) and 88% (n = 14) of articles, respectively.
The low proportion (20%) of articles that reported on non-lethal interventions is most likely due to the limited theoretical support for their effectiveness in mitigating ecological impacts. Although the precise relationship between impacts and ungulate population density is complex and context-specific, theoretically there exists a threshold above which species begin to put unsustainable pressure on the environment [33, 34, 76]. Most non-lethal interventions (barriers, diversionary feeding, repellents and deterrents) do not affect population density or reproductive performance and so are more likely to displace the environmental pressure caused by ungulates to other geographic areas, rather than bring about an overall reduction [77, 78]. Immunocontraception may be a viable alternative to lethal interventions and has been successfully developed for more than 85 different wildlife species [79]. However, most of the research on wildlife contraception has focussed on captive populations. There are several factors that currently inhibit the wider use of immunocontraceptive vaccines in free-ranging populations, including the variability of efficacy across species, limited long-term safety testing, the lack of effective delivery systems for elusive and mobile animals and concerns over the potential side-effects on behaviour [79]. Further research is needed to overcome these challenges and achieve general acceptance of immunocontraception as a management tool.
Evidence distribution: Outcomes
Our results show that most studies focused on population size and space-use outcomes. This is likely because there are established links between these responses and ecological impacts. For example, the relationship between wild ungulate population densities and indices of ecological impact (e.g., forest regeneration) has been investigated in several studies [e.g., 19, 76, 80] and variation in space-use has been linked to the distribution of damage [e.g., 81] as well as the spread of diseases [e.g., 82] and parasites [83]. The types of biological responses examined may also be influenced by data availability. Demographic responses, such as variations in population size, are likely to be observable over much shorter timeframes than changes in physiology or morphology, which require longer periods of population monitoring. Estimating population sizes is relatively straightforward and can be achieved using a range of techniques such as track counts, distance sampling and dung surveys, which require minimal resources. Cull records may also be utilised and are often the only source of population data regularly collected over long timeframes and at regional or national scales [55, 84]. Data on individual health, physiology and morphology are more challenging to collect. Considerable effort is needed to obtain the blood, tissue or whole-organism samples typically required for analyses. Furthermore, accurately measuring indicators of responses, such as stress hormone levels, body condition and the size and shape of anatomical features often requires expertise and specialist equipment that are unavailable to most practitioners [56].
Recommendations for policy and management
Members of the international scientific community recently advocated for the implementation of an adaptive approach to management of wild ungulate species based on a continuous and systematic process of trial-and-error [14]. They highlight the importance of evaluating the outcomes of management interventions using a set of environmental (e.g., browsing index, vegetation composition, ungulate-vehicle collisions) and population (e.g., body mass, antler quality, reproductive performance) indices. Our results show that, to date, very few studies have utilised population-based metrics beyond estimates of population-size. Therefore, we strongly support the existing call [14] for practitioners to record key information on the health, reproduction and genetic integrity of ungulate populations. We encourage a participatory approach to research, in which managers carrying out adaptive management, become integrated participants in the wider research programme.
As the financial and human resources available to managers are typically limited, it may be sensible firstly to exploit opportunities for broadening the types of data collected from sources already utilised by existing monitoring programmes. For example, cull records could include information on indicators of health, such as body mass, jaw length and antler quality [85]. Blood and tissue samples used for the monitoring of diseases, could also be made available for studies on population genetics and physiology [86, 87]. Data-sharing through collaborative projects, such as the EuroBoar (www.euroboar.org) and EuroDeer (www.eurodeer.org) networks, should be encouraged to facilitate comparative studies of populations under different socio-ecological conditions [56]. The results of alternative strategies are particularly valuable in finding novel solutions to management challenges. For example, a study by [88] proposed shooting in a way that creates a ‘landscape of fear’ to mimic the effects of a natural predator. Critically assessing approaches such as this would facilitate the refinement of existing practices and policies.
Recommendations for primary research
Researchers should focus on addressing knowledge gaps by conducting studies based on robust experimental designs (such as before-after-control-intervention) that account for different types of bias [89, 90]. Resources should be invested in long-term studies that collect data for 10 or more years, which would provide valuable knowledge on the long-term effects of management and species responses to environmental variation, such as climate and land-use changes [56]. We suggest the following three questions as research priorities: (1) how do ungulate species respond to non-lethal interventions (supplementary feeding, barriers, deterrents and administering contraception)? (2) what are the side-effects of shooting on ungulate (i) morphology, (ii) population genetics, (iii) physiology and (iv) species interactions? and (3) what are the effects of management interventions on sika deer and Chinese muntjac?
Non-lethal interventions provide important alternative methods of mitigating the impacts of ungulates in contexts where lethal interventions are not legally or socially acceptable to use (e.g., urban areas). Understanding species responses to non-lethal interventions is critical for developing more effective techniques and ensuring their long-term safety (e.g., exploring possible side-effects of contraceptives). More research on non-lethal interventions would also assist in identifying the combination of techniques that are most effective at the population-level scale of the landscape or region.
Identifying the side-effects of shooting is important for several reasons. Firstly, shooting is often a non-random process and individuals with certain morphological traits (e.g., large body mass or large antlers) may be preferentially targeted [36, 91]. This can place selection pressures on populations that can cause undesirable life-history changes over shorter time-periods than would be expected from natural selection [36, 92]. Secondly, the relatively slow rate of reproduction exhibited by ungulates puts them at risk of overexploitation [93, 94]. Extensive shooting and anthropogenic barriers (e.g., roads, buildings, fences etc.) can isolate populations, which may increase the rate of inbreeding (i.e., mating among closely related individuals), leading to inbreeding depression [i.e., the decreased fitness of inbred individuals, 93, 95]. Finally, shooting can affect the rate of contact between individuals, which may influence the spread of diseases [96, 97]. There is also evidence to suggest that the social stress of culling activities causes immunosuppression, leading to greater disease expression [98]. There is a need to better understand the full range of side-effects associated with shooting to ensure the long-term viability of ungulate populations and improve management efficiency.
Chinese muntjac and with sika deer, are among the worst invasive non-native species in Europe in terms of risk of causing environmental impacts [99, 100]. In the UK, high densities of Chinese muntjac have been associated with a range of impacts on native species of flora [101], birds [102] and invertebrates [103]. Sika deer present an additional threat to native ungulate species through hybridisation with native red deer populations [e.g., 104–106]. Reliably predicting the responses of Chinese muntjac and sika deer to management interventions is critical in developing effective strategies to reduce population spread. We recommend researchers initially focus on outcomes relating to population growth (e.g., population size, fecundity, survival etc.) and space-use (e.g., distributions, dispersal, movement rates), as they are likely to be the most important factors driving population expansion.
Recommendations for systematic reviews and meta-analyses
Scholars may look to expand this review by including a broader range of species. Widening the scope of the review to include North American species such as elk (Cervus elaphus canadensis), moose (Alces alces) and white-tailed deer (Odocoileus virginianus) is likely to yield a much greater volume of literature that may provide a more comprehensive overview of the evidence-base. Reviews that include a critical appraisal of the literature should prioritise estimating the relationship between outcomes and environmental factors (e.g., climate or land-use, analysed as ’effect modifiers’ if the data permit a meta-analysis to be carried out). Systematic reviews or meta-analyses are needed to assess the validity of transposing results from one geographic region or ecological context to another. Future reviewers may categorise studies by ecological context and critically evaluate the results to estimate the effects of environmental conditions on species responses.
Our map shows that shooting is the only intervention for which a sufficient volume of evidence currently exists to permit a meaningful systematic review or meta-analysis. Systematic reviews would provide insights on the quality of the literature as well as determining the magnitude, directionality and heterogeneity of effects between different species and ecological contexts (i.e., ’effect modifiers’). Systematic reviews and meta-analyses assessing the relationship between outcomes and variation in shooting practices (e.g., intensity, spatial scale, timing, selectivity) would be particularly valuable for understanding the mechanisms of how shooting works, and what modifiers affect species responses [8, 14].
Limitations of the search strategy
It is important to consider the limitations of the search strategy when interpreting our study results. Although the searches were comprehensive, finite time and resources prohibited actions, such as combing review papers, forward and backward screening of articles and searching additional databases, which may have yielded a greater number of relevant studies. The searches were also restricted to articles presented in the English language and ’grey’ literature was obtained from UK-based sources only. Efforts to build on this map should focus on expanding the geographic scope of the review by searching for studies from a wider range of sources, ideally through collaborations between multiple reviewers, which provide different institutional accesses and the option of screening articles in a broader range of languages. We also expect that a number of studies exist based on environmental IEC containing information on species responses to management that are not reported in the title or abstract. Such articles would have been excluded at the screening stages of our search strategy in its current form. We recommend that researchers consistently report population-based metrics and, where appropriate, include these details in their title, abstract or keyword list, which will enable future reviewers to more easily access this information.
Additionally, there are more general caveats associated with interpreting the outputs of systematic maps (for further details see CEE guidelines, www.environmentalevidence.org). Firstly, data were extracted to broadly characterise the evidence of linkages between interventions, outcomes and species. The synthesis did not extend to exploring the directionality of effects or estimating average effect sizes, as is typical of systematic reviews or meta-analyses. Secondly, the set of species responses covered in our study was derived from a synthesis of the included articles and is not exhaustive. Assessments of the literature related to other wild ungulate species may identify linkages between interventions and a wider range of outcomes than those reported by the studies in our map. Finally, although study designs give an indication of the robustness of evidence, our map does not provide a critical appraisal of the included articles. A detailed evaluation of how studies mitigate biases and account for heterogeneous effects is needed to more accurately assess the quality of the literature.
Conclusion
The management of wild ungulate populations should be informed by regular monitoring of both environmental and population-based indicators of ecological change [14, 15]. Our map reveals that the extent of the literature reporting on population-based responses to management is limited. The current lack of primary research constrains our ability to reliably predict the full range of effects an intervention will have on target species, which is critical for developing sustainable, effective and efficient strategies. We encourage researchers and practitioners to monitor a wider range of responses to interventions as an essential part of adaptive population management. New research and the articles identified in this review should be synthesized and, if reliable, utilized as the evidence-base for public policy and management practice decision-making. Although our results suggest that research effort in this field is increasing, the considerable gaps and biases in the current evidence-base need to be addressed before this knowledge can be transferred to real-world applications.
Supporting information
S4 File. Database of articles excluded at the full-text level.
https://doi.org/10.1371/journal.pone.0267385.s004
(XLSX)
Acknowledgments
The authors wish to thank Prof Andrew Pullin for his advice on methodologies for systematic mapping and Dr Alastair Ward for his assistance in defining the topic and scope of the review. We also thank Lee Oliver and David Jam for their support in identifying the needs of stakeholders and for providing a practical perspective on the current challenges faced by wildlife management practitioners. Finally, we would like to thank two anonymous reviewers for their comments and helpful feedback on the manuscript.
References
- 1. Manier DJ, Hobbs NT. Large herbivores in sagebrush steppe ecosystems: Livestock and wild ungulates influence structure and function. Oecologia. 2007;152(4):739–50. pmid:17375334
- 2. Fornara DA, Du Toit JT. Browsing-induced effects on leaf litter quality and decomposition in a southern African savanna. Ecosystems. 2008;11(2):238–49.
- 3. Murray BD, Webster CR, Bump JK. Broadening the ecological context of ungulate-ecosystem interactions: The importance of space, seasonality, and nitrogen. Ecology. 2013;94(6):1317–26. pmid:23923495
- 4. Ohashi H, Hoshino Y. Disturbance by large herbivores alters the relative importance of the ecological processes that influence the assembly pattern in heterogeneous meta-communities. Ecology and Evolution. 2014;4(6):766–75. pmid:24683459
- 5. Hobbs NT. Modification of Ecosystems by Ungulates. Journal of Wildlife Management. 1996;60(4):695–713.
- 6. Côté SD, Rooney TP, pierre Tremblay J, Dussault C, Waller DM. Ecological Impacts of Deer Overabundance. Annual Review of Ecology, Evolution, and Systematics. 2004;35(2004):113–47.
- 7. Dolman PM, Wäber K. Ecosystem and competition impacts of introduced deer. Wildlife Research. 2008;35(3):202–14.
- 8.
Apollonio M, Andersen R, Putman R. European ungulates and their management in the 21st century. Cambridge: Cambridge University Press; 2010. 1–14 p.
- 9. Linnell JDC, Cretois B, Nilsen EB, Rolandsen CM, Solberg EJ, Veiberg V, et al. The challenges and opportunities of coexisting with wild ungulates in the human-dominated landscapes of Europe’s Anthropocene. Biological Conservation. 2020 Apr 1;244.
- 10.
Putman R, Apollonio M, Andersen R. Ungulate Management in Europe: Problems and Practices. Cambridge: Cambridge University Press; 2011.
- 11. Lewis JS, Farnsworth ML, Burdett CL, Theobald DM, Gray M, Miller RS. Biotic and abiotic factors predicting the global distribution and population density of an invasive large mammal. Scientific Reports. 2017;7(March):1–12. pmid:28276519
- 12. Acevedo P, Farfán MÁ, Márquez AL, Delibes-Mateos M, Real R, Vargas JM. Past, present and future of wild ungulates in relation to changes in land use. Landscape Ecology. 2011;26(1):19–31.
- 13. Putman R, Langbein J, Hewison AJM, Sharma SK. Relative roles of density-dependent and density-independent factors in population dynamics of British deer. Mammal Review. 1996;26(213):81–101.
- 14. Apollonio M, Belkin V v., Borkowski J, Borodin OI, Borowik T, Cagnacci F, et al. Challenges and science-based implications for modern management and conservation of European ungulate populations. Mammal Research. 2017;1;62(3):209–17.
- 15. Carpio AJ, Apollonio M, Acevedo P. Wild ungulate overabundance in Europe: contexts, causes, monitoring and management recommendations. Mammal Review. 2021;1;51(1):95–108.
- 16. Osawa T, Hata K, Kachi N. Eradication of feral goats enhances expansion of the invasive shrub Leucaena leucocephala on Nakoudo-jima, an oceanic island. Weed Research. 2016;56(2):168–78.
- 17. Katona K, Kiss M, Bleier N, Székely J, Nyeste M, Kovács V, et al. Ungulate browsing shapes climate change impacts on forest biodiversity in Hungary. Biodiversity and Conservation. 2013 May;22(5):1167–80.
- 18. Eichhorn MP, Ryding J, Smith MJ, Gill RMA, Siriwardena GM, Fuller RJ. Effects of deer on woodland structure revealed through terrestrial laser scanning. Journal of Applied Ecology. 2017;1839.
- 19. Bleier N, Lehoczki R, Újváry D, Szemethy L, Csányi S. Relationships between wild ungulates density and crop damage in Hungary. Acta Theriologica. 2012;57(4):351–9.
- 20. Arrington DA, Beach WP. Effects of rooting by feral hogs Sus scrofa L. on the structure of a floodplain vegetation assemblage. Wetlands. 1999;19(3):535–44.
- 21. Siemann E, Carrillo JA, Gabler CA, Zipp R, Rogers WE. Experimental test of the impacts of feral hogs on forest dynamics and processes in the southeastern US. Forest Ecology and Management. 2009;258(5):546–53.
- 22. Singer FJ., Swank WT., Clebsch EE. C. Effects of Wild Pig Rooting in a Deciduous Forest. The Journal of Wildlife Management. 1984;48(2):464–73.
- 23. Seiler A. Trends and spatial patterns in ungulate-vehicle collisions in Sweden. Wildlife Biology. 2004;10(4):301–13.
- 24.
Langbein J, Putman R, Pokorny B. Traffic collisions involving deer and other ungulates in Europe and available measures for mitigation. In: Ungulate Management in Europe. Cambridge University Press; 2011. p. 215–59.
- 25. Groot GWTA, Hazebroek E. Ungulate Traffic Collisions in Europe. Conservation Biology. 1996;10(4):1059–67.
- 26. Martín-Hernando MP, Höfle U, Vicente J, Ruiz-Fons F, Vidal D, Barral M, et al. Lesions associated with Mycobacterium tuberculosis complex infection in the European wild boar. Tuberculosis. 2007;87(4):360–7. pmid:17395539
- 27. Sato Y, Kobayashi C, Ichikawa K, Kuwamoto R, Matsuura S, Koyama T. An occurrence of Salmonella Typhimurium infection in sika deer (Cervus nippon). Journal of Veterinary Medical Science. 2000;62(3):313–5. pmid:10770606
- 28. Gilbert L, Maffey GL, Ramsay SL, Hester AJ. The effect of deer management on the abundance of Ixodes ricinus in Scotland. Ecological Applications. 2012;22(2):658–67. pmid:22611862
- 29. Böhm M, White PCL, Chambers J, Smith L, Hutchings MR. Wild deer as a source of infection for livestock and humans in the UK. Veterinary Journal. 2007;174(2):260–76. pmid:17258479
- 30. Barrios-Garcia MN, Ballari SA. Impact of wild boar (Sus scrofa) in its introduced and native range: A review. Biological Invasions. 2012;14(11):2283–300.
- 31.
Putman R, Langbein J. The Deer Manager’s Companion: A Guide to the Management of Deer in the Wild and in Parks. Shrewsbury: Swan Hill Press; 2003. 29–60 p.
- 32. Bengsen AJ, Gentle MN, Mitchell JL, Pearson HE, Saunders GR. Impacts and management of wild pigs Sus scrofa in australia. Mammal Review. 2014;44(2):135–47.
- 33. Fattorini N, Lovari S, Watson P, Putman R. The scale-dependent effectiveness of wildlife management: A case study on British deer. Journal of Environmental Management. 2020 Dec 15;276. pmid:32947117
- 34. Putman R, Langbein J, Green P, Watson P. Identifying threshold densities for wild deer in the UK above which negative impacts may occur. Mammal Review. 2011;41(3):175–96.
- 35. Tanentzap AJ, Burrows LE, Lee WG, Nugent G, Maxwell JM, Coomes DA. Landscape-level vegetation recovery from herbivory: Progress after four decades of invasive red deer control. Journal of Applied Ecology. 2009;46(5):1064–72.
- 36. Rivrud IM, Sonkoly K, Lehoczki R, Csányi S, Storvik GO, Mysterud A. Hunter selection and long-term trend (1881–2008) of red deer trophy sizes in Hungary. Journal of Applied Ecology. 2013;50(1):168–80.
- 37. Jarnemo A, Wikenros C. Movement pattern of red deer during drive hunts in Sweden. European Journal of Wildlife Research. 2014;60(1):77–84.
- 38. Wäber K, Spencer J, Dolman PM. Achieving landscape-scale deer management for biodiversity conservation: The need to consider sources and sinks. Journal of Wildlife Management. 2013 May;77(4):726–36.
- 39. Rajský M, Vodňanský M, Hell P, Slamečka J, Kropil R, Rajský D. Influence supplementary feeding on bark browsing by red deer (Cervus elaphus) under experimental conditions. European Journal of Wildlife Research. 2008;54(4):701–8.
- 40. Bieber C, Ruf T. Population dynamics in wild boar Sus scrofa: Ecology, elasticity of growth rate and implications for the management of pulsed resource consumers. Journal of Applied Ecology. 2005;42(6):1203–13.
- 41. Simard MA, Dussault C, Huot J, Côté SD. Is hunting an effective tool to control overabundant deer? A test using an experimental approach. Journal of Wildlife Management. 2013;77(2):254–69.
- 42. Chynoweth MW, Lepczyk CA, Litton CM, Hess SC, Kellner JR, Cordell S. Home range use and movement patterns of non-native feral goats in a tropical island montane dry landscape. PLoS ONE. 2015;10(3):1–15.
- 43. Haddaway NR, Bernes C, Jonsson BG, Hedlund K. The benefits of systematic mapping to evidence-based environmental management. Ambio. 2016;1;45(5):613–20. pmid:26984257
- 44. Tilman D, Clark M, Williams DR, Kimmel K, Polasky S, Packer C. Future threats to biodiversity and pathways to their prevention. Nature. 2017;31;546(7656):73–81. pmid:28569796
- 45. Pullin AS, Frampton GK, Livoreil B, Petrokofsky G, Editors. Guidelines and Standards for Evidence synthesis in Environmental Management. Version 5.0 www.environmentalevidence.org/information-for-authors [accessed 25/06/21]. Collaboration for Environmental Evidence. 2018.
- 46. Haddaway NR, Macura B, Whaley P, Pullin AS. ROSES Reporting standards for Systematic Evidence Syntheses: Pro forma, flow-diagram and descriptive summary of the plan and conduct of environmental systematic reviews and systematic maps. Environmental Evidence. 2018 Mar 19;7(1).
- 47. Moher D, Liberati A, Tetzlaff J, Altman DG, Altman D, Antes G, et al. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Vol. 6, PLoS Medicine. 2009.
- 48. Keiter DA, Mayer JJ, Beasley JC. What is in a “common” name? A call for consistent terminology for nonnative Sus scrofa. Wildlife Society Bulletin. 2016;1;40(2):384–7.
- 49. Putman R, Nelli L, Matthiopoulos J. Changes in bodyweight and productivity in resource-restricted populations of red deer (Cervus elaphus) in response to deliberate reductions in density. European Journal of Wildlife Research. 2019;1;65(1).
- 50. Servanty S, Gaillard JM, Ronchi F, Focardi S, Baubet É, Gimenez O. Influence of harvesting pressure on demographic tactics: Implications for wildlife management. Journal of Applied Ecology. 2011;48(4):835–43.
- 51. McKinnon MC, Cheng SH, Dupre S, Edmond J, Garside R, Glew L, et al. What are the effects of nature conservation on human well-being? A systematic map of empirical evidence from developing countries. Environmental Evidence. 2016 Apr 27;5(1).
- 52. Acevedo P, Croft S, Smith GC, Blanco‐Aguiar JA, Fernandez‐Lopez J, Scandura M, et al. ENETwild modelling of wild boar distribution and abundance: update of occurrence and hunting data‐based models. EFSA Supporting Publications. 2019;16(8).
- 53. Croft S, Ward AI, Aegerter JN, Smith GC. Modeling current and potential distributions of mammal species using presence-only data: A case study on British deer. Ecology and Evolution. 2019;9(15):8724–35. pmid:31410275
- 54. Morellet N, Gaillard JM, Hewison AJM, Ballon P, Boscardin Y, Duncan P, et al. Indicators of ecological change: New tools for managing populations of large herbivores. Vol. 44, Journal of Applied Ecology. 2007. p. 634–43.
- 55. Putman R, Watson P, Langbein J. Assessing deer densities and impacts at the appropriate level for management: A review of methodologies for use beyond the site scale. Mammal Review. 2011;41(3):197–219.
- 56. Festa-Bianchet M, Douhard M, Gaillard JM, Pelletier F. Successes and challenges of long-term field studies of marked ungulates. Journal of Mammalogy. 2017;29;98(3):612–20.
- 57. Prosekov A, Kuznetsov A, Rada A, Ivanova S. Methods for monitoring large terrestrial animals in the wild. Vol. 11, Forests. MDPI AG; 2020.
- 58. Grignolio S, Apollonio M, Brivio F, Vicente J, Acevedo P, P. P, et al. Guidance on estimation of abundance and density data of wild ruminant population: methods, challenges, possibilities. EFSA Supporting Publications. 2020;17(6).
- 59. Massei G, Genov P v. The environmental impact of wild boar. Galemys. 2004;16:135–45.
- 60. McClure ML, Burdett CL, Farnsworth ML, Sweeney SJ, Miller RS. A globally-distributed alien invasive species poses risks to United States imperiled species. Scientific Reports. 2018;1;8(1).
- 61. Doherty TS, Glen AS, Nimmo DG, Ritchie EG, Dickman CR. Invasive predators and global biodiversity loss. Proc Natl Acad Sci U S A. 2016;4;113(40):11261–5. pmid:27638204
- 62. Hone J. How many feral pigs in Australia? An update. Australian Journal of Zoology. 2020;10;67(4):215–20.
- 63. Seward N, Vercauteren KC, Witmer GW, Engeman RM. Feral Swine Impacts on Agriculture and the Environment. Sheep & Goat Research Journal 12 Sheep & Goat Research Journal. 2004;19.
- 64. Masters P, Markopoulos N, Florance B, Southgate R. The eradication of fallow deer (Dama dama) and feral goats (Capra hircus) from Kangaroo Island, South Australia. Australasian Journal of Environmental Management. 2018;2;25(1):86–98.
- 65. Heriot S, Asher J, Williams MR, Moro D. The eradication of ungulates (sheep and goats) from Dirk Hartog Island, Shark Bay World Heritage Area, Australia. Biological Invasions. 2019;15;21(5):1789–805.
- 66. McIlroy JC. New techniques for an old problem—recent advances in feral pig control in Australia. Ibex JME. 1995;3:241–4.
- 67. Kaji K, Saitoh T, Uno H, Matsuda H, Yamamura K. Adaptive management of sika deer populations in Hokkaido, Japan: Theory and practice. Vol. 52, Population Ecology. 2010. p. 373–87.
- 68. Honda T. A Sound Deterrent Prevented Deer Intrusions at the Intersection of a River and Fence. Mammal Study. 2019;44(4):269–74.
- 69. Honda T, Kubota Y, Ishizawa Y. Ungulates-exclusion grates as an adjoining facility to crop damage prevention fences. European Journal of Wildlife Research. 2020;1;66(1).
- 70. Giménez-Anaya A, Herrero J, García-Serrano A, Garcíagonzález R, Prada C. Wild boar battues reduce crop damages in a protected area. Folia Zoologica. 2016;1;65(3):214–20.
- 71. Hothorn T, Müller J. Large-scale reduction of ungulate browsing by managed sport hunting. Forest Ecology and Management. 2010;260(9):1416–23.
- 72. Quirós-Fernández F, Marcos J, Acevedo P, Gortázar C. Hunters serving the ecosystem: the contribution of recreational hunting to wild boar population control. European Journal of Wildlife Research. 2017;1;63(3).
- 73. Gentle M, Pople A. Effectiveness of commercial harvesting in controlling feral-pig populations. Wildlife Research. 2013;40(6):459–69.
- 74.
Alves RRN, Souto WMS, Fernandes-Ferreira H, Bezerra DMM, Barboza RRD, Vieira WLS. The Importance of Hunting in Human Societies. In: Ethnozoology Animals in our Lives. Elsevier Inc.; 2018. p. 95–118.
- 75. Gordon IJ, Hester AJ, Festa-Bianchet M. The management of wild large herbivores to meet economic, conservation and environmental objectives. Journal of Applied Ecology. 2004;41(6):1021–31.
- 76. Spake R, Bellamy C, Gill R, Watts K, Wilson T, Ditchburn B, et al. Forest damage by deer depends on cross-scale interactions between climate, deer density and landscape structure. Journal of Applied Ecology. 2020;1;57(7):1376–90.
- 77. Valente AM, Acevedo P, Figueiredo AM, Fonseca C, Torres RT. Overabundant wild ungulate populations in Europe: management with consideration of socio-ecological consequences. Mammal Review. 2020;1;50(4):353–66.
- 78. Geisser H, Reyer HU. Efficacy of hunting, feeding and fencing to reduce crop damage by wild boars. Journal of Wildlife Management. 2004;68(4):939–46.
- 79. Kirkpatrick JF, Lyda RO, Frank KM. Contraceptive Vaccines for Wildlife: A Review. American Journal of Reproductive Immunology. 2011;66(1):40–50. pmid:21501279
- 80. Nuttle T, Ristau TE, Royo AA. Long-term biological legacies of herbivore density in a landscape-scale experiment: Forest understoreys reflect past deer density treatments for at least 20 years. Journal of Ecology. 2014;102(1):221–8.
- 81. Thurfjell H, Spong G, Ericsson G. Effects of hunting on wild boar Sus scrofa behaviour. Wildlife Biology. 2013 Mar;19(1):87–93.
- 82. Magle SB, Kardash LH, Rothrock AO, Chamberlin JC, Mathews NE. Movements and habitat interactions of white-tailed deer: Implications for chronic wasting disease management. American Midland Naturalist. 2015;1;173(2):267–82.
- 83. Mysterud A, Qviller L, Meisingset EL, Viljugrein H. Parasite load and seasonal migration in red deer. Oecologia. 2016;1;180(2):401–7. pmid:26450650
- 84. Engeman RM, Massei G, Sage M, Gentle MN. Monitoring wild pig populations: A review of methods. Environmental Science and Pollution Research. 2013;20(11):8077–91. pmid:23881593
- 85. Ramanzin M, Sturaro E. Habitat quality influences relative antler size and hunters’ selectivity in roe deer. European Journal of Wildlife Research. 2014;60(1):1–10.
- 86. Réveillaud É, Desvaux S, Boschiroli ML, Hars J, Faure É, Fediaevsky A, et al. Infection of wildlife by Mycobacterium bovis in France Assessment through a national surveillance system, Sylvatub. Frontiers in Veterinary Science. 2018;30;5. pmid:30430112
- 87. Martin C, Pastoret PP, Brochier B, Humblet MF, Saegerman C. A survey of the transmission of infectious diseases/infections between wild and domestic ungulates in Europe. Veterinary Research. 2011;42(1). pmid:21635726
- 88. Cromsigt JPGM, Kuijper DPJ, Adam M, Beschta RL, Churski M, Eycott A, et al. Hunting for fear: Innovating management of human-wildlife conflicts. Journal of Applied Ecology. 2013;50(3):544–9.
- 89. Christie AP, Amano T, Martin PA, Shackelford GE, Simmons BI, Sutherland WJ. Simple study designs in ecology produce inaccurate estimates of biodiversity responses. Journal of Applied Ecology. 2019;1;56(12):2742–54.
- 90. Smokorowski KE, Randall RG. Cautions on using the Before-After-Control-Impact design in environmental effects monitoring programs. FACETS. 2017;1;2(1):212–32.
- 91. Mysterud A, Bischof R. Can compensatory culling offset undesirable evolutionary consequences of trophy hunting? Journal of Animal Ecology. 2010;79(1):148–60. pmid:19840171
- 92. Carroll SP, Hendry AP, Reznick DN, Fox CW. Evolution on ecological time-scales. Functional Ecology. 2007;21(3):387–93.
- 93. de Jong JF, van Hooft P, Megens HJ, Crooijmans RPMA, de Groot GA, Pemberton JM, et al. Fragmentation and Translocation Distort the Genetic Landscape of Ungulates: Red Deer in the Netherlands. Frontiers in Ecology and Evolution. 2020;29;8.
- 94. Ripple WJ, Newsome TM, Wolf C, Dirzo R, Everatt KT, Galetti M, et al. Collapse of the world’s largest herbivores. Vol. 1, Science Advances. American Association for the Advancement of Science; 2015. pmid:26601172
- 95. Ralls K, Ballou JD, Dudash MR, Eldridge MDB, Fenster CB, Lacy RC, et al. Call for a Paradigm Shift in the Genetic Management of Fragmented Populations. Conservation Letters. 2018;1;11(2).
- 96. Miguel E, Grosbois V, Caron A, Pople D, Roche B, Donnelly CA. A systemic approach to assess the potential and risks of wildlife culling for infectious disease control. Communications Biology. 2020;1;3(1). pmid:32636525
- 97. Prentice JC, Fox NJ, Hutchings MR, White PCL, Davidson RS, Marion G. When to kill a cull: Factors affecting the success of culling wildlife for disease control. Journal of the Royal Society Interface. 2019;1;16(152).
- 98. Riordan P, Delahay RJ, Cheeseman C, Johnson PJ, Macdonald DW. Culling-induced changes in badger (Meles meles) behaviour, social organisation and the epidemiology of bovine tuberculosis. PLoS ONE. 2011;14;6(12). pmid:22194946
- 99. Volery L, Jatavallabhula D, Scillitani L, Bertolino S, Bacher S. Ranking alien species based on their risks of causing environmental impacts: A global assessment of alien ungulates. Global Change Biology. 2021;1;27(5):1003–16.
- 100. Nentwig W, Bacher S, Kumschick S, Pyšek P, Vilà M. More than “100 worst” alien species in Europe. Biological Invasions. 2018;1;20(6):1611–21.
- 101. Cooke AS. Effects of grazing by muntjac (Muntiucus reevesi) on bluebells (Hyucinthoides non-scripta) and a field technique for assessing feeding activity. Journal of the Zoological Society of London. 1997;242:365–9.
- 102. Gill RMA, Fuller RJ. The effects of deer browsing on woodland structure and songbirds in lowland Britain. Ibis. 2007;149(2):119–27.
- 103. Pollard E, Cooke AS. Impact of muntjac deer Muntiacus reevesi on egg-laying sites of the white admiral butterfly Ladoga camilla in a Cambridgeshire wood. Biological Conservation. 1994;70:189–91.
- 104. Smith SL, Senn H v., Pérez-Espona S, Wyman MT, Heap E, Pemberton JM. Introgression of exotic Cervus (nippon and canadensis) into red deer (Cervus elaphus) populations in Scotland and the English Lake District. Ecology and Evolution. 2018;1;8(4):2122–34. pmid:29468030
- 105. Biedrzycka A, Solarz W, Okarma H. Hybridization between native and introduced species of deer in Eastern Europe. Journal of Mammalogy. 2012;93(5):1331–41.
- 106. McFarlane SE, Hunter DC, Senn H v., Smith SL, Holland R, Huisman J, et al. Increased genetic marker density reveals high levels of admixture between red deer and introduced Japanese sika in Kintyre, Scotland. Evolutionary Applications. 2020;13:432–41. pmid:31993087