RESEARCH ARTICLE
Assessing Animal Welfare Impacts in the
Management of European Rabbits
(Oryctolagus cuniculus), European Moles
(Talpa europaea) and Carrion Crows (Corvus
corone)
a11111
Sandra E. Baker1*, Trudy M. Sharp2, David W. Macdonald1
1 Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, Oxford, Oxfordshire,
United Kingdom, 2 Fowlers Gap Arid Zone Research Station, Centre of Ecosystem Science, School of
Biological, Earth and Environmental Sciences, University of New South Wales, Kensington, NSW 2052,
Australia
* sandra.baker@zoo.ox.ac.uk
OPEN ACCESS
Citation: Baker SE, Sharp TM, Macdonald DW
(2016) Assessing Animal Welfare Impacts in the
Management of European Rabbits (Oryctolagus
cuniculus), European Moles (Talpa europaea) and
Carrion Crows (Corvus corone). PLoS ONE 11(1):
e0146298. doi:10.1371/journal.pone.0146298
Editor: Kathleen R. Pritchett-Corning, Harvard
University Faculty of Arts and Sciences, UNITED
STATES
Received: June 4, 2015
Accepted: December 15, 2015
Published: January 4, 2016
Copyright: © 2016 Baker 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 Statement: All relevant data are
within the paper and its Supporting Information files.
Funding: SB was supported by a fellowship from the
Humane Society International/UK (http://www.hsi.org/
world/united_kingdom/) and the Elinor Patterson
Baker Foundation (https://fdo.foundationcenter.org/
grantmaker-profile?collection = grantmakers&key=
BAKE011&page=8&from_search=1/). TS received no
specific funding for this work. DM was supported by
funding from Dr and Mrs Tom Kaplan and the
Peoples’ Trust for Endangered Species (http://ptes.
Abstract
Human-wildlife conflict is a global issue. Attempts to manage this conflict impact upon wild
animal welfare, an issue receiving little attention until relatively recently. Where human activities harm animal welfare these effects should be minimised where possible. However, little is
known about the welfare impacts of different wildlife management interventions, and opinions
on impacts vary widely. Welfare impacts therefore need to be assessed objectively. Our
objectives were to: 1) establish whether an existing welfare assessment model could differentiate and rank the impacts of different wildlife management interventions (for decision-making
purposes); 2) identify and evaluate any additional benefits of making formal welfare assessments; and 3) illustrate issues raised by application of the model. We applied the welfare
assessment model to interventions commonly used with rabbits (Oryctolagus cuniculus),
moles (Talpa europaea) and crows (Corvus corone) in the UK. The model ranked interventions
for rabbits (least impact first: fencing, head shot, chest shot) and crows (shooting, scaring,
live trapping with cervical dislocation). For moles, managing molehills and tunnels scored
least impact. Both spring trapping, and live trapping followed by translocation, scored greater
impacts, but these could not be compared directly as they scored on different axes of the
model. Some rankings appeared counter-intuitive, highlighting the need for objective formal
welfare assessments. As well as ranking the humaneness of interventions, the model
highlighted future research needs and how Standard Operating Procedures might be
improved. The model is a milestone in assessing wildlife management welfare impacts, but
our research revealed some limitations of the model and we discuss likely challenges in
resolving these. In future, the model might be developed to improve its utility, e.g. by refining
the time-scales. It might also be used to reach consensus among stakeholders about relative
welfare impacts or to identify ways of improving wildlife management practice in the field.
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
1 / 24
Assessing Animal Welfare Impacts in Wildlife Management
org/). Publication fees were provided by the Humane
Society International. The funders had no role in
study design, data collection and analysis, or decision
to publish. Andrew Rowan of HSI/US and Mark Jones
previously of HSI/UK made helpful comments on an
earlier draft of the paper but had no other role in
preparation of the manuscript.
Competing Interests: The authors have declared
that no competing interests exist.
Introduction
Human-wildlife conflict is a pervasive global issue [1], with diverse causes [2] (e.g. competition
for food or other resources [3], damage to livestock [4] or property [5], threats to conservation
[6] and risk of disease spread [7, 8], injury or death [2, 9]), and it occurs in a wide variety of circumstances (agriculture, game-rearing, fisheries, forestry, food processing, amenities, business
and domestic settings [e.g. [10–12]). As well as threatening livelihoods, conservation and
human lives, human-wildlife conflict costs many millions of US dollars per annum globally,
e.g. annual livestock losses through depredation alone have been estimated at US$171 million
in South Africa [13], while livestock losses to coyotes, in the USA, cost US$40 million [14]. As
the global human population continues to grow and people and wildlife are forced into closer
proximity, human-wildlife conflicts [15, 16] and human impacts on wild animals [17] are set
to increase.
Typically, people try to manage human-wildlife conflict, and there may even be a legal obligation on a land owner or manager to kill, or otherwise control, certain species (e.g., in Britain,
rabbits, hares (Lepus europaeus), rats (Rattus norvegicus), mice (Mus musculus), deer (e.g.
Dama dama, Capreolus capreolus), foxes (Vulpes vulpes), moles and certain birds, under the
Pests Act 1954 [18], the Prevention of Damage by Pests Act 1949 [19] or the Agriculture Act
1947 [20]). While lethal and non-lethal methods are available (their suitability depending on
the species and circumstances concerned), some managers may rely heavily on lethal methods
(e.g. shooting, snaring, poisoning, gassing, spring trapping [spring traps are lethal traps powered by a spring]) [21], especially in the management of carnivores [2], where there may be an
element of retaliation involved if livestock have been killed [22]. Sometimes, where a species is
perceived as living at high density, lethal control may be a matter of tradition or conducted
prophylactically, or simply routinely, e.g. some mole catching in Britain [23]. Many non-lethal
methods are available, with some having been used for centuries, e.g. scarecrows [24]. Some
non-lethal methods are widely used (e.g. habitat management, fencing, tree-guards, scaring
devices), while some are used in particular scenarios (e.g. fertility control, diversionary feeding,
translocation), and others (e.g. learned food aversions) require further development [21, 25].
Whether lethal or non-lethal methods are used, wildlife management clearly has the capacity
to impact upon the welfare of target (and non-target) animals [26]. Where people adversely
affect the welfare of animals there is an ethical obligation to minimise this impact where possible, and it is important to consider seriously whether control is necessary and, if so, to use the
most humane option available that achieves the desired aims, whether lethal or non-lethal [27].
Humane, in this sense, and the sense used throughout this paper, means that pain, suffering
and distress is avoided or minimised [28]. It is important however to note that ‘humane’ is
sometimes used by other authors, or in general use in different cultures, to convey other concepts e.g. ethical, or non-lethal (e.g. see ‘humane mole tube traps’ in Baker et al [29]).
The importance of animal welfare is gathering recognition internationally [30]. However,
until the second half of the 20th century, relatively little attention was paid to anthropogenic
impacts on the welfare of wild animals, compared to domestic and laboratory animals [31]. In
the 1950s and 60s spring trap regulation was introduced and certain traps and poisons were
banned in the UK. In the 1980s and 1990s a number of papers were published on the welfare
impacts of traps on wildlife, e.g. by Warburton and Zelin and their respective colleagues [32,
33], and International Organization for Standardization (ISO) trap standards were developed
[34, 35]. Recent studies have addressed wild animal welfare considerations in wildlife reintroductions [36], the wildlife trade [37], the exotic pet trade [38], and wildlife tourist attractions
[39]. Nevertheless, even in the 21st century, the welfare of wild animals continues to lag behind,
with even animal welfare scientists paying the issue little attention until recently [40]. Indeed,
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
2 / 24
Assessing Animal Welfare Impacts in Wildlife Management
in 2008, David Fraser used wolves, pigs and dogs as examples, to contrast the way, even now,
people in Western cultures treat wild, farmed and pet animals with similar capacities for suffering [41]. The welfare of pest animals has been particularly undervalued [15], but now respect
for wild animal welfare is growing rapidly [2, 15, 42, 43] and there is increasing concern,
among the wider community in some parts of the world, regarding the acceptability of killing
wild animals considered pests [2, 16, 42].
Legislative changes also reflect greater attention to wild animal welfare. For example, in the
late 1990s, Europe signed the Agreement on International Humane Trapping Standards with
Canada, Russia and the United States of America, which banned the import of wild fur products unless they come from countries where leg hold traps are prohibited and where trapping
methods meet internationally-agreed welfare standards. Also, wild animals in Britain have
recently been granted wider protection through the Wild Mammals Protection Act 1996 [44],
the Protection of Wild Mammals (Scotland) Act 2002 [45], the Hunting Act 2004 [46], the
Animal Welfare Act 2006 [47] and the Animal Health and Welfare (Scotland) Act 2006 [48].
Under the Wild Mammals Protection Act it is an offence, except under certain exemptions, to
mutilate, kick, beat, nail or otherwise impale, stab, burn, stone, crush, drown, drag or asphyxiate any wild mammal with intent to inflict unnecessary suffering [44]. The Animal Welfare Act
introduces a general duty of care for all animals under the control of man, including wild vertebrates held captive or restrained by man’s actions, e.g., caught in a net or snare, held in the
hand, in an enclosure, pen or cage trap or during transportation [49].
Selection of a wildlife management method may be influenced by many factors, including
its perceived humaneness, efficacy, cost-effectiveness, target specificity, practicality, ease of
application, speed of effect, durability, legality (e.g. statutory restrictions/requirements), safety
for operators and other people, environmental impact, acceptability to the public and, to some
extent, how tolerable any conflict is perceived to be. If the management has another aim, this
may be an additional consideration, e.g. if the animal is to be harvested for fur then it might
need to be live-trapped and killed followed by immediate skinning. Humaneness should (and
is increasingly likely to) be taken into account in deciding whether and how wild animals are
managed [2, 43]. Littin et al. [27] propose that, as well as using the most humane management
methods that achieve the aims in any given situation, people should aim to maximise the
humaneness of existing methods and to identify new methods that are more humane. However, there is little reliable information available with which to evaluate and compare the
humaneness of wildlife management methods [42], and the opinions of wildlife managers on
the humaneness of a management method may vary widely, for example, depending on which
stakeholder group the manager belongs to and whether they believe they have suffered losses to
the species in question [4, 50]. This may be related to the fact that the perceived importance of
humaneness in choosing a management method also varies with stakeholder group. There is
therefore a clear need for objective assessment of the welfare impacts of different methods, so
that humaneness may be considered without bias when deciding on a course of wildlife management action [27, 42].
Assessing animal welfare is notoriously difficult [51–53], but various approaches have been
used [41], and a large number of objective and semi-objective measures proposed (e.g., physiological and behavioural [54]), for determining the welfare state of an animal [30]. However, a
key problem in assessing animal welfare can be that interpretation of the many proposed objective welfare measures requires some subjective judgement [42], which may be influenced by
the assessor’s regard for the animal involved [52]. Also, no single measure is likely to represent
adequately an animal’s welfare status and there are potential problems associated with combining separate indicators to estimate overall welfare impact. In 1979, The Farm Animal Welfare
Council was charged with advising the UK government on farm animal welfare and produced
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
3 / 24
Assessing Animal Welfare Impacts in Wildlife Management
its Five Freedoms to define the ideal physical and mental states for an animal [55]. Today these
are expressed as: 1. freedom from hunger and thirst; 2. freedom from discomfort; 3. freedom
from pain, injury or disease; 4. freedom to express normal behaviour; and 5. freedom from fear
and distress [56]. In 1994, Mellor and Reid developed, from the Five Freedoms, five ‘domains
of potential [welfare] compromise’ to produce a system for assessing the welfare impacts of a
proposed animal experiment or usage [57]. This, and a revised version, have been used in New
Zealand since 1997 to assess and record the level of animal welfare compromise imposed by
research, testing and teaching [42, 58]. Mellor and Reid’s five welfare domains consider
impacts on an animal’s nutrition, environment, health, behaviour and mental state. Their system was designed to be comprehensive, aiming to capture all possible welfare impacts, such
that the welfare impact outcome identified depends on all five domains, without the need to
combine or weight scores in any way (which could create unplanned biases) [53]. Their system
has been adapted for use with farm animals [59] and pests [60, 61], and incorporated into the
Zoo and Aquarium Association’s animal welfare position statement [62]; the five domains
model and other systems devised for assessing farm animal welfare are reviewed by Botreau
et al. [63, 64]. In 1994, Kirkwood and co-authors examined ways of assessing adverse human
impacts on the welfare of free-living wild animals [31]. They proposed that the welfare impact
of human interventions could be evaluated by considering: 1) the nature of the harm caused; 2)
the duration of the harm; 3) the numbers of animals affected; and 4) their capacity for suffering. Then, in 1999, Broom suggested that an estimate of the severity of a pest management procedure could be obtained by multiplying the extent of poor welfare by its duration [65].
In 2008, Sharp and Saunders developed a model for assessing the relative humaneness of
pest animal management interventions in Australia [42, 66]. This has been used to assess the
welfare impact of various management interventions on a range of wild vertebrates in Australia
and New Zealand [26, 42]. The model allows for the assessment of a wide range of both lethal
and non-lethal management interventions. It provides a systematic, comprehensive and transparent process designed to promote consensus among stakeholders about the humaneness of
management interventions. Evidence-based assessments are made using information from the
literature regarding the animal’s physiological, behavioural and pathological responses to a
particular intervention. Assessments involve thorough literature searching and the documentation of evidence. Sharp and Saunders developed their model in collaboration with stakeholders,
with particular expertise in animal welfare and pest management, including farming groups,
animal welfare organisations, government and non-government land managers and the community. The authors reported that the final model received widespread support from stakeholders, with most considering it effective and practical [42].
To demonstrate the use of the Sharp and Saunders’ model (‘the model’), we assessed the relative welfare impacts (on target animals) for three commonly used interventions for managing
each of European rabbits, European moles and carrion crows. These species were chosen as
they are widely regarded as pests in Britain [67–69] and elsewhere in Europe [70–72], a range
of options for their management are available and data were likely to be available for use with
the model. Our objectives were to: 1) determine whether the model could be used to differentiate and rank, systematically, the impacts of different wildlife management interventions used
with each species (thereby providing a basis for decision-making); 2) demonstrate the value of
making formalised welfare assessments in identifying interventions, or components of interventions, that pose a relatively greater welfare threat, or which are currently under-researched
and poorly understood; and 3) to identify issues raised by application of the model. These
objectives were achieved.
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
4 / 24
Assessing Animal Welfare Impacts in Wildlife Management
Materials and Methods
Standard operating procedures (SOPs)
The humaneness of wildlife management depends on which intervention is used, how it is
applied and the skill of the operator [42]. Variation in details, such as doses, frequency of trap
inspection, speed and skill in handling animals, confirmation of death etc, may have a significant effect on the level and duration of any welfare impact and so the exact details of a management intervention are crucial in determining its welfare and other outcomes. A welfare
assessment therefore needs to apply to a particular standard operating procedure (SOP) that
makes explicit the exact methodology of the intervention. Meaningful comparison of the welfare impacts of different management interventions is only possible if SOPs are followed. As
well as providing the basis for making welfare assessments, a SOP allows uniform implementation of ‘best practice’ wildlife management, and management skills training, and by standardising the details of a management intervention, welfare impacts may be reduced or prevented
[42].
Before developing their welfare assessment model (‘the model’), Sharp and Saunders produced a series of SOPs covering various management interventions used with invasive species
in Australia [73]). SOPs are generally not available for wildlife management interventions in
Britain and so we developed British SOPs, covering three management interventions used with
each of rabbits, moles and crows (these are listed in Table 1 and the full SOPs are available at
S1–S8 SOPs). We followed the format of Sharp’s SOPs as a guide [73]. Our SOPs were designed
to incorporate best practice as described in a variety of relevant sources, including Natural
England Information Notes and Advice Notes, Codes of Practice (produced by the Department
of Environment, Food and Rural Affairs (DEFRA), British Association for Shooting and Conservation (BASC), the Game and Wildlife Conservation Trust (GWCT) and the National
Farmers Union (NFU)), Forestry Authority Practice Notes, Natural England Licenses, Australian government SOPs (produced by Sharp and Saunders), reports by the Ministry of Agriculture Fisheries and Food (MAFF) and by its successor, DEFRA, and by the Pesticides Safety
Directorate (PSD), product manufacturers’ instructions and safety information, the scientific
literature and books. These SOPs do not constitute advice and have been produced for the purposes of this study only.
Assessments
The model comprises parts A and B. Part A is based on Mellor and Reid’s five welfare impact
domains [57] and examines the impact of a lethal or non-lethal management intervention on
an individual animal’s welfare, and the duration of this impact. For lethal interventions, Part A
of the assessment examines only the impact before the action causing death, while for nonlethal interventions it examines the impact of the whole procedure. We refer to this as the
‘non-lethal welfare impact’ (although Sharp and Saunders called it the ‘overall welfare impact’
[42]). Part B of the model applies only to lethal interventions and is based on Broom’s suggested approach [65]. It assesses the impact on welfare of any killing method involved, by evaluating the intensity and duration of suffering caused by the killing technique alone. Therefore
lethal interventions were scored under both Parts A and B, and non-lethal interventions under
Part A only.
Part A impacts were considered under five separate domains: 1) water deprivation, food
deprivation or malnutrition; 2) environmental challenge; 3) injury, disease, functional
impairment; 4) behavioural, interactive restriction; 5) anxiety, fear, pain, distress, thirst, hunger
etc. A welfare impact category (‘no impact’, ‘mild impact’, ‘moderate impact’, ‘severe impact’
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
5 / 24
Assessing Animal Welfare Impacts in Wildlife Management
Table 1. Details of the eight standard operating procedures created and the nine associated welfare assessments (both head and chest shots for
rabbits are covered by a single SOP).
Rabbits
Moles
Crows
Standard Operating
Procedure (SOP)
Welfare assessment
Summary of main features
Shooting rabbits (S1 SOP)
Shooting rabbits; head shot
Head shot, specified rifle or shotgun (depending on distance),
specified ammunition, lamp used if at night
Shooting rabbits; chest shot
Chest shot, specified rifle or shotgun (depending on distance),
specified ammunition, lamp used if at night
Fencing rabbits from crops
(S2 SOP)
*Fencing rabbits from crops
(installation); Fencing rabbits from crops
(established)
Permanent, non-electric, wire-mesh fencing, around wheat field,
installed after harvest/before winter planting. Assessments for 2
month period at installation (Sept-Oct) and again once established
(spring)
Spring trapping moles (S3
SOP)
Spring trapping moles
Scissor, Duffus or Talpa spring traps that meet welfare approval
standards, during spring (but outside breeding period), checked
every 24 hours
Live trapping and
translocation of moles (S4
SOP)
*Live trapping moles; Translocating
moles
Plastic tube traps, with food (earthworms), no bedding, during
spring (but outside breeding period), checked every 4 hours. Softrelease at suitable and apparently unoccupied sites, in man-made
chambers with bedding and food, released during spring (but
outside breeding period)
Managing molehills and
tunnels (S5 SOP)
Managing molehills and tunnels on
lawns
Molehill soil carefully lifted using a shovel or spade, and
redistributed elsewhere, surface tunnels gently trodden down
Shooting crows (S6 SOP)
Shooting crows
Chest shot; specified shotgun; specified ammunition; daylight hours
only; outside breeding period; under Natural England General
Licence WML-GL04
Cage trapping and cervical
dislocation of crows (S7 SOP)
Cage trapping with cervical dislocation
of crows
Single-capture Larsen traps, checked every 24 hours; outside
breeding period; under Natural England General Licence
WML-GL04
Scaring crows using gas guns
(S8 SOP)
Scaring crows using gas guns
Propane or acetylene gas guns; daylight only; outside breeding
period. Assessments for 2 month period between harvest and
winter wheat planting (Sept-Oct)
*In two cases, above, we made two separate assessments: 1) where a method consisted of two non-lethal parts (live trapping moles followed by
translocation); and 2) where a method consisted of two separable phases (installation of a rabbit fence in autumn, and once the fence was established the
following spring).
doi:10.1371/journal.pone.0146298.t001
or ‘extreme impact’) was assigned for each domain by referring to a set of impact scales for
Part A (S1–S5 Tables). The impact categories assigned reflected the level of impact at the time
of maximum impact. Where there was insufficient information to assign a single impact category, a range of categories was assigned, e.g. moderate to severe impact, and supporting references cited where appropriate. The score in domain 5 was assessed as the cumulative effect of
the other four domains. This was usually equivalent to the maximum impact assigned to any of
the domains 1–4, but could be greater. Ultimately the overall impact category for the management intervention was determined; this was usually the same as the category assigned to
domain 5 (mental state), but if domain 5 could not be assessed for some reason then the overall
impact category would be based on the level of welfare compromise under the other domains.
Next, the duration of the impact (‘immediate/seconds’, ‘minutes’, ‘hours’, ‘days’, ‘weeks’) was
determined. Then, the scoring matrix for Part A (S6 Table) was consulted, using the overall
impact category, and the duration of that impact, to identify the non-lethal welfare impact of
the intervention (ranging between 1 [no impact] and 8 [maximum impact]). Crucially, the scientific evidence for the impact scores assigned to the five domains was recorded as referenced
notes.
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
6 / 24
Assessing Animal Welfare Impacts in Wildlife Management
To make an assessment under Part B, the time to insensibility from the application of the
action causing death was determined (‘immediate/seconds’, ‘minutes’, ‘hours’, ‘days’, ‘weeks’).
[Note, a lag time was deducted where there were no negative welfare impacts immediately, e.g.
between setting a mole trap and trapping a mole.] Then the level of suffering (‘no suffering’,
‘mild suffering’, ‘moderate suffering’, ‘severe suffering’ or ‘extreme suffering’) was identified
from the impact scale for Part B (S7 Table). Where a single impact category could not be
assigned with confidence, a range of categories was allocated, e.g. mild to moderate suffering.
Then the scoring matrix for Part B (S8 Table) was consulted, using the level of suffering and
the time to insensibility, to identify the impact of the killing method (ranging between A [no
impact] and H [maximum impact]). The evidence used to determine the level and duration of
suffering was recorded as referenced notes. For lethal interventions, the scores for Parts A and
B of the assessment were combined to give the overall assessment, ranging 1A-8H. Scores for
non-lethal interventions ranged 1–8. Ultimately the welfare impact scores were compared for
different management interventions applied to the same species.
When welfare assessments are made using the model for widespread use, this should be done
by a panel of experts [42]. However, our purpose here was to demonstrate both the use of the
model, and its associated benefits, and to identify issues raised by its application, and the assessments were made by SB with guidance from TS and DM. We assessed the management interventions listed in Table 1, assuming they were conducted according to best practice as specified
in the relevant SOPs. Full details of the method for applying the model are available elsewhere
[42] and are summarised here. Assessments were recorded in a standard format (e.g. S9 Table).
Before beginning an assessment, any assumptions were made explicit, including that best practice was followed, according to a particular SOP. Where relevant, the timing of the management
intervention was recorded, e.g. which season, or time of day, and, for those non-lethal interventions without a specific end-point, the duration of the intervention conducted (for scaring crows
and fencing rabbits this was assumed to be two months). Other key details, such as trap-checking frequencies, were also recorded. Comments (relating, for example, to impacts on dependent
offspring or other non-target animals, or what the effect might be if the operator deviated from
the SOP in a particular way etc) were noted at the end of an assessment. Each assessment related
to the welfare impact of a management intervention on a single target animal. Assessments were
based on objective evidence from the literature and where necessary this was extrapolated from
other species, including humans. If no objective data were available for a particular part of an
assessment, we chose a welfare impact category based on informed judgement. Where there was
doubt or a lack of objective knowledge about whether an animal would suffer severely, the animal was given the benefit of the doubt. Assessments considered the likely welfare impact in the
majority of situations [42]. Where Sharp and Saunders had already made assessments of related
methods, as used in Australia, e.g. shooting rabbits and birds, and trapping birds [74–76], we
used these where appropriate as a basis for our assessments, adding or omitting literature to
ensure assessments were made according to the British SOPs.
Results
Comparing welfare impact scores
Results of the welfare assessments are summarised here (and full details are given in S9–S19
Tables). Widely varying impact scores were attributed to the different interventions used for
each species. Scores on the two axes (numbers 1–8 and letters A-H) are not intended for comparison with each other [42], but nevertheless useful comparisons could usually be made, even
between lethal and non-lethal interventions. Applying the model also demonstrated the value
of making formalised welfare assessments for identifying components of interventions that
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
7 / 24
Assessing Animal Welfare Impacts in Wildlife Management
pose a relatively greater welfare threat, or which are currently under-researched and poorly
understood. These aspects are highlighted for each species below.
Rabbits
Rabbit management interventions were clearly ranked by the model (Fig 1). Shooting rabbits
with a head shot scored a lower level of suffering (score A, Fig 1 R1; see S9 Table) for the killing
method, under Part B of the model, than using a chest shot (score B, Fig 1 R2; see S10 Table).
This difference originated from chest shots scoring ‘mild’ suffering over seconds (‘immediate/
seconds’), and head shots no suffering (‘none’) [77] with death occurring immediately (also
‘immediate/seconds’) [78]. Chest shots were considered to produce only mild suffering in rabbits because of the relative scale of the damage likely to be inflicted, by a chest shot, to an animal the small size of a rabbit. Rabbits, shot elsewhere than in the head or chest, are likely to
suffer more. The non-lethal welfare impact occurring before the rabbit was actually shot
(under Part A of the model), of either a head or chest shot, was graded as ‘2–3’. This reflected
the likelihood that multiple rabbits from the same social group [79], cited in [80], would be
shot in a single shooting exercise and that most of these would therefore have experienced
members of their social group being shot (‘mild’ impact)–together with the associated fear/
panic from the noise and general disturbance—over a period of up to minutes (‘immediate/seconds’ to ‘minutes’), before they themselves were shot. Our assessments indicate that rabbit welfare could be significantly improved by targeting the head rather than the chest or any other
body part. It is reassuring that the model aligns with this common-sense finding.
Because head shots scored no impact (score A) for the killing method (under Part B of the
model), we were able to compare the other (non-lethal) impacts of head shots directly with
those of wire-mesh fencing (under Part A of the model). Fence installation (in autumn, for the
protection of imminently planted winter wheat) scored a greater impact (score 5, Fig 1 R3(i); see
S11 Table) than shooting (score 2–3). This difference arose because, while both interventions
were attributed a ‘mild’ impact, this was likely to last ‘days’ following fence installation (which
would disturb nearby rabbit populations and interfere with rabbits’ usual access to foraging
areas on other sides of the field) [81] and between no time (‘immediate/seconds’) and ‘minutes’
for a head shot (because a rabbit would suffer distress and behavioural restrictions when other
rabbits are shot before it is). However, once a rabbit fence is properly installed (and rabbit ranging behaviour has adapted to the presence of the fence), it should, if well maintained, last for
about 10 years [82], and without further welfare impact (score 1, Fig 1 R3(ii); see S12 Table).
Moles
Of the three mole management options assessed, managing molehills and tunnels (Fig 2 M3)
scored lowest with ‘no impact’ (score 1; see S13 Table). Spring trapping scored 1E (Fig 2 M1;
see S14 Table), with no welfare impact (under Part A) before the trap was triggered, but the
killing method scored ‘severe’ suffering, most likely as a result of acute haemorrhaging [83],
potentially for ‘minutes’ (under Part B). Because mole traps are exempt from welfare approval,
no data are available on how long it takes for spring trapped moles to reach irreversible unconsciousness and this is likely to remain the case unless the exemption is revoked. For the purposes of this assessment the SOP assumed time to irreversible unconsciousness (TIU)
for 80% of moles trapped was 5 minutes, which is the requirement for non-exempt spring
traps in England and Wales [84]. The suffering caused by spring trapping moles could be
reduced if TIU was decreased [85].
Live trapping and translocation (Fig 2 M2(i) and M2(ii); see S15 and S16 Tables), which
need to be considered cumulatively in a translocation exercise, scored non-lethal welfare
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
8 / 24
Assessing Animal Welfare Impacts in Wildlife Management
Fig 1. Welfare assessment grid for rabbit management interventions.
doi:10.1371/journal.pone.0146298.g001
impacts of 5–6 and 6–8 respectively. A range of potential impacts was attributed to both
because there are very few data regarding their impact on moles. The live trapping component
represented a ‘moderate’ to ‘severe’ impact for ‘hours’, largely because moles survive poorly in
live traps (e.g. [83]) and the particular type of traps available and assessed here (tube traps) do
not accommodate the provision of bedding [29]. The translocation component scored a ‘moderate’ to ‘extreme’ impact over several ‘days’, because of the risks involved in either encountering existing territory holders [86, 87] or dispersing above ground [88, 89], and the difficulties
associated with setting up an independent territory of feeding tunnels [87]. The impacts of live
trapping moles might be reduced by checking traps more frequently, or using different traps
that allow the use of bedding [29], but the potential of both live trapping and translocation for
managing moles needs more research to determine whether it can be done successfully and
with acceptably low welfare impact levels [29]. These assessments highlight two issues with
applying the model: first, how to compare total impact scores between some lethal and nonlethal interventions (as seen for spring trapping and for live-trapping followed by translocation,
where only non-lethal scores can be compared, under Part A); and second, how to assess two
methods used in sequence as part of a single management intervention (whether two nonlethal methods or a non-lethal followed by a lethal method).
Crows
The relative welfare impacts of the three crow management interventions were clearly ranked
by the model. Shooting scored the least impact (score 3A, Fig 3 C1; see S17 Table), with a ‘mild’
non-lethal welfare impact occurring, potentially for ‘minutes’, before the target crow itself was
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
9 / 24
Assessing Animal Welfare Impacts in Wildlife Management
Fig 2. Welfare assessment grid for mole management interventions.
doi:10.1371/journal.pone.0146298.g002
shot (Part A). Crows are often shot at in a group, and any particular individual is likely to be
distressed by the shooting of nearby conspecifics before it is shot [90]. The actual shooting of
the target crow scored ‘no impact’ (Part B) [91]. Non-lethal scaring using a propane gas gun
had a greater impact (score 5, Fig 3 C3; S18 Table), involving a ‘mild’ non-lethal welfare
impact, potentially lasting ‘days’, as a result of crows being disturbed by repeated noise from
intermittent gunfire close to feeding or roosting areas [92]. Cage trapping with cervical dislocation had the greatest impact (score 5C, Fig 3 C2; see S19 Table), with trapping causing a ‘moderate’ non-lethal welfare impact over ‘hours’ (while the bird was in the trap) and the cervical
dislocation causing ‘moderate’ but short-lived (‘immediate/seconds’) suffering [93]. Trapped
birds can suffer distress, injury or panic during confinement in the trap (see [94] about unrestricted minimum cage size for crows), while birds being euthanized will be distressed by handling and the response of the decoy bird to the handler, and can experience hypoxia following
cervical dislocation [95–97]. The assessment for cage trapping with cervical dislocation reveals
that the impact of this intervention might be considerably reduced if traps were checked more
frequently. However, reducing trap-checking frequency from once every 24, even to once every
2 hours, would not be detected by the model in its current form.
Discussion
The Sharp and Saunders model, created in collaboration with experts in animal welfare, wildlife management and veterinary science [42], marks a turning-point in the assessment of welfare impacts in vertebrate wildlife management. The model provides a transparent, evidencebased method for ranking the relative welfare impacts of different management interventions
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
10 / 24
Assessing Animal Welfare Impacts in Wildlife Management
Fig 3. Welfare assessment grid for crow management interventions.
doi:10.1371/journal.pone.0146298.g003
involving lethal and/or non-lethal methods, and in doing so provides helpful information for
decision-makers. It is designed for assessing impacts on individual target animals but assessments can also be made for each type of non-target animal likely to be affected. The scores
attributed under Parts A (non-lethal welfare impact) and B (impact of killing method) are not
intended to be comparable with each other but in our study the model allowed the ranking of
most interventions, by their impacts, even including lethal / non-lethal comparisons (see also
Sharp et al.’s assessments of lethal and non-lethal camel removal procedures [98]). The model
distinguishes physical and affective (emotional) impacts, enabling better consideration of negative affective impacts [61] and it can be modified to address the assessment of a particular class
of interventions, e.g. toxic agents [26], or spring traps. Importantly, the model allows identification of gaps in existing knowledge about welfare impacts (and the incorporation of new
knowledge as this arises [61]), thus revealing where further research would be best directed.
The model also highlights ways of improving SOPs to reduce welfare impacts, and provides a
tool for informing debate on the acceptability of management interventions and for setting limits on acceptable and unacceptable levels of welfare impact [99].
Assessments
Our assessments of management interventions used with rabbits, moles and crows indicated
that applying the model produces helpful information for deciding which interventions to use,
where interventions might be improved and where further research would best be directed. It
must be borne in mind however that the assessments presented here are for interventions conducted according to a best practice SOP, and the relative welfare impacts of different interventions could be different if SOPs are not followed.
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
11 / 24
Assessing Animal Welfare Impacts in Wildlife Management
Rabbits. Our assessments for rabbits suggest that, while the installation of fencing in
autumn may have a mild impact for a few days, established fencing has the least welfare impact
(none), followed by head shots and then chest shots. However, in some situations, e.g. involving transitory rabbit damage, fencing may not be appropriate and shooting may be the best
practical option. Shooters should target the rabbit’s head, because not only is the impact of a
chest shot greater than that of a head shot, but it is also more variable [100], even when a chest
shot is conducted well. It may be that shooters are unaware of this. Of course, the impact scores
attributed to head and chest shots depend on how strictly the SOP is followed, e.g. in terms of
weapon, ammunition and distance; rabbits shot not in accordance with the SOP are likely to
suffer more, e.g. see Hampton et al [101], who found that the greater the shooting distance, the
more likely a rabbit was to be wounded or missed. This raises questions about what proportion
of the many thousands of rabbits shot in Britain each year are shot cleanly in the head, in the
chest and elsewhere, and using the appropriate weapon, ammunition and range needed to
achieve the welfare impact scores derived here.
Moles. Our assessments for moles indicate that managing molehills and tunnels according
to the SOP is likely to have little or no welfare impact, while the two removal interventions,
spring trapping, and live trapping followed by translocation, have large impacts on different
axes. While impacts for these two interventions can be compared under Part A (spring trapping scored 1, whereas live trapping and translocation scored 5–6 and 6–8 respectively), they
cannot be compared under Part B because non-lethal interventions are not be scored on this
axis. We assumed that spring traps met the approval standard generally required under the UK
Pests Act 1954 [18], that at least 80% of 12 animals should reach irreversible unconsciousness
within 5 minutes [84, 85]. However mole traps are exempt from approval under the Small
Ground Vermin Traps Order 1958 [102]. Probably because of this, there is wide variation in
the mechanical performance of mole traps available in Britain, and therefore in their potential
welfare impacts [85], and at least some might fail to meet approval standards if they were
tested. Better information, on TIU for mole spring traps, is required before the impact of mole
trapping can be properly assessed. Withdrawal of their exemption from regulation would help
to ensure that mole spring traps at least meet the minimum standards assessed here. A recent
report by the Food and Environment Research Agency recommended that spring traps for all
species should be required to meet specified minimum welfare standards, and suggested that
two additional, stricter welfare tiers should be introduced, giving three thresholds for TIU of 5
minutes, 3 minutes and 30 seconds [103]. Clearly, differences in TIU in the order of seconds,
and very few minutes, are considered significant in welfare terms. However, because the model
uses categorical time units (immediate/seconds, minutes, hours, days, weeks [42]), it may not
always be sensitive to relatively large differences in the duration of suffering (and hence the
welfare impact) under Parts A or B. For example, it would not distinguish traps taking 3, 5 or
even 50 minutes to cause TIU, but where two interventions are attributed the same welfare
impact score, their relative rankings might sometimes be determined simply by looking at the
details underlying the assessments. Alternatively, the time categories of the model could be
modified to usefully distinguish the impacts of, for example, different types of mole trap.
For mole live trapping we assessed the plastic tube trap, seemingly the only mole live trap
available ‘off-the-shelf’ in Britain. While any live trap will prevent a trapped animal having normal interactions with conspecifics, the design of tube traps is particularly likely to compromise
welfare. Being narrow, they restrict the movement of a trapped mole and do not allow the provision of bedding, or addition of a nest box, and the one-way swing doors potentially allow
more than one animal to become trapped, which could lead to fighting [29]. Moles are poorly
disposed to live trapping although it is not clear whether this is due to starvation, hypothermia
or shock [87, 104]. And, because moles have a high metabolic rate, Natural England
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
12 / 24
Assessing Animal Welfare Impacts in Wildlife Management
recommends that tube traps are checked more frequently than the usually recommended once
every 24 hours [87]. Mellanby reported that moles may survive for 24 hours without food, but
recommended that live traps are checked at least every 8 hours to prevent trapped moles from
dying from hypothermia, starvation and from throwing themselves at the trap walls (although
the latter would not be possible in the close-fitting tube trap) [104]. Of the eight moles trapped
by Shaw et al, in Friesian and Talpa live traps (both types provisioned with food, and with nest
boxes filled with hay), the two caught overnight (14 hours in the trap) were found dead in the
morning, while the six caught during the day (10 hours in the trap) survived (Ros Shaw, University of Exeter, personal communication). Currently there is no legal requirement to check
live traps (other than Larsen traps and snares which must be checked at least every 24 hours
[94, 105]). Our assessment here related to mole tube traps being checked every 4 hours and it
seems little can be done to improve their welfare impact, except checking them even more frequently (although the model would not distinguish between checking traps every 4 or every 2
hours). However, larger, bespoke wooden Friesian traps with a nest box attached, and allowing
single captures only, might have a lower impact [88, 104]. Better information is needed on how
to maximise mole welfare and survival in live traps, and better traps (or trapping procedures)
could be designed for the mass market as a result.
Natural England warns that releasing a mole into an already occupied territory can lead to
fighting, while releasing it into an area without an existing run (feeding tunnel) system may be
an offence under The Animal Welfare Act 2006 [49, 87]. Natural England therefore recommends that live trapped moles are despatched humanely [49]. Better information is needed on
how to identify whether an adequate, unoccupied run system exists at potential release sites,
whether and in which conditions moles are capable of quickly establishing an adequate run system where necessary. Even if a mole could be live trapped well, there are currently insurmountable issues regarding mole translocation and it may not be possible to reduce welfare impacts
adequately to justify this type of intervention with moles.
A more general point highlighted by the assessment for live trapping followed by translocation is that it is difficult to interpret together the sequential impacts of the two separate stages
of an intervention (as we have attempted here). However, the advantage of assessing each component of an intervention separately, according to the model (as we have done), is that comparisons can be made between different secondary techniques following the same primary
technique, thereby helping with decisions on what the best secondary technique might be. In
the case of two or more non-lethal methods, used sequentially, an alternative approach would
be to assess the component parts separately and then to score the combined process the same
as the highest scoring component part (as done in the Australian assessments of camel removal
and killing at an abattoir, a process consisting of several non-lethal stages before the killing
method is applied [98]). While the overall score identified in this way may not be particularly
informative by itself, the associated welfare assessment worksheets and matrix can be consulted
to identify which of the component methods has the greatest welfare impact. In the case of
mole live-trapping followed by translocation the overall score would be 6–8 (the score attributed to the translocation component on its own, which exceeded that for live-trapping).
Crows. Our assessments for crows suggest that shooting has least impact, followed by scaring, and then cage trapping with cervical dislocation. The impact of cage trapping could be
reduced by increasing the frequency of trap-checking, but even if traps were checked every 2
hours, instead of every 24, the model would still rank it worst of the three interventions. In
addition, Larsen trapping requires the use of a live decoy bird to lure target birds into the trap,
and inevitably involves impacts on the decoy, whenever the trap is set, even when no target
bird is caught. The model does not assess impacts on non-target animals, whether these are
conspecifics (including decoys, dependent offspring, or would-be target animals that are
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
13 / 24
Assessing Animal Welfare Impacts in Wildlife Management
impacted but not successfully targeted), or members of non-target species (such as predators,
by-catch etc). However, a separate assessment can be made for each non-target animal likely to
be affected [42].
Territorial animals (such as crows) removed from an area, e.g. by shooting, or cage trapping
with cervical dislocation, are likely to be replaced by incoming conspecifics [106], which might
then also be removed. However, crows that were previously scared away might return to the
site, and be scared again, or be replaced by new individuals that would in turn be scared away.
Crows can only be shot or cage trapped under Natural England General Licence WML-GL04
and only “where the authorised person is satisfied that appropriate legal methods of resolving
the problem, such as scaring and proofing, are either ineffective or impracticable” [107]. If
birds have been subjected to scaring, before being shot or cage trapped, any welfare impacts
might be compounded, potentially over an extended time-scale. This brings us back to the
issue of sequential impacts in general and where the line should be drawn regarding what is
considered a single impact, and what is considered two, to be scored separately? This is especially relevant for ongoing or repeated non-lethal interventions, e.g. scaring / hazing or mustering. Here we treated a 2-month period of crow scaring as a single intervention (and for rabbits,
assessed the impact of fencing over 2 months), and while the model may be used in this way to
assess the impact of individual bouts of an intervention, this would not take account of potential cumulative effects.
The model
We have drawn attention to some issues raised by the model and we explore here the challenges in trying to address them.
Comparability of assessments. An ideal welfare assessment model would allow direct
comparison of the total impact of any management interventions, whether lethal or non-lethal.
However, for example, while we were able to compare the non-lethal impacts of spring trapping moles with those of live-trapping followed by translocation, we were not able to rank the
two interventions on the basis of their total impacts (including lethal impact of spring trapping) because scales on the two axes are not (and are not intended to be) comparable. The
scores for lethal and non-lethal impacts are expressed separately (and represented on separate
axes), under the Sharp and Saunders model, because it uses two different systems to assess
lethal and non-lethal impacts. A model using a single system to assess both lethal and nonlethal impacts (the results of which could be shown on a single axis), would be ideal, but difficulties in designing such a model include producing a single set of impact scales relating to
both lethal and non-lethal impacts, and combining these scores in the case of lethal interventions. In reality such a model might be impossible to achieve but the Sharp and Saunders
model goes part way towards this.
The total welfare impacts of interventions scoring on two different scales would be comparable if the scores on the two axes of the model (1–8 and A-H) were comparable, e.g. 3 = C, and
interval in nature, such that each impact increment on either axis was of equal value (e.g.
1xF = 2xC). However there is a difficulty with this because it is not possible to create with confidence impact scores that are either interval, or comparable between axes. The scores on both
axes of the model (1–8 for Part A and A-H for Part B) are the product of impact (or severity)
categories on an ordinal scale (no impact, mild, moderate, severe, extreme), and time categories
on an irregular, semi-logarithmic scale (seconds, minutes, hours, days, weeks). (See scoring
matrices in S6 and S8 Tables). And so, while the impact categories are ordinal (no
impact < mild < moderate < severe < extreme), the difference between pairs of adjacent categories do not necessarily correspond to an equivalent change in welfare status [61], e.g. the
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
14 / 24
Assessing Animal Welfare Impacts in Wildlife Management
increase in severity between moderate and severe, may not be the same as that between severe
and extreme. The same is true for the time categories, in the scoring matrices, which increase
by irregular quantities (60 seconds per minute, 60 minutes per hour, 24 hours per day, 7 days
per week). It is most likely not possible to create interval scales of welfare impact severity and
duration, unless suffering is known to increase consistently and the pattern of increase does
not depend on the type of suffering involved [53].
Once this limitation of the model is understood however its real benefits can be appreciated.
The model is intended to provide an overall view of relative welfare impacts of a range of different management interventions. The numerical and alphabetical scores are discrete ordinal
scores, which when placed on a grid can facilitate the visual comparison of welfare impact
across a range of management methods [61].
Breadth of impact scores. Each of the impact scores produced using the model can be
arrived at in a number of different ways. For example, a score of ‘E’ under Part B of the model
could represent anything from an extreme impact lasting seconds, right through to a mild
impact lasting days. However, because of the irregular nature of the impact and time scales
underlying these scores, not all interventions attributed the same score can necessarily be considered equivalent. Also, because of the breadth of each of the time categories, the model may
not always be sufficiently sensitive to detect potentially important differences in impact scores,
such as those dependent on, for example, trap-checking times or TIU. Beausoleil and Mellor
[61] make the related point that the model outputs may suggest a precision that is not currently
possible. However, the model was developed to assess and compare the wide range of methods
currently used in Australia and as a result the scales are quite coarse in order to accommodate
methods taking seconds and those taking weeks; the model also worked well in our study. In
cases where a group of similar methods need to be assessed (e.g. different mole traps, as mentioned above, or different types of poisons) the duration timescales could be adapted to make
the intervals finer.
Over and underestimation of impacts. A model is necessarily imperfect, and the Sharp
and Saunders model might, in some cases, overestimate or underestimate the welfare impact of
an intervention. This could happen in several ways: 1) if there is doubt about the impact on an
animal, the rules of the model require that the animal is given the benefit of the doubt (potentially overestimating the impact); 2) the model is supposed to assign the greatest welfare impact
scores occurring at any point in the management process, but also to assume that the duration
of impact or suffering is the total duration of impact or suffering regardless of how much of
this was at the maximal level (also potentially overestimating); 3) application of the model is
based on a SOP for, and on various assumptions about, the intervention, stated at the outset
(potentially overestimating or underestimating welfare impacts if the SOP is not followed); and
4) the model assesses what happens to the majority of animals, e.g. 51–100% of the animals
affected (in extreme examples it might be possible for 51% of animals to suffer enormously,
and 49% only a little, or vice-versa, potentially leading to large over or underestimation of the
impact). Where the welfare impact of an intervention is overestimated, this might be considered to protect the welfare of an animal [42]. However, because the model is used for measuring relative welfare impacts of different interventions, overestimating the impact of one
intervention might potentially improve the relative ranking of another, which actually has a
greater welfare impact. If this worse (but higher ranking) intervention was selected for use as a
result, this might result in a greater level of animal suffering as a result of the intervention. Of
course, it may not be possible to detect an over or underestimation, but attention should be
drawn to either, where it is suspected to have occurred, so that anyone interpreting impact
scores can examine the details of the assessment.
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
15 / 24
Assessing Animal Welfare Impacts in Wildlife Management
Lack of scientific data. Our assessments illustrate that there are often large gaps in scientific understanding of the animal welfare impacts of management interventions. Often there
may be no information about what happens to the majority of animals and when objective data
are lacking, assessments—rather than being evidence-based—will be based on guidance from a
range of experts. A benefit of the model is that it can help to identify precisely where future
research should be targeted.
Wider perspectives
It is increasingly important that humaneness is considered when deciding how (and even
whether) human-wildlife conflict should be tackled [2, 43]. Managers need to think and rethink
about management more often, as pest situations differ or change, management options evolve
and improve, and knowledge about impacts increases. However, managers may have preconceptions about lethal and non-lethal interventions, or may turn automatically to familiar,
favoured methods without much thought. Even if managers do try to take the humaneness of
interventions into account, their opinions on the impacts of different methods on animal welfare may vary widely [4, 50]. Also, the real welfare impact of a method can sometimes be
counter-intuitive to our perceptions of impact; our assessments revealed that the relative welfare impacts of different interventions are not always easy to predict, thus confirming the need
for objective formal assessments. For example, live-trapping and translocating moles may be
associated with a very high welfare impact, although to many, this intervention may intuitively
seem ‘the kindest option’ for managing moles. Shooting crows is likely to cause very little welfare impact prior to death, whereas scaring crows with gas guns may result in a short period of
food restriction, noise and fear/distress before they leave the area. And while shooting rabbits
with a head shot is unlikely to have much impact on their welfare before death, installing rabbit
fencing may result in a short period of food and behavioural restrictions and fear/distress for
rabbits (although—once established—fencing may have no further welfare impact). Littin et al.
propose that wildlife managers should use the most humane methods that achieve the aims in
any given situation, which means that any decision regarding choice of method needs to incorporate other considerations, e.g. ethics and conservation (as in the latter examples), as well as
whether the method is effective and easy to use, affordable, safe for human users and other people, specific to the target species or individuals, and safe for the environment [27]. While it
might seem desirable to develop a holistic model that could help to achieve the right balance of
all these factors, this would be complex and would require judgements to be made about the
relative importance of potentially competing priorities. As it stands the model is a useful tool
for simplifying and clarifying the details of welfare impacts, so that these can be taken into
account consistently in any decisions about wildlife management.
Assessing welfare impacts in wildlife management is much more difficult than doing the
same in livestock farming or laboratory animal experimentation, where managers have more
(in some cases, complete) control over the details and duration of any intervention they make,
and with greater knowledge of how many, and which, individuals are affected. In wildlife management, impacts can be influenced by a host of environmental factors, including the weather,
and which and how many target and non-target animals happen to enter the fray. The total
animal welfare impact of a particular wildlife management operation will depend on the severity of impact on an individual and the number of individuals involved (for both target and
non-target animals) [31, 65, 108]; this may be seen as an ethical or philosophical issue that can
be considered after the severity of impact on an individual animal is known (e.g. see [21]).
Also, there are wider issues about the balance between the number of animals and the level
of suffering involved, and uncertainties about how a target population responds to an
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
16 / 24
Assessing Animal Welfare Impacts in Wildlife Management
intervention. The balance of numbers and suffering is especially relevant for most non-lethal
interventions, which often maintain an unknown number of the same individuals in their habitat, subjecting them to repeated or even continuous welfare impacts which are difficult to compare with those resulting from a removal intervention (culling or translocation), conducted in
a different pattern, potentially on a known number of animals, each affected once. In our case
of a cohort of rabbits suffering the mild impacts of a new fence for a few days, compared to ten
cohorts (each potentially consisting of multiple litters [109]) of rabbits managed by shooting
(as well as individuals born to fill vacancies created, within a cohort, by density-dependent
responses [110]), it is relatively easy to judge that over a 10 year period the total welfare impact
of a fencing operation (including installation) will be less than that of an annual shooting operation. In other comparisons it might be far less obvious which option involves less total suffering. Also there may be uncertainties about how a target population will respond to an
intervention, for example, where an animal is removed (by killing or translocation) it may be
replaced by another, and in time others [106], which may then be subject to the same or a different intervention. Conversely, an animal exposed to certain types of non-lethal control may
be subjected repeatedly to the same or different interventions. It may be useful therefore to
think in terms of both the ‘lifetime welfare impact’ of multiple interventions on a particular
individual, and perhaps the ‘community welfare impact’ of an intervention on all animals
affected by it. Despite the difficulties involved, it is important that welfare scientists continue to
develop tools for assessing the humaneness of wildlife management interventions and for
reducing these impacts where possible.
There are some parallels between Sharp and Saunders’ welfare assessment model and the
quality-adjusted life years (QALYs) system used to provide a common currency for measuring
the extent of health benefits resulting from human healthcare interventions and for making
choices based on this. The QALYs system incorporates the quality and quantity of life that a
patient can expect following a particular medical treatment (represented as a positive score)
[111]. Similarly, but in reverse, Sharp and Saunders’ model provides a common currency for
measuring the extent of welfare impacts resulting from wildlife management interventions.
Broadly speaking, the model incorporates the welfare impact and duration of suffering associated with an intervention (represented as a negative score). As well as informing decision making about the humaneness of different interventions, the model can be used for identifying
ways of reducing the welfare impact of an intervention and for directing future research as discussed above. The model could also be used to improve the way that interventions are practised, e.g., by comparing the welfare impacts of an intervention conducted according to a SOP
(based, for example, on an organisation’s Code of Practice or Best Practice Guidelines) and the
impacts of the same intervention conducted as it is in practice (perhaps by that same organisation’s members). This could help to identify where pressure might most efficiently be applied
to improve wildlife management practise, in order to benefit animal welfare.
For the purposes of this study welfare assessments were performed to demonstrate the application of the model and various related issues. Our plan for taking this work forward is to lead
assessments using a panel of experts in an effort to reach consensus (a Delphi approach) on the
relative welfare impacts of a much wider range of management interventions on a larger number
of species. The participation of, and agreement among, diverse stakeholders should reduce any
effects of subjective judgement and increase acceptance of the resulting impact scores.
Supporting Information
S1 SOP. Standard Operating Procedure for shooting rabbits.
(PDF)
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
17 / 24
Assessing Animal Welfare Impacts in Wildlife Management
S2 SOP. Standard Operating Procedure for fencing rabbits from crops.
(PDF)
S3 SOP. Standard Operating Procedure for spring trapping moles.
(PDF)
S4 SOP. Standard Operating Procedure for live trapping and translocation of moles.
(PDF)
S5 SOP. Standard Operating Procedure for managing molehills and tunnels on lawns.
(PDF)
S6 SOP. Standard Operating Procedure for shooting crows.
(PDF)
S7 SOP. Standard Operating Procedure for cage trapping and cervical dislocation of crows.
(PDF)
S8 SOP. Standard Operating Procedure for scaring crows using gas guns.
(PDF)
S1 Table. Impact scale for part A of the model (assessment of non-lethal welfare impact)
Domain 1: Water deprivation, food deprivation, malnutrition. From Sharp and Saunders
(2011).
(PDF)
S2 Table. Impact scale for part A of the model (assessment of non-lethal welfare impact)
Domain 2: Environmental challenge. From Sharp and Saunders (2011).
(PDF)
S3 Table. Impact scale for part A of the model (assessment of non-lethal welfare impact)
Domain 3: Injury, disease, functional impairment. From Sharp and Saunders (2011).
(PDF)
S4 Table. Impact scale for part A of the model (assessment of non-lethal welfare impact)
Domain 4: Behavioural, interactive restriction. From Sharp and Saunders (2011).
(PDF)
S5 Table. Impact scale for part A of the model (assessment of non-lethal welfare impact)
Domain 5: Anxiety, fear, pain, distress, thirst, hunger etc. From Sharp and Saunders (2011).
(PDF)
S6 Table. Scoring matrix for part A of the model: assessment of non-lethal welfare impact.
From Sharp and Saunders (2011).
(PDF)
S7 Table. Impact scale for part B of the model (assessment of killing method). From Sharp
and Saunders (2011).
(PDF)
S8 Table. Scoring matrix for part B of the model: assessment of mode of death. From Sharp
and Saunders (2011).
(PDF)
S9 Table. Welfare assessment for shooting rabbits (head shot).
(PDF)
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
18 / 24
Assessing Animal Welfare Impacts in Wildlife Management
S10 Table. Welfare assessment for shooting rabbits (chest shot).
(PDF)
S11 Table. Welfare assessment for fencing against rabbits (fence installation).
(PDF)
S12 Table. Welfare assessment for fencing against rabbits (fence established).
(PDF)
S13 Table. Welfare assessment for managing molehills on lawns.
(PDF)
S14 Table. Welfare assessment for spring trapping moles.
(PDF)
S15 Table. Welfare assessment for live-trapping moles.
(PDF)
S16 Table. Welfare assessment for translocating moles.
(PDF)
S17 Table. Welfare assessment of shooting crows.
(PDF)
S18 Table. Welfare assessment for scaring crows.
(PDF)
S19 Table. Welfare assessment for cage-trapping and cervical dislocation of crows.
(PDF)
Acknowledgments
Mark Jones (Humane Society International/UK), Dr Andrew Rowan (Humane Society International/US) and Dr Paul Johnson (WildCRU/UK) contributed useful ideas and made helpful
comments on an earlier draft of this paper.
Author Contributions
Conceived and designed the experiments: SB TS DM. Performed the experiments: SB TS. Analyzed the data: SB TS. Contributed reagents/materials/analysis tools: TS. Wrote the paper: SB
TS DM. Created Standard Operating Procedures: SB TS. Conducted literature searches: SB.
References
1.
Inskip C, Zimmermann A. Review of human-felid conflict: a review of patterns and priorities worldwide.
Oryx. 2009; 43(1):18–34.
2.
Baker PJ, Boitani L, Harris S, Saunders G, White PCL. Terrestrial carnivores and human food production: impact and management. Mammal Rev. 2008; 38(2–3):123–66.
3.
Treves A, Naughton-Treves L, Shelley V. Longitudinal Analysis of Attitudes Toward Wolves. Conserv
Biol. 2013; 27:315–23. doi: 10.1111/cobi.12009 PMID: 23293913
4.
Baker SE, Macdonald DW. Foxes and foxhunting on farms in Wiltshire: a case study. The Journal of
Rural Studies. 2000; 16(2):185–201.
5.
Treves A, Kapp KJ, MacFarland DM. American black bear nuisance complaints and hunter take.
Ursus. 2010; 21(1):30–42.
6.
Wanless RM, Ratcliffe N, Angel A, Bowie BC, Cita K, Hilton GM, et al. Predation of Atlantic Petrel
chicks by house mice on Gough Island. Anim Conserv. 2012; 15(5):472–9.
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
19 / 24
Assessing Animal Welfare Impacts in Wildlife Management
7.
Harrison A, Newey S, Gilbert L, Haydon DT, Thirgood S. Culling wildlife hosts to control disease:
mountain hares, red grouse and louping ill virus. J Appl Ecol. 2010; 47:926–30.
8.
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; 6(12):e28904. doi: 10.1371/journal.pone.0028904 PMID: 22194946
9.
Quammen D. Monster of God: The Man-Eating Predator in the Jungles of History and the Mind: Norton; 2004.
10.
Conover M. Resolving human-wildlife conflicts: The science of wildlife damage management. Florida,
USA: CRC Press; 2001.
11.
Klenke RA, Ring I, Kranz A, Jepsen N, Rauschmayer F, Henle K. Human-wildlife conflicts in Europe:
fisheries and fish-eating vertebrates as a model case Heidelberg, New York, Dordrecht, London:
Springer-Verlag; 2013.
12.
Natural England. A guide to cage-trapping birds in premises to preserve public health or public safety.
Technical Information Note TIN0712009. Available from: http://publications.naturalengland.org.uk/
publication/33010?category=28001.
13.
Van Niekerk H. The Cost of Predation on Small Livestock in South Africa by Medium Sized Predators
[MSc]: Free State University, Bloemfontien, South Africa; 2010.
14.
Conner M, Ebinger M, Knowlton F. Evaluating coyote management strategies using a spatially
explicit, individual-based, socially structured population model. Ecol Model. 2008; 219:234–47.
15.
Mathews F. Wild animal conservation and welfare in agricultural systems. Anim Welf. 2010; 19:159–
70.
16.
White PCL, Ward AI. Interdisciplinary approaches for the management of existing and emerging
human—wildlife conflicts. Wildl Res. 2010; 37(8):623–9.
17.
Kirkwood JK. Wild animal welfare. Anim Welf. 2013; 22:147–8.
18.
UK Government. Pests Act 1954. http://www.legislation.gov.uk/ukpga/Eliz2/2-3/68/contents: 1954.
19.
UK Government. Prevention of Damage by Pests Act 1949. http://www.legislation.gov.uk/ukpga/
Geo6/12-13-14/55/contents: 1949.
20.
UK Government. Agriculture Act 1947. http://www.legislation.gov.uk/ukpga/Geo6/10-11/48/contents:
1947.
21.
Warburton B, Norton BG. Towards a Knowledge-Based Ethic for Lethal Control of Nuisance Wildlife.
J Wildl Manag. 2009; 73(1):158–64.
22.
Kissui B. Livestock predation by lions, leopards, spotted hyenas, and their vulnerability to retaliatory
killing in the Maasai steppe, Tanzania. Anim Conserv. 2008; 11(5):422–32.
23.
Nicholls J. Mole Catching; A Practical Guide. Marlborough, UK: Crowood; 2010.
24.
Crocker J. How to build a better scarecrow. New Sci. 1984; 101(1403):10–2.
25.
Baker SE, Macdonald DW. Non-lethal predator control: exploring the options. In: Cowan PD, Feare
CJ, editors. Advances in Vertebrate Pest Management. Furth, Germany: Filander Verlag; 1999. p.
251–66.
26.
Fisher P, Beausoleil NJ, Warburton B, Mellor DJ, Campion M, Booth L. How humane are our pest control tools? (09–11326) Ministry of Agriculture and Forestry Biosecurity New Zealand Technical Paper
No: 2011/01. Lincoln, New Zealand: Landcare Research, 2010.
27.
Littin KE, Mellor DJ, Warburton B, Eason CT. Animal welfare and ethical issues relevant to the
humane control of vertebrate pests. New Zealand Veterinary Journal. 2004; 52(1):1–10. PMID:
15768076
28.
Humane Vertebrate Pest Control Working Group. A national approach towards humane vertebrate
pest contrl. Discussion paper arising from the proceddingsof an RSPCA Australia/AWC/VPC joint
workshop, August 4–5 2003, Melbourne. Canberra: ACT, 2004 August 4–5 2003. Report No.
29.
Baker SE, Macdonald DW. Not so humane mole tube traps. Anim Welf. 2012; 21(4):613–5.
30.
Broom DM. Quality of life means welfare: how is it related to other concepts and assessed? Anim
Welf. 2007; 16 (Supplement 1):45–53.
31.
Kirkwood JK, Sainsbury AW, Bennett PM. The welfare of free-living wild animals—methods of
assessment. Anim Welf. 1994; 3(4):257–73.
32.
Warburton B, Hall J. Impact momentum and clamping force thresholds for developing standards for
possum kill traps N Z J Zool. 1995; 22(1):39–44.
33.
Zelin S, Jofriet J, Percival K, Abdinoor D. Evaluation of humane traps: momentum thresholds for furbearers. J Wildl Manag. 1983; 47(3):863–8.
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
20 / 24
Assessing Animal Welfare Impacts in Wildlife Management
34.
ISO. TC191. Animal (mammal) traps. Part 4: methods for testing killing trap systems used on land or
underwater. International Standard ISO/DIS 10990–4. Geneva: International Organization for Standardization, 1999.
35.
ISO. TC191. Animal (mammal) traps. Part 5: methods for testing restraining traps. International Standard ISO/DIS 10990–5. Geneva: International Organization for Standardization, 1999.
36.
Harrington LA, Moehrenschlager A, Gelling M, Atkinson R, Hughes J, Macdonald DW. Conflicting and
complementary ethics of animal welfare considerations in reintroductions Conserv Biol. 2013; 27
(3):486–500. doi: 10.1111/cobi.12021 PMID: 23506045
37.
Baker SE, Cain R, van Kesteren F, Zommers ZA, D'Cruze N, Macdonald DW. Rough Trade: Animal
Welfare in the Global Wildlife Trade. Bioscience. 2013; 63(12):928–38.
38.
Bush ER, Baker SE, Macdonald DW. Global trade in exotic pets 2006–2012. Conserv Biol. 2014; 28
(3):663–76. doi: 10.1111/cobi.12240 PMID: 24661260
39.
Moorhouse T, Dahlsjö C, Baker S, D'Cruze N, Macdonald D. The customer isn't always right—conservation and animal welfare implications of the increasing demand for wildlife tourism. PLoS ONE.
2015; 10(10):e0138939. doi: 10.1371/journal.pone.0138939 PMID: 26489092
40.
Fraser D. Toward a synthesis of conservation and animal welfare science. Anim Welf. 2010; 19:121–
4.
41.
Fraser D. Understanding animal welfare; the science in its cultural context. Kirkwood JK, Hubrecht
RC, editors. Oxford, UK: Wiley-Blackwell; 2008.
42.
Sharp T, Saunders G. A model for assessing the relative humaneness of pest animal control methods.
Second edition. Canberra, ACT: Australian Government Department of Agriculture, Fisheries and
Forestry. Available from http://www.daff.gov.au/animal-plant-health/welfare/aaws/humaneness-ofpest-animal-control-methods, 2011.
43.
Meerburg BG, Brom FWA, Kijlstra A. The ethics of rodent control. Pest Manag Sci. 2008; 64
(12):1205–11. doi: 10.1002/ps.1623 PMID: 18642329
44.
UK Government. Wild Mammals (Protection) Act 1996. http://www.legislation.gov.uk/ukpga/1996/3/
contents: 1996.
45.
Scottish Government. Protection of Wild Mammals (Scotland) Act. http://www.legislation.gov.uk/asp/
2002/6/contents. 2002.
46.
UK Government. The Hunting Act 2004. http://www.legislation.gov.uk/ukpga/2004/37/contents: 2004.
47.
UK Government. Animal Welfare Act 2006. http://www.legislation.gov.uk/ukpga/2006/45/contents:
2006.
48.
Scottish Government. Animal Health and Welfare (Scotland) Act. http://www.legislation.gov.uk/asp/
2006/11. 2006.
49.
Natural England. The Animal Welfare Act 2006—what it means for wildlife; Technical Information
Note TIN0722010. Available from: http://publications.naturalengland.org.uk/publication/23021.
50.
Macdonald DW, Johnson PJ. The impact of sport hunting: a case study. In: Taylor VJ, Dunstone N,
editors. The Exploitation of Mammal Populations. London: Chapman and Hall; 1996. p. 160–207.
51.
Dawkins MS. A user's guide to animal welfare science. TRENDS in Ecology and Evolution. 2006; 21
(2):77–82. PMID: 16701478
52.
Mason G, Mendl M. Why is there no simple way of measuring animal welfare?. Anim Welf. 1993 2
(4):301–19.
53.
Mellor DJ, Patterson-Kane E, Stafford KJ. The Sciences of Animal Welfare. Kirkwood JK, Hubrecht
RC, editors. Oxford, UK: Wiley-Blackwell; 2009. 212 p.
54.
Moorhouse TP, Gelling M, McLaren GW, Mian R, Macdonald DW. Physiological consequences of
captive conditions in water voles (Arvicola terrestris). Journal of Zoology. 2007; 271(1):19–26.
55.
Farm Animal Welfare Council. Farm Animal Welfare Council Press Statement. (19 February 2013;
www.fawc.org.uk/pdf/fivefreedoms1979.pdf)1979.
56.
Farm Animal Welfare Council. Five Freedoms. (19 February 2013; www.fawc.org.uk/freedoms.htm)
2009.
57.
Mellor DJ, Reid CSW. Concepts of animal well-being and predicting the impact of procedures on
experimental animals. In: Baker RM, Jenkin G, Mellor DJ, editors. Improving the Well-being of Animals
in the Research Environment; October 1993; Marriott Hotel, Sydney, Australia: Australian and New
Zealand Council for the Care of Animals in Research and Training (ANZCCART): Glen Osmond,
South Australia; 1994. p. 3–18.
58.
Mellor DJ, Williams VM, Marbrook J. Revision of a scale for assessing the severity of live animal
manipulations. Palmerston North, New Zealand: Animal Welfare Science and Bioethics Centre, Operational Research Project FRM236, 2005.
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
21 / 24
Assessing Animal Welfare Impacts in Wildlife Management
59.
Mellor DJ, Stafford KJ. Integrating practical, regulatory and ethical strategies for enhancing farm animal welfare. Aust Vet J. 2001; 79(11):762–8. PMID: 11789912
60.
Beausoleil NJ, Fisher P, Mellor DJ, Warburton B. Ranking the negative impacts of wildlife control
methods may help to advance the Three Rs. Alternatives to Animal Experimentation (ALTEX). 2012;
29 (Special Issue):481–5.
61.
Beausoleil NJ, Mellor DJ. Advantages and limitations of the Five Domains model for assessing welfare impacts associated with vertebrate pest control. New Zealand Veterinary Journal. 2015; 63
(1):37–43. doi: 10.1080/00480169.2014.956832 PMID: 25147947
62.
Zoo and Aquarium Association. Animal Welfare Position Statement. http://www.zooaquarium.org.au/
wp-content/uploads/2014/01/ZAA_AnimalWelfare_PS.pdf: 2014.
63.
Botreau R, Bonde M, Butterworth A, Perny P, Bracke MBM, Capdeville J, et al. Aggregation of measures to produce an overall assessment of animal welfare. Part 1: a review of existing methods. Animal. 2007; 1:1179–87. doi: 10.1017/S1751731107000535 PMID: 22444862
64.
Botreau R, Bracke MBM, Perny P, Butterworth A, Capdeville J, Van Reenen CG, et al. Aggregation of
measures to produce and overall assessment of animal welfare. Part 2. analysis of constraints. Animal. 2007; 1:1188–97. doi: 10.1017/S1751731107000547 PMID: 22444863
65.
Broom DM. The welfare of vertebrate pests in relation to their management. In: Cowan DP, Feare CJ,
editors. Advances in Vertebrate Pest Management. Furth, Germany: Filander Verlag; 1999. p. 309–
29.
66.
Sharp T, Saunders G. A model for assessing the relative humaneness of pest animal control methods.
Canberra, ACT: Australian Government Department of Agriculture, Fisheries and Forestry, 2008.
67.
Atkinson RPD, Macdonald DW, Johnson PJ. The status of the European mole Talpa europea L. as an
agricultural pest and its management. Mammal Rev. 1994; 24(2):73–90.
68.
Martin J. The wild rabbit: plague, polices and pestilence in England and Wales, 1931–1955. Agricultural History Review. 2010; 58(2):255–76.
69.
Packer JJ, Birks JDS. An assessment of British farmers' and gamekeepers' experiences, attitudes
and practices in relation to the European Polecat Mustela putorius. Mammal Rev. 1999; 29(2):75–92.
70.
Henzell RP, Cooke BD, Mutze GJ. The future biological control of pest populations of European rabbits, Oryctolagus cuniculus. Wildl Res. 2008; 35(7):633–50.
71.
Quy R, Poole D. A review of methods used within the European Union to control the European mole,
Talpa europea. 2004.
72.
Teunissen W, Schekkerman H, Willems F, Majoor F. Identifying predators of eggs and chicks of Lapwing Vanellus vanellus and Black-tailed Godwit Limosa limosa in the Netherlands and the importance
of predation on wader reproductive output. Ibis. 2008; 150 (Supplement 1):74–85.
73.
Sharp T, Saunders G. Humane codes: model codes of practice and standard operating
procedures.2012.
74.
Sharp T, Saunders G. BIR002 trapping pest birds; standard operating procedure. 2012. Available
from: http://www.feral.org.au/wp-content/uploads/2012/07/bir-002_SOP2005.pdf.
75.
Sharp T, Saunders G. BIR001 shooting of pest birds; standard operating procedure. 2012. Available
from: http://www.feral.org.au/wp-content/uploads/2012/07/bir-001_SOP2005.pdf.
76.
Sharp T, Saunders G. RAB009 ground shooting of rabbits; standard operating procedure. 2012. Available from: http://www.feral.org.au/wp-content/uploads/2012/07/rab-009_SOP2005.pdf.
77.
American Veterinary Medical Association. 2000 Report of the AVMA Panel on Euthanasia. Journal of
the American Veterinary Medical Association. 2001; 218(5):669–96. PMID: 11280396
78.
Longair J. Guidelines for euthanasia of domestic animals by firearms. Canadian Veterinary Journal.
1991; 32:724–6.
79.
Marsh M. The effects of behaviour in disease transmission: understanding RHDV dynamics in Australian rabbit populations. PhD thesis. York, UK: University of York; 2009.
80.
Sharp T, Saunders G. Ground shooting of rabbits; welfare assessment. 2009. Available from: http://
www.feral.org.au/wp-content/uploads/2012/02/rabbit_ground_shooting.pdf.
81.
McKillop IG, Wilson CJ. The behaviour of free-living European wild rabbits at electric fences. Crop
Prot. 1999; 18:193–7.
82.
Natural England. Rabbits: management options for preventing damage; Technical Information Note
TIN003 2011. Available from: http://www.newcastle-staffs.gov.uk/Documents/Environment/Pest%
20Control/NE%20Rabbits%20tin003.pdf.
83.
Baker SE, Shaw RF, Atkinson RPD, West P, Macdonald DW. Potential welfare impacts of kill-trapping
European moles (Talpa europaea) using scissor traps and Duffus traps: a post-mortem examination
study. Anim Welf. 2015; 24:1–14.
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
22 / 24
Assessing Animal Welfare Impacts in Wildlife Management
84.
Defra. Spring trap and collarum test criteria. London, UK: Department for Environment, Food and
Rural Affairs, 2009.
85.
Baker SE, Ellwood SA, Tagarielli VL, Macdonald DW. Mechanical Performance of Rat, Mouse and
Mole Spring Traps, and Possible Implications for Welfare Performance. PLoS ONE. 2012; 7(6):
e39334. doi: 10.1371/journal.pone.0039334 PMID: 22768073
86.
Atkinson R, Macdonald D. Can repellents function as a nonlethal means of controlling moles (Talpa
europaea). J Appl Ecol. 1994; 31:731–6.
87.
Natural England. Moles: options for management and control. Technical Information Note
TIN0332011. Available from: http://publications.naturalengland.org.uk/publication/34015?category=
41004.
88.
Gorman ML, Stone RD. The Natural History of Moles. London, UK: Christopher Helm; 1990.
89.
Morris P. The mole as a surface dweller. Journal of Zoology. 1966; 149:46–9.
90.
Munck A, Guyre P, Holbrook N. Physiological Functions of Glucocorticoids in Stress and Their Relation to Pharmacological Actions. Endocr Rev. 1984; 5:25–44. PMID: 6368214
91.
Merck MD. Veterinary forensics: animal cruelty investigations. Iowa: Blackwell Publishers; 2007.
92.
Inglis IR. Humane control of rural birds. In: Britt DP, editor. Humane control of land mammals and
birds. Potters Bar, England: UFAW; 1985. p. 83–95.
93.
Gregory NG, Wotton SB. Comparison of neck dislocation and percussion of the head on visual
evoked responses in the chicken's brain. Veterinary Record. 1990; 126:570–2. PMID: 2368304
94.
UK Government. Wildlife and Countryside Act 1981. http://www.legislation.gov.uk/ukpga/1981/69/
contents: 1981.
95.
Cornell HN, Marzluff JM, Pecoraro S. Social learning spreads knowledge about dangerous humans
among crows. Proceedings of the Royal Society B—Biological Sciences. 2012; 279(1728):499–508.
96.
Erasmus MA, Lawlis P, Duncan IJH, Widowski TM. Using time to insensibility and estimated time to
death to evaluate a nonpenetrating captive bolt, cervical dislocation, and blunt trauma for on-farm killing of turkeys. Poult Sci. 2010; 89:1345–54. doi: 10.3382/ps.2009-00445 PMID: 20548061
97.
Marzluff JM, Walls J, Cornell HN, Withey JC, Craig DP. Lasting recognition of threatening people by
wild American crows. Anim Behav. 2010; 79(3):699–707.
98.
Hart Q, Jones B, Hampton J, Gee P. Case study: Ensuring acceptable animal welfare standards
under the Australian Feral Camel Management Project. Department of Land Resource Management,
Northern Territory Government, Australia and Australian Feral Camel Management Project. http://
www.feralcamels.com.au/resource/AnimalWelfareCaseStudy.pdf. Alice Springs: Ninti One; 2013.
99.
Littin K, Fisher P, Beausoleil NJ, Sharp T. Welfare aspects of vertebrate pest control and culling: ranking control techniques for humaneness. Revue Scientifique et Technique (International Office of Epizootics). 2014; 33(1):281–9.
100.
Gregory N. Physiology and behaviour of animal suffering. Oxford, UK: Blackwell; 2004.
101.
Hampton JO, Forsyth DM, Mackenzie DI. A simple quantitative method for assessing animal welfare
outcomes in terrestrial wildlife shooting: the European rabbit as a case study. Anim Welf. 2015; 24
(3):307–17.
102.
UK Government. Small Ground Vermin Traps Order. http://www.legislation.gov.uk/uksi/1958/24/
contents/made: 1958.
103.
Talling JC, Inglis IR. Improvements to trapping standards. http://ec.europa.eu/environment/
biodiversity/animal_welfare/hts/pdf/final_report.pdf: DG ENV, 2009.
104.
Mellanby K. The Mole: Harper Collins; 1971.
105.
Natural England. Licence (General): To kill or take certain wild birds to prevent serious damage or disease, WML-GL042013. Available from: http://www.naturalengland.org.uk/Images/wml-gl04_tcm624149.pdf.
106.
Reynolds JC, Goddard HN, Brockless MH. Reynolds J.C., Goddard H.N. & Brockless M.H. The
impact of local fox (Vulpes vulpes) removal on fox populations at two sites in southern England. Gibier
Faune Sauvage. 1993; 10:319–34.
107.
Natural England. LICENCE (General) WML-GL04 To kill or take certain wild birds to prevent serious
damage or disease2013.
108.
Warburton B, Tompkins D, Choquenot D, Cowan P. Minimising number killed in long-term vertebrate
pest management programmes, and associated economic incentives. Anim Welf. 2012; 21(S1):141–9.
109.
Rodel H, von Holst D, Kraus C. Family legacies: short- and long-term fitness consequences of earlylife conditions in female European rabbits. J Anim Ecol. 2009; 78(4):789–97. doi: 10.1111/j.13652656.2009.01537.x PMID: 19298614
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
23 / 24
Assessing Animal Welfare Impacts in Wildlife Management
110.
Rodel H, Bora A, Kaiser J, Kaetzke P, Khaschei M, von Holst D. Density-dependent reproduction in
the European rabbit: a consequence of individual response and age-dependent reproductive performance. Oikos. 2004; 104(3):529–39.
111.
Phillips C, Thompson G. Phillips, C. and Thompson, G. (2001) What is a QALY? www.evidencebased-medicine.co.uk. 2001.
PLOS ONE | DOI:10.1371/journal.pone.0146298 January 4, 2016
24 / 24