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1 23 European Journal of Wildlife Research ISSN 1612-4642 Volume 61 Number 3 Eur J Wildl Res (2015) 61:445-455 DOI 10.1007/s10344-015-0916-6 Monitoring trap-related injury status during large-scale wildlife management programmes: an adaptive management approach Andrew W. Byrne, James O’Keeffe, Ursula Fogarty, Pat Rooney & S. Wayne Martin

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Page 1: bovine tb · the study period. Eighty-four percent of captured badgers ex-hibited no impact or only superficial hair/skin compression (scale 0–1). Logistic models indicated that

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European Journal of WildlifeResearch ISSN 1612-4642Volume 61Number 3 Eur J Wildl Res (2015) 61:445-455DOI 10.1007/s10344-015-0916-6

Monitoring trap-related injury statusduring large-scale wildlife managementprogrammes: an adaptive managementapproach

Andrew W. Byrne, James O’Keeffe,Ursula Fogarty, Pat Rooney & S. WayneMartin

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ORIGINAL PAPER

Monitoring trap-related injury status during large-scale wildlifemanagement programmes: an adaptive management approach

Andrew W. Byrne1,6 & James O’Keeffe1,2 & Ursula Fogarty3 & Pat Rooney4 &

S. Wayne Martin5

Received: 22 March 2014 /Revised: 18 March 2015 /Accepted: 25 March 2015 /Published online: 8 April 2015# Springer-Verlag Berlin Heidelberg 2015

Abstract Wildlife management and research programmes of-ten rely on the capturing of live animals. All capture methodsfor wildlife involve a risk of injury. For that reason, monitor-ing of injuries should be completed concurrently, and effi-ciently, throughout the intervention programme, or study pe-riod, to uphold welfare standards. Here, we present a practicaladaptive management system to monitor trap-related injuriesas a component of broader attempts to maintain welfare stan-dards. Themonitoring system described is part of a large-scaletuberculosis-control management programme of Europeanbadgers (Meles meles) in the Republic of Ireland. Badgerswere captured in stopped cable restraints. A standardised op-erating procedure was developed to allow for the necropsy oflarge numbers of badgers (N=18,596) by a veterinary pathol-ogist. As part of this programme, badger injury status was

evaluated using a categorical severity scale ranging from 0(no impact due to capture) to 6 (death) for badgers capturedin restraints. No restraint-related deaths were recorded overthe study period. Eighty-four percent of captured badgers ex-hibited no impact or only superficial hair/skin compression(scale 0–1). Logistic models indicated that injury severitywas significantly influenced by year, season, age class, gen-der, weight and the body position where the badger was cap-tured. Despite the low prevalence of severe injuries recorded,the proportion of animals with a minor injury type (skin oe-dema; scale 2) increased during the study period. This high-lights the need for continual sensitive welfare vigilance duringprolonged programmes. We suggest improvements to the cur-rent programme and additional adjustments for future vacci-nation campaigns. We contend that this type of monitoring,coupled with adaptive management strategies, is essential forwildlife programmes to maintain high animal welfare stan-dards, at least in terms of injuries, but also highlight that trapinjuries are only one component of animal welfare. We sug-gest that this adaptive management system could serve as atemplate for other similar wildlife programmes.

Keywords Animal welfare . Badger . Meles meles . Wirerestraint trap . Live trapping

Introduction

Many studies and wildlife management interventions requirethe live capture of animals using traps. All practicable effortsshould be made to monitor and counteract trap-related injuriesor mortalities to the target animals where live trapping is re-quired (Proulx et al. 1993; Frame and Meier 2007; O’Néillet al. 2007; Iossa et al. 2007; Will et al. 2010). This is espe-cially true during large-scale interventions, for example,

Communicated by A. W. Sainsbury

Electronic supplementary material The online version of this article(doi:10.1007/s10344-015-0916-6) contains supplementary material,which is available to authorized users.

* Andrew W. [email protected]; [email protected]

1 Centre for Veterinary Epidemiology and Risk Analysis, UniversityCollege Dublin, Belfield, Dublin 4, Ireland

2 Department of Agriculture, Agriculture House, Dublin 2, Ireland3 Irish Equine Centre, Johnstown, Naas, Co. Kildare, Ireland4 Monaghan Veterinary Office, Department of Agriculture, Food and

the Marine, Monaghan, Ireland5 Department of Population Medicine, University of Guelph,

Guelph, Canada6 Present address: Veterinary Sciences Division, Bacteriology Branch,

Agri-Food and Biosciences Institute, Stormont, Stoney Road,Belfast BT4 3SD, UK

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during disease control or conservation monitoringprogrammes during which large numbers of animals aretrapped (Littin and Mellor 2005; Spotswood et al. 2012). Inthese instances, even a relatively low injury or mortality ratecould result in large numbers of animals suffering unduly(Littin and Mellor 2005; Spotswood et al. 2012). A great dealof effort and research have been employed into developingguidelines for trapping methods to reduce the likelihood oftrap-related injuries in animals captured (e.g. Iossa et al.2007; Talling and Inglis 2009; Sikes and Gannon 2011).However, with wildlife management programmes of long du-ration, trap-related injuries patterns need to be monitored overtime (Powell and Proulx 2003). This element of wildlifeprogrammes is somewhat understudied and limited monitor-ing, best practice guidelines or case studies have been under-taken (but see Arnemo et al. 2006 for discussions with mor-talities). Longitudinal monitoring of wildlife injuries may al-low for iterative re-evaluations of trap design and deploymentprocedures (i.e. adaptive management approaches). The cen-tral tenet of such programmes is to learn from past experiencesin order to improve programmes and reduce uncertainties(Cowan and Warburton 2011). Developing efficientstandardised operating procedures (SOPs) that are sensitiveenough to detect change in injury patterns and rates, whilstbeing efficient enough to allow for the processing of largenumbers of animals, can be challenging during large-scalewildlife management programmes. Here, we present one suchsystem used to assess injuries to European badgers (Melesmeles) caught in stopped cable restraint traps in the Republicof Ireland.

Badgers are a host species of Mycobacterium bovis, thecausative agent of bovine tuberculosis (bTB), and have beenimplicated in the epidemiology of bTB in cattle in theRepublic of Ireland (ROI) and Great Britain (GB; Griffinet al. 2005; Bourne et al. 2007; Donnelly et al. 2006; Kellyet al. 2008; Byrne et al. 2014c). Due to this, there have been anumber of projects to establish ways to manage bTB preva-lence within badger populations, in the anticipation of reduc-ing spill-back transmission to cattle (Griffin et al. 2005;Bourne et al. 2007; Sheridan 2011; Sheridan et al. 2014).The two main approaches have been to cull or vaccinate(using Bacille Calmette Guérin (BCG) vaccines), both ofwhich require animals to be trapped (though free-shootingnon-trapped badgers has been trialled in GB and oral-baitformulations for the delivery of vaccines are in developmentin both ROI and GB). The two main trapping methods havebeen stopped cable restraints and cage traps (DAFF 1996;Woodroffe et al. 2005; Murphy et al. 2009). Both methodscan exhibit moderate trapping efficacy and can potentiallybe biased, for example, between adults and cubs (Tuyttenset al. 1999; Byrne et al. 2012). There is a significant differencein costs between the methods (restraints tend to be cheaper toimplement), as well as restraints being logistically easier to

employ, which has encouraged the use of restraints in vaccinetrials and prospective programmes in the Republic of Ireland(Byrne et al. 2012, 2013a). Both methods result in low prev-alence of serious injury (Woodroffe et al. 2005; Murphy et al.2009). However, both trapping methods could cause otherwelfare concerns related to stress or environmental exposure(Sharp and Saunders 2008; Talling and Inglis 2009). In thispaper, we concentrate solely on visible trap-related injuries butrecognise that this is only one component of animal welfare(Farm Animal Welfare Council 1992).

In the ROI, badgers are predominantly trapped usingstopped cable restraints for culling and vaccinationprogrammes, in efforts to control bTB (Sheridan 2011;Byrne et al. 2012, 2013a). Currently, badger population den-sities are reduced through culling (capture and then humanelykilled) in areas with chronic cattle bTB problems, with theintention of reducing interspecific disease transmission(O’Keeffe 2006; Sheridan 2011; Byrne et al. 2013b;Sheridan et al. 2014). Since 2009, culled badgers in the ROIhave undergone a standardised necropsy, performed by a vet-erinary pathologist who evaluates trap-related injuries. In thecurrent study, a system is described that could serve as a casestudy for other similar programmes and highlights the benefitsof a flexible adaptive management regime. The system is cur-rently being assessed for use in a forthcoming large-scale intra-muscular vaccination programme (Byrne et al. 2013a; Moreand Good 2015).

Methods

Study area

Badgers were removed from 24 counties in the ROI (totalcounties area: 59,000 ha). Badgers caught in CountyDonegal and County Mayo were not processed within thesame laboratory as all other counties, thus they were excludedfrom this analysis.

Capturing procedure

Badgers were captured as part of a national interim strategy toreduce badger population densities in cattle bTB hotspotareas, as implemented by the Department of Agriculture,Food and the Marine in the ROI (O’Keeffe 2006; Sheridan2011). Badgers were captured mainly at setts (complex sub-terranean burrow systems) or along ‘runs’ that radiate outfrom badger setts. In this ongoing programme, badger captureevents (11 nights of consecutive effort) were initially instigat-ed in response to a local cattle herd episode of bTB. Surveysby teams of trained, experienced field staff (n≈100 total staffmembers) were undertaken to locate badger setts. The locationof all setts identified were recorded and entered into a

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centralised geo-database. Setts were classified as active, orinactive, based on a number of field signs (presence of freshspoil, tracks, and bedding material; absence of vegetationgrowth within the sett entrance (Byrne et al. 2013b)).Attempts were made to capture badgers at active setts on ayearly basis (approximately), once a sett was recruited into themanagement programme (Byrne et al. 2013b). Badgers werecaptured using stopped cable restraints of 3 mm in diameterand 143 cm in length, which were constructed of a multi-strand steel cable wound around a core nylon filament(Murphy et al. 2009). The nylon filament within the multi-strand cable increased the flexibility of the restraint. The re-straints were fitted with a stop to prevent them closing beyonda minimum circumference of 28 cm (Murphy et al. 2009).This minimum was employed to reduce the likelihood of in-juries to adult badgers, but as a consequence, the traps areineffective for capturing immature badgers (Byrne et al.2012). Restraints were fitted with a swivel to reduce cabletwisting, as this can cause fraying or failure, and may lead tosevere injuries (see Darrow et al. 2009 for example with coy-ote). Restraints were fixed in the ground with an angle iron barand were held in place by two vertical wooden sticks whichsuspended the restraint 1–2 cm above the ground (Murphyet al. 2009). The design of the restraint was developed bythe Department of Agriculture, Food and the Marine (DAFF1996).

One or more restraints were laid at setts and on paths, in amanner to maximise captures (e.g. at the entrance of activeopenings; Byrne et al. 2013b). Traps were checked as early aspossible every morning, with all traps being checked before12.00 p.m. Captured badgers were humanely killed, whilstrestrained within the trap, by lethal gunshot (0.22 calibre rifle)to the head. All staff responsible for euthanizing badgers werelicenced and trained marksmen. Badger removals were madeunder licence from the responsible government department(National Parks and Wildlife Service). The restraints usedconformed with national legislation for humane trapping(Wildlife Act, 1976, Regulations 2003, (S.l. 620 of 2003)).All licencing, capturing and culling adhered to the IrishWildlife Acts (1976 to 2010—section 23(6)(A)).

All badgers captured during this programme, within the 24counties sampled, were sent to a centralised laboratory for PMby the same veterinary pathologist, ensuring standardisationacross the study period. Badgers were transported, via cou-riers, three times per week to reduce the period between cap-ture in the field and arrival at the laboratory (Byrne et al.2014a). Badgers were transported double-bagged in two ‘cat-egory 1’ (high risk) biological material bags, clearly labelled‘for disposal only’ (in accordance with EU legislation).Badgers awaiting transportation by courier were kept in securestorage within District Veterinary Offices (DVOs) before col-lection and transportation. The majority of badgers were proc-essed within the centralised laboratory (PM and tissue

harvesting) on the day of arrival. When badgers were notprocessed on the day of arrival, the cadavers were kept in coldstorage (0–1 °C) until being processed.

Post-mortem assessment

There was no selection bias in this study as all badgers cap-tured from the 24 counties sampled were assessed by a veter-inary pathologist. Each badger captured was necropsied andassessed for damage, through visual inspection of the skin andsubcutaneous tissues. Observations were made in relation tothe external condition of the badger, hair loss, abrasions andexternal bite wounds. Any fractures of the limbs or ribs wererecorded. A standardised operating procedure (SOP) was de-veloped to quantify/classify the extent, or degree, of injuriessustained by badgers due to trapping. A rapid SOP was re-quired in order to process the large volumes of badgers beingassessed, whilst maintaining sensitivity for the detection ofpotential changes in the injury status of badgers captured overtime. The development of the SOP was informed by experi-ences gained from a previous large-scale badger removal pro-ject (the Four Area Project; Griffin et al. 2005). A scoringsystem was developed based on the study by Murphy et al.(2009) but was simplified by combining injury categories(skin, subcutaneous tissue, muscle and more severe injuries(limb fractures)) to give one overall score for injury (Table 1).The injuries were assessed by gross visual inspection solely(similar to Woodroffe et al. 2005), without histopathology,due to the large volumes of animals processed (as recom-mended by Murphy et al. 2009). Continual development ofthe systemwas undertaken to ensure it was fit-for-purpose anddelivering efficient welfare standards (in terms of trap-relatedinjuries) in a consistent manner. At a later stage in the pro-gramme (after 2009), a precautionary principle was applied,whereby badgers that were borderline between the scores 0and 1 were always elevated to score 1. As most injuries in-curred were minor, the scoring system developed was moresensit ive than the International Organization forStandardization (ISO) standards (ISO 1999; see Murphyet al. 2009). The equivalent European (DG-ENV) HumaneTrapping Standards categories, for testing restraining traps,for each score are included in Table 1 (Talling and Inglis2009). We assign the trauma description, as presented onpages 139–142 of Talling and Inglis (2009), to each category.It should be noted that the categories closely follow the NewZealand trap approval system (New Zealand Animal WelfareAdvisory Committee 2005).

Lymph nodes and organ tissues were harvested from ap-proximately one third of the animals for bacterial culture (seeByrne et al. 2014a for details). The pregnancy status of allfemale badgers was assessed, whether there was evidence ofthe animal being or having been pregnant (e.g. inspecting thethickness of the uterine wall, the presence of placental scars

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and teat morphology; Byrne et al. 2014a). All badgers wereweighed, sexed, and age-classed using tooth wear and size(young, adult or old; Murphy et al. 2009). Badgers weighedon average 9.7 kg, but weight varied significantly across sea-sons, lightest in March to July (mean weight 8–8.5 kg), andheaviest in October through to December (mean weight 10.5–11.5 kg; Byrne et al. 2015). Males were, on average, heavierthan females (mean difference ~0.5 kg; Byrne et al. 2015). Forbadgers captured during September 2012 to December 2012(n=2040), the position of the cable restraint on the body wasalso recorded as restraint position may affect injury (abdomen,shoulder/axilla or thorax; see Murphy et al. 2009).

Analysis

Logistic models (logit model for a binary response by maxi-mum likelihood estimation) were used to analyse factors af-fecting injury severity score. To do this, injury classes wereaggregated in order to create a binary outcome. The first suiteof models aggregated classes zero and one (no damage or skinindentation/hair removed) and classes two to five (subcutane-ous oedema to fractures). The second suite of models aggre-gated classes zero to two, and classes three to five were ag-gregated. The independent variables (possible predictors ofinjury) are listed in Table 2. For each suite, two models werebuilt. The first model used data on all badgers that underwentPM (captured from March 2009 to December 2012) with fullcapture and PM records. A second model was built using thesubset of data that included restraint position.

Univariable models were run between each potential pre-dictor variable and the outcome. All independent variablesassociated with the outcome (injury) variable at a P<0.2 werecandidate variables for the multivariable logistic model(Dohoo et al. 2009). A backwards-elimination approach wasused to build parsimonious multivariable models, withBayesian information criterion (BIC) used to compare com-peting models. Two-way interaction terms were tested duringmodel building and retained only if significant at P<0.05. Amodel with the lowest BIC value was considered the preferredmodel. Model fit was assessed using the Hosmer–Lemeshow

Table 1 Classifications and descriptions of injuries incurred by 18,596 badgers assessed at post-mortem for injuries in the Republic of Ireland from2009–2012

Injuryscore

Classification Description Trapping standardsequivalenta

Freq. % Cum. %

0 No impact No effect found due to capturing process. Mild 497 2.59 2.67

1 Skin/hair compression Skin/hair compression. Hair loss and/or denudingof epithelium but no cutting of the skin. Withor without linear congestion or minorhaemorrhage immediately below the cablerestraint, with no extension beyond thecable restraint.

Mild 15,084 78.7 83.79

2 Subcutaneous oedema Skin indentations with subcutaneous oedemaand/or haemorrhage that extend beyond theline of cable restraint and may extend intothe superficial layers of muscle beneath.

Mild 2887 15.06 99.31

3 Skin abrasions Skin cuts 0–8 cm in length. Subcutaneousoedema and/or haemorrhage extendinginto the muscle.

Mild 88 0.46 99.78

4 Severe skin abrasions Severe skin cuts >8 cm in length. Mild/moderate 26 0.14 99.92

5 Fracture Fractured limb or rib. Moderate/moderatelysevere

14 0.07 100

6 Death Death due to being captured within a restraint Severe 0 0 100

a Talling and Inglis 2009, pages 139–142

Table 2 Predictors evaluated in multivariable analyses, investigatingpotential factors associated with injury risk in badgers

Predictor Description

Season (meteorological) Spring (March–May); summer (June–August);autumn (referent; September–November);winter (December–February)

Year Calendar year (2009; referent)

Weight Weight at post-mortem (kg)

Gender Male or female

Pregnancy status Evidence of being pregnant at some stage ofanimal’s life (yes/no)

Age class Young, adult or old (based on tooth wear)

Restraint position(2012 only)

Position of cable restraint on the badger bodyas recorded at post-mortem (abdomen,shoulder/axilla or thorax; see Murphy et al.2009 for details)

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test (Dohoo et al. 2009). All analyses were performed in Stata11 ® (StataCorp, College Station, Texas, USA).

Results

In total, 18,596 badgers were captured within a restraint andassessed at PM (Table 1). The majority of badgers assessed(n=15,581; 84 %) during the present study had no impact ofrestraint recorded or hair loss and mild denuding of the skin(score 0–1; Table 1). Of the badgers that exhibited more se-vere damage, 96 % (n=2887) had subcutaneous oedema(score 2). There were no badger deaths attributable to re-straints recorded during the study.

Model suite 1: injuries scores greater than one

The injury severity score was significantly affected by year,season, age class, and gender (Table 3) but not pregnancystatus or weight (P>0.1). There was a significant increase inthe probability of a badger exhibiting scores >1 if caught laterin the study (2009 vs. all other years; P<0.001), with thehighest risk of badger injury recorded in 2012. Injury riskwas also significantly higher in summer or autumn vs. thewinter or spring (P<0.001; Table 3). ‘Older’ badgers had sig-nificantly higher probabilities of being in the higher injurycategory than other badgers (P<0.01). However, there wasno significant difference in injury risk between young andadult badgers (P=0.699). Male badgers had 1.7 times the oddsof being in the higher injury category than female badgers(P<0.001).

The majority of the badgers evaluated in 2012 were re-strained around the thorax (56 %), with the remainder beingrestrained around the abdomen (41 %; Table 4) or across theshoulders, neck and/or forelimb (2.7 %; Table 4). There was alarge difference in the odds of exhibiting higher injury scoresdepending on the site of injury (Table 5). Badgers restrainedaround the thorax had the highest probability of being in thehigher injury category, with a mean predicted probability of0.46 (P<0.001; Table 5). Badgers restrained around theshoulder-axilla area were at significantly lower risk of injury(mean predicted probability of 0.29) in comparison with bad-gers restrained around the thorax (P=0.007) and were at sig-nificantly higher risk of injury than badgers restrained aroundthe abdomen (mean predicted probability of 0.03; P<0.001;Fig. 1).

Model suite 2: injuries scores greater than two

Similar to the results frommodel suite 1, there was greater riskof severe badger injury for males than females (OR 1.44;P<0.001; Table 6) and decreased risk for badgers capturedin winter than other seasons (OR 0.81; P=0.011). Severe in-jury risk did not significantly increase between 2009 and2011; however, there was a significant decrease in risk ofsevere injuries in 2012 in comparison with 2010 and 2011(P<0.02; Table 6). Age class was not related to risk of injury,but increased weight decreased the odds of injury (OR 0.829;P<0.001; Fig. 2).

For badgers assessed for injuries in relation to restraintposition, there was a significant decreased risk for adults com-pared with old badgers (P<0.001; Table 7) and increased risk

Table 3 Factors affecting theprobability of a culled badgerexhibiting an injury score >1,during 2009–2012

Odds ratio Std. Err. z P>|z| Lower 95 % Upper 95 %

2009 1

2010a 2.850 0.279 10.70 0.000 2.352 3.452

2011a 1.714 0.170 5.44 0.000 1.412 2.081

2012a 3.365 0.325 12.57 0.000 2.785 4.066

Old 1

Adultb 0.169 0.093 −3.23 0.001 0.058 0.497

Youngb 0.182 0.106 −2.93 0.003 0.058 0.569

Autumn 1

Springc 0.704 0.036 −6.92 0.000 0.637 0.777

Summerc 0.979 0.161 −0.13 0.895 0.709 1.351

Winterc 0.739 0.038 −5.94 0.000 0.669 0.817

Female 1.000

Male 1.651 0.068 12.21 0.000 1.524 1.790

aWald tests: 2010 vs. 2011: χ2 (DF 1)=85.85; Prob>χ2 <0.001; 2010 vs. 2012: χ2 (DF 1)=11.28; Prob>χ2 <0.001; 2011 vs. 2012: χ2 (DF 1)=173.15; Prob>χ2 <0.001bWald test: adult vs. young: χ2 (DF 1)=0.15; Prob>χ2 =0.699cWald tests: spring vs. summer: χ2 (DF 1)=4.01; Prob>χ2 =0.045; Spring vs. Winter: χ2 (DF 1)=0.94;Prob>χ2 =0.333; summer vs. winter: χ2 (DF 1)=2.89; Prob>χ2 =0.089

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of injury if caught at the thorax in comparison with the abdo-men (borderline significant: P=0.064; Table 7).

Monitoring and adaptive management system case study

Badgers with injury scores of grade 3 or above, fromNovember 2009 onwards, were investigated through the adap-tive management system, specifically to determine the mostlikely cause of severe injuries. Field staff, involved in thecapture, were contacted to comment on the condition of thebadger when trapped and to gain additional information. Intotal, 87 badger captures were investigated (0.5 % of total)with a response rate from field staff of 87 % (informationwas not attained on 11 specific captures).

Few severe injuries were received due to the cable restraintmechanism (13 %; n=10; 4 failures, 6 restraint damage).Based on our best judgement, placing restraints at inappropri-ate sites accounted for 13 % of the severe injuries (n=10; 6wire fencing, 2 suspension, 2 prolonged restraint).Inappropriate deployment of the fixed iron bar contributedanother 16 % (n=12) to severely injured badgers. The causeof severe injuries could not be identified in 18 % of badgers.Injuries due to illegal snaring (by unidentified persons)accounted for 12 % of severe injuries investigated. On 16occasions, badgers were re-captured after being restrained ata previous capture event (these constituted 21 % of the 76badgers with severe injuries)—on 12 of these occasions bad-gers escaped due to bar placement failure (bar pulled out), theremaining four occasions were due to restraint failure. Further

details of the badgers investigated for severe injuries are pre-sented in Table 8. Where inappropriate practices were identi-fied, the field staff was notified of the welfare policyemployed during the programme. Field staff were also askedfor feedback to improve the functioning of the programme, inan effort to limit future injury risk to badgers. These sugges-tions were then assimilated into yearly professional develop-ment courses, so improvements across the programme couldbe made in an iterative fashion. An example of the value ofthis monitoring occurred during the study period (2012), whenbadgers received injuries (predominantly injury scores of two)from restraints due to excessive cable kinking. This was re-ported by both field staff and the veterinary pathologist(through the injury monitoring) and investigated furtherthrough the adaptive management system. A temporary re-straint manufacturing error was identified, whereby the centralnylon cord was absent from a batch of restraints, increasingthe likelihood of kinking, fraying and potential failure. Thebatch was immediately re-called, and a new batch with nylonfilaments was dispatched. No other severe injury caused bythis manufacturing error was detected thereafter, with contin-ued monitoring.

Discussion

During this study, no badger mortalities directly associatedwith capture within a restraint was recorded, despite the cap-ture of a large number of animals (n=18,596). Arnemo et al.

Table 4 Frequency table forinjuries incurred by badger inrelation to the position at whichthe cable restraint was located

Injury score category Abdomen Shoulder/axilla Thorax Total (column %)

Skin ident/hair removal 806 39 630 1475 (72.3 %)

Subcutaneous oedema 20 16 517 553 (27.1 %)

Skin abrasions 1 0 10 11 (0.5 %)

Severe skin abrasions 0 0 0 0 (0.0 %)

Fracture 0 0 1 1 (<0.1 %)

Total

(row %)

827

(40.5 %)

55

(2.7 %)

1158

(56.8 %)

2040

(100 %)

Table 5 The effect of therestraint position on theprobability of a culled badgerexhibiting a higher injury score(score >1), during September toDecember 2012

Odds ratio Std. Err. z P>|z| Lower 95 % Upper 95 %

Autumn (referent) 1

Winter 2.005 0.263 5.30 0.000 1.551 2.593

Abdomen (referent) 1

Shoulder-axillaa 15.638 5.843 7.36 0.000 7.519 32.524

Thoraxa 35.728 8.257 15.47 0.000 22.714 56.199

Female (referent) 1

Male 1.581 0.181 4.00 0.000 1.263 1.979

aWald tests: shoulder-axilla vs. thorax: χ2 (DF 1)=7.23; Prob>χ2 =0.007

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(2006) suggest that mortality rate should be below 2 %, butideally zero, for large free-living mammals. The zeromortalityrate was achieved within this system by implementing therecommendations of Arnemo et al. (2006): ‘(1) using an ex-perienced professional capture team, (2) developing and fol-lowing a capture protocol specific to [the target] species and(3) requiring that a mortality assessment be undertaken afterany capture-related death’. Coupled with these were robustpractical evaluations, communication between stakeholdersand adaptive management processes.

We found that a minority of animals trapped had experi-enced minor (score 2; 15.5 %) or more severe injuries (score≥3; 0.69 %). However, severe injuries did occur, and thesewere investigated specifically (see below). We found thatmales consistently were at higher risk of experiencing an in-jury whilst trapped than females, which was not found inprevious assessments of trap-related badger injuries(Woodroffe et al. 2005, n=5964; Murphy et al. 2009, n=343). This finding suggests that male badgers struggle morewhilst being restrained than female badgers. There was evi-dence that the site at which the restraint was positioned on thebody of the badger had a significant bearing on the severity ofinjury to the badger. The least likely position for injury wasaround the abdomen, with the most likely being the thorax.The thorax may be at increased injury risk due to pressureexerted between the sternum/rib cage and the cable restraint.The risk of severe injuries, with an injury score of three ormore, was significantly affected by badger weight. Heavier

Fig. 1 Mean predicted probability of a badger exhibiting injury (injuryscore >1) depending on position of the restraint around the body (ABabdomen, SA shoulder-axilla, T thorax)

Table 6 Factors affecting the probability of a culled badger exhibitingan injury score >2, during 2009–2012

Odds Std. Err. z P>|z| Lower 95 % Upper 95 %

2009 1

2010a 1.059 0.157 0.39 0.699 0.792 1.416

2011a 1.062 0.156 0.41 0.679 0.797 1.416

2012a 0.843 0.127 −1.13 0.257 0.628 1.133

Autumn 1

Springb 0.856 0.091 −1.47 0.141 0.695 1.053

Summerb 1.107 0.290 0.39 0.698 0.662 1.849

Winterb 0.743 0.076 −2.89 0.004 0.608 0.909

Weight 0.829 0.020 −7.87 0.000 0.791 0.869

Female 1

Male 1.436 0.106 4.91 0.000 1.243 1.659

aWald tests: 2010 vs. 2011 χ2 (DF 1)=0.00; Prob>χ2 =0.971; 2010 vs.2012 χ2 (DF 1)=5.51; Prob>χ2 =0.019; 2011 vs. 2012 χ2 (DF 1)=6.21;Prob>χ2 =0.013bWald tests: spring vs. summer: χ2 (DF 1)=1.04; Prob>χ2 =0.308;spring vs. winter: χ2 (DF 1)=2.19; Prob>χ2 =0.139; summer vs. winter:χ2 (DF 1)=2.38; Prob>χ2 =0.122

Fig. 2 Predicted probability of a badger exhibiting injury (injury score>2) in relation to weight at capture (grey dots). Dashed line representslocally weighted smoothed curve (LOWESS curve)

Table 7 The effect of the restraint position on the probability of a culledbadger exhibiting a higher injury score (score >2), during September toDecember 2012 (n=1989). Young and shoulder-axilla were omitted dueto collinearity and zero positive observations, respectively

Odds Std. Err. z P>|z| Lower95 %

Upper95 %

Old 1.000

Adult 0.072 0.048 −3.92 0.000 0.019 0.269

Young Omitted

Abdomen 1.000

Shoulder-axilla Omitted

Thorax 3.306 2.137 1.85 0.064 0.931 11.735

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animals had a lower risk of having a severe injury than lighteranimals. This may be due to a protective effect of subcutane-ous body fat (Murphy et al. 2009), especially around areassuch as the thorax, decreasing the pressure between therestraint and the sternum/rib cage. There was significant sea-sonal variation in injury risk. Badgers were at greater riskduring summer and autumn than winter and spring periods.Murphy et al. (2009) found that summer was the highest riskperiod for trap-related badger injuries and suggested this wasrelated to the seasonal fluctuation in badger body weight asbadgers are lightest in the summer and heaviest in the lateautumn and early winter (Murphy et al. 2009; Byrne et al.2015). From a practical management perspective, due to thetraps being non-selective amongst badgers, mitigating actionsto reduce additional risk to males relative to females, or olderrelative to other age classes, or body position is limited.However, the seasonal variation in injury risk could be miti-gated by reducing the amount of capturing undertaken duringsummer months, when badger weights are at their lowest (themonth with the lowest mean badger weight was July; Byrneet al. 2015). Currently, as part of the interim cull policy inROI, the least number of badgers are caught in July (Byrneet al. 2013b), but consideration could be made to reduce theamount of trapping with stopped restraints even further duringthis period.

There was an increased risk of injuries, with a score of twoor greater, across years of the study; with the highest riskrecorded during 2012 (Table 6; Fig. 3). This suggested thatthe adaptive management regime was not effectively decreas-ing the risk of trap-related injuries. However, when the risk ofbadgers exhibiting severe injuries (score of three and above)

Table 8 Details derived frominvestigations of severe (score ≥3)injuries to badger, recordedduring post-mortem in theRepublic of Ireland (2009–2012)

Cause Freq. Percent Details

Escaped with restraintbut re-captured

16 21.05 Escaped with restraint around body due to bar (12) or restraint (4)failure. Badgers were re-capturedwith restraint still on the body.

Unknown 14 18.42 Unable to establish cause of injury. These captures are usuallydeemed ‘unexceptional’ by field staff. Normal captureprocedures were undertaken and no problems reported.

Tangled in roots/briars 11 14.47 Badgers, or restraints, get tangled in tree roots (8) or thorny briarvegetation (3).

Illegal snare 9 11.84 Evidence of badgers being caught previously in illegally set free-running snares.

Restraint damage 6 7.89 Badgers were damaged due to the restraint mechanism. Examplesinclude excessive twisting (1), constricting due to cablewrapped tightly around bar (1), badger being caught in tworestraints (1).

Wire fencing 6 7.89 Badgers damaged due to tangling with barbed wire (4) or wirefencing (2).

Wedged in sett 4 5.26 Badgers wedged within sett opening.

Dogs 3 3.95 Evidence of restrained badger being attacked by dogs.

Road casualty 3 3.95 Badgers that already experienced injury and damage due to a roadtraffic accident.

Suspension 2 2.63 Badgers captured upon steep clay bank, where the captured badgerwas unable to regain footing. The badger was suspended by therestraint.

Prolonged restraint 2 2.63 On one exceptional occasion, two badgers were restrained for 48 hdue to flash flooding making the sett inaccessible under workerhealth and safety regulations.

Total 76 100

Fig. 3 Trends in the proportion of assessed badgers with injury scores of2 and injury scores of 3–5

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was modelled, there was no evidence of an increased temporaltrend (Table 6). Indeed, 2012 had the lowest risk of moreserious injury (Table 6; Fig. 3). Therefore, as depicted inFig. 3, the increased risk was driven by the increased preva-lence of badgers with injury scores of two. This was at leastpartially driven by a manufacturing error (as described above),which was subsequently identified and rectified. However,details that may shed more light on the drivers of this patternare currently lacking. Further investigation of this phenome-non is recommended (see below). Potentially, the length oftime badgers were restrained could contribute to increased riskof injury (Proulx et al. 1994, 2015). However, this has notbeen found in previous badger research (Woodroffe et al.2005; Murphy et al. 2009). Furthermore, the set diameter ofthe restraint aperture may impact on the subsequent capturesite (smaller aperture may result in restraint locating at theshoulder/axilla or thorax; Murphy et al. 2009), resulting inincreased risk of injury. Reducing the aperture of the restraintmay increase the capture probability, by decreasing the possi-bility of badgers freeing themselves from the restraint. Duringlongitudinal management programmes, where density is re-duced by repeated removals (Byrne et al. 2013b) and in-creased effort may be required to capture badgers (i.e. dimin-ished returns) (Byrne et al. 2012), there may be a trade-offbetween maintaining high-welfare standards and trapping ef-ficacy. It is our opinion, in such situations, that practitionersshould err on the side of caution and not increase the risk ofinjury for the potential benefits of increased efficacy. Instead,improvements in trap design and deployment methods shouldbe implemented, where possible.

Template for injury monitoring with adaptivemanagement

During large-scale trapping programmes, we recommend theuse of integrated adaptive management systems to monitor,and reduce where possible, trapping-related injuries. A sche-matic of such a system is presented in SupplementaryMaterialFig. 1. Where large numbers of trapped animals require as-sessment, the system relies on the development of a standardpractical assessment of injuries applied by a qualified teammember(s) (for example, a veterinarian or pathologist).Excessively detailed assessments increase costs and time bud-gets and increase the period under which an animal needs tobe handled for live-trapping assessments, for example duringvaccination programmes. Alternatively, insensitive techniquescan result in a poor monitoring tool, incapable of identifyingchanges in injury rates. Development of a robust standardprotocol may require specific research projects; however, itmay also be improved through adaptive management. Thecreation of the role of an investigator (for example, a seniorfield staff member) is required; responsible for both the dis-semination of information throughout the stakeholders within

the programme (managers, field staff, trapmanufacturers, etc.)and to investigate cases of serious injury. Feedback on expe-riences of different stakeholders throughout the system shouldbe disseminated, and innovations (e.g. in trapping deploymenttechnique) should be incorporated through an ongoing itera-tive process. Serious issues should be dealt with in short timeframes, with recommended changes implemented quickly tosupport best practice (e.g. technical faults with equipment orinappropriate deployment of traps). Non-essential innova-tions, that may improve general efficiencies within the system,could be introduced on a yearly basis during annual profes-sional development training days, allowing uniform imple-mentation across the programme as opposed to piecemealchanges. Communication throughout the stakeholders groupsand transparency of information is essential for developingself-evaluation and regulation.

With regards the current badger management scheme in theROI (O’Keeffe 2006; Sheridan 2011; Sheridan et al. 2014),the system has worked well to reduce frequency of trap-related injuries and ensured that field staff continually upholdbest practice guidelines. The identification of a temporary trapdefect was one obvious example of an accrued benefit of themonitoring programme, though continual evaluation ensuredthat standards were kept high over an extended period. Aparticular benefit of the structured approach was to identifyclear areas for future research (see below). These future inves-tigations will be clearly important as badger managementmoves from the interim culling programme, towards BCGvaccination of captured badgers using stopped cable restraintswithin the Republic of Ireland (O’Keeffe 2006; Sheridan2011; Byrne et al. 2013a; Sheridan et al. 2014).

We recommend the following for the future developmentand improvement of the system:

& Improved communication between investigators, localmanagement and field staff. Develop formalised proce-dures (e.g. develop injury checklists) to allow greaterscope for analysis and improve efficiencies. Improve theresponse rate from field staff to investigators during eval-uation of serious injury investigations.

& The development of an annual reporting mechanism, in-cluding trend analysis based on current data, to ensure thatstakeholders can access up-to-date information quicklyand self-evaluate against their peers, locally andnationally.

& Publish annual reports to ensure transparency within thesystem and for interested stakeholders outside of the sys-tem (e.g. NGOs, government officials and wildlife practi-tioners in other jurisdictions).

& Generate, and test, hypotheses as to the drivers of low-grade badger injuries. For example, record restraint periodaccurately and assess if this measure correlates with injurystatus (see Murphy et al. 2009).

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& Continual implementation of stringent guidelines for thedeployment of cable restraints (i.e. strict avoidance of lay-ing restraints near barbed wire, avoid areas with potentialfor dogs to attack trapped animals and avoid potentiallyinaccessible sites like spate rivers (liable to quicklyflood)).

& Development of external audits, on a sample of animalsassessed, to ensure necropsy evaluations standards aremaintained.

& Develop SOPs for live-trapping monitoring, for currentand future large-scale vaccination programmes, where an-imals will be marked-released-re-captured (e.g. Byrneet al. 2013a, 2014b). For re-captured badgers, assessmentsof any longer-term physical effects of being capturedwith-in restraints should be developed, evaluated, and reportedon (Cattet et al. 2008; Dechen Quinn et al. 2014).

& Whilst there was a zero mortality rate recorded during thepresent study, we cannot discount the possibility that asmall number of animals that escaped restraint may havesubsequently died from injuries and had gone undetected(Proulx et al. 2015).We recommend further evaluations ofthe frequency and impact of animals that free themselvesfrom restraints during culling programmes. Record thefrequency of unsuccessful trapping attempts (count thenumber of empty traps sprung by target species), as apotential indicator of the proportion of the target popula-tion evading capture from restraints.

& Develop research projects to assess other factors influenc-ing welfare impacts (e.g. stress monitoring) other thantrap-related injury and develop practical methods for re-ducing such issues.

Conclusion

Monitoring of trap-related injuries is essential to maintain thehigh standards, in one important aspect of animal welfare,during large-scale programmes where the live capture of ani-mals is required. The current capturing system (the practicaland inexpensive use of stopped cable restraints) and monitor-ing system employed in the ROI, for the capture of badgers,has resulted in a zero mortality rate and very low rates ofmoderate/severe injury. The flexible, adaptive managementapproach to managing such a system could be applied to otherprogrammes (for example, vaccination programmes), wherelive capturing of wildlife is undertaken. Essential to the suc-cess of such a system is the continual re-evaluation (both self-evaluation against peers and managerial overseeing) and re-development (flexibility to incorporate changes to improveefficiencies and welfare outcomes); ongoing communicationbetween stakeholders (both formalised and non-formalised);

and incorporation of best practices (based on robust science)and transparency (in reporting).

Acknowledgments AWB was funded by a post-doctoral fellowship(PDF-1) in University College Dublin. Data collection and managementfor this study was funded by the Department of Agriculture, Food and theMarine, Ireland (www.agriculture.gov.ie).

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