How to mitigate impacts of wind farms on bats? A review of potential conservation measures in the...

Environmental Impact Assessment Review 51 (2015) 10ndash22

Contents lists available at ScienceDirect

Environmental Impact Assessment Review

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How to mitigate impacts of wind farms on bats A review of potentialconservation measures in the European context

Filipa Peste ab Anabela Paula c Luiacutes P da Silva abd Joana Bernardino e Pedro Pereira e Miguel Mascarenhas cHugo Costa e Joseacute Vieira f Carlos Bastos f Carlos Fonseca ab Maria Joatildeo Ramos Pereira agh

a Centre for Environmental and Marine Studies (CESAM) Portugalb Department of Biology University of Aveiro Portugalc Bioinsight - Ambiente e Biodiversidade Lda Lisboa Portugald MARE and CEF Department of Life Sciences University of Coimbra Portugale Bio3 - Estudos e Projectos em Biologia e Recursos Naturais Lda Almada Portugalf Department of Electronics Telecommunications and Informatics IEETA University of Aveiro Portugalg PPGBAN Department of Zoology Institute of Biosciences Federal University of Rio Grande do Sul Brazilh PPGEC Federal University of Mato Grosso do Sul Brazil

Corresponding author at Centre for EnvironmentalDepartment of Biology University of Aveiro Campus dPortugal Tel +351 234247138

E-mail addresses filipapestegmailcom fpcostauap

httpdxdoiorg101016jeiar2014110010195-9255copy 2014 Elsevier Inc All rights reserved

a b s t r a c t

a r t i c l e i n f o

Article historyReceived 17 July 2014Received in revised form 5 November 2014Accepted 26 November 2014Available online xxxx

KeywordsWind farmsImpactsBatsMitigation hierarchyOffsetscompensation measures

Wind energy is growing worldwide as a source of power generation Bat assemblages may be negatively affectedbywind farms due to the fatality of a significant number of individuals after collidingwith themoving turbines orexperiencing barotrauma The implementation ofwind farms should follow standard procedures to prevent suchnegative impacts avoid reduce and offset in what is known as the mitigation hierarchy According to thisapproach avoiding impacts is the priority followed by the minimisation of the identified impacts and finallywhen residual negative impacts still remain those must be offset or at least compensated This paper presentsa review on conservation measures for bats and presents some guidelines within the compensation scenariofocusing on negative impacts that remain after avoidance and minimisation measures The conservationstrategies presented aim at the improvement of the ecological conditions for the bat assemblage as a wholeWhile developed under the European context the proposed measures are potentially applicable elsewheretaking into consideration the specificity of each region in terms of bat assemblages present landscape featuresand policy context regarding nature and biodiversity conservation and management An analysis of potentialopportunities and constraints arising from the implementation of offsetcompensation programmes and gapsin the current knowledge is also considered

copy 2014 Elsevier Inc All rights reserved

Introduction

In the last 20 years wind energy became the fastest growing sourceof power generation in theworld and it is expected to continue growingin Europe North America and in the developing markets of China andIndia There is also a growing trend in Latin America new Asian andEastern European markets and in some African countries (Ledec et al2011 WWEA 2013) though in the past three years due to the globaleconomic crisis the rate of growth has slowed down (WWEA 2013)

In Europe during the last 30 years wind energy has grown from100 MW to over 100000 MW (EWEA 2012) Among European coun-tries Germany Spain Italy France UK and Portugal have shown an

and Marine Studies (CESAM) ampe Santiago 3810-193 Aveiro

t (F Peste)

extraordinary growth in wind energy in the last decade (WWEA2013) In fact energy produced from renewable sources is a priority inthe European Union (EU) agenda especially after the implementationof the Renewable Energy Directive in 2009 (200928EC) and subse-quent amending acts This directive establishes mandatory targets for2020 imposing a 20 share of energy from renewable sources by2020 in all member states As a consequence several member stateshave seriously invested in the development of wind energy as a crucialway to attain this goal

This goal shift towards a more sustainable production of energy toreduce the emission of greenhouse gases is certainly desirable but thedevelopment of wind energy facilities does not come free of risk ofnegative impacts on biodiversity (Voigt et al 2012) as well as noiseand visual impacts for local human communities (Leung andYang 2012)

Among vertebrates bats are pointed out as one of the most affectedgroups (Arnett et al 2011 Barclay et al 2007 Johnson et al 2003Rydell et al 2010) In the last few years the concern about the negativeimpact of wind farms on bat assemblages has significantly increased

11F Peste et al Environmental Impact Assessment Review 51 (2015) 10ndash22

among the scientific community Since the implementation of the firstwind farms in Europe and the USA it was assumed that bats could beaffected by collision with the moving turbines However this grouponly became a research focus when bat fatalities were documented aspotentially higher than bird fatalities (Cryan and Barclay 2009Rodrigues et al 2008 Rydell et al 2010)

Bat fatalities result from direct collision or from barotraumaie experiencing rapid pressure changes that cause severe internalorgan damage especially in the lungs (Baerwald et al 2008 Grodskyet al 2011 Rollins et al 2012) Bat fatality rates show significant vari-ation among sites and years and although there are general recommen-dations from EUROBATS for the monitoring and estimation of fatalities(eg Rodrigues et al 2008) the lack of standardised methods to esti-mate these rates hinders comparisons (EUROBATS 2012) Nonethelesssignificant fatality rates have been recorded in both theUSA and EuropeIn a review of the patterns of bat fatalities at wind energy facilities inNorth America (USA and Canada) Arnett et al (2008) present asmany as 696 bat fatalities per turbine per year In Europe although aglobal study has not been done yet it is known that fatality rates varylargely among sites and high numbers were also reported especiallyfrom Hohe Eck wind farm in southern Germany where rates of 411bat fatalities per turbine per year occurred (Rydell et al 2010)

In the European Union all wind energy developments that are likelyto have a significant impact on environment should be subjected to anenvironmental impact assessment (EIA) (Article 2 Directive 85337EEC) That is the formalised procedure that ensures that the likelyeffects of a new wind farm on the environment are fully understood(Jay et al 2007) and taken into account before the proposed project isgiven development consent For that reason they are a good decision-making tool on project viability (Rajvanshi 2008 McKenney andKiesecker 2010) and should identify and if possible quantify impactson biodiversity confirm the need for mitigation and set out the mitiga-tion required for the identified impacts (BBOP 2009a Marshall 2001)The negative impacts are mitigated through the implementation ofmeasures that aim at the reduction of those impacts to the pointwhere they have no adverse effects (BBOP 2012a) Within the EUthere are regulations that consider population effects and also regula-tions focusing on individual specimens of species that are strictlyprotected Ultimately both focus on negative effects that will occur atthe population level though considering that in threatened speciesthese effects are more severe so even a reduced number of fatalities isof great concern

Mitigation involves any process activity or action designed to avoidreduce or compensate those significant adverse impacts (Marshall2001) The mitigation measures are categorised according to theirgoals and following the mitigation hierarchy (a) avoid (b) reducemoderateminimise (c) offsetcompensate (Fig 1) (BBOP 2012dDarbi et al 2009 PricewaterhouseCoopers 2010) This hierarchy im-plies that avoidance strategies have priority over remedial solutions(Marshall 2001) and that those impacts that cannot be avoided orminimised must be addressed through biodiversity offsets or

Reduce Moderate Minimise

Avoid

Offset amp Compensate

Fig 1Mitigation hierarchy (adapted from PricewaterhouseCoopers 2010)

compensatory measures (BBOP 2009a PricewaterhouseCoopers2010) Strictly following the mitigation hierarchy it is important to un-derline that offsets or compensatory measures are the ldquolast resortrdquo andmust not provide a justification for proceeding with projects for whichthe residual impacts on biodiversity are unacceptable This means thatthe ldquono gordquo option has to be considered seriously and applied in caseswhere the destruction of unique habitats or irreversible loss wouldotherwise occur (BBOP 2012c Bishop 2006)

The last step of themitigation hierarchy the offset or compensationhas been acquiring importance and popularity among conservationists(McKenney and Kiesecker 2010 Kiesecker et al 2010) The clarifica-tion between those two concepts has been under discussion in recentyears and Biodiversity Offsets were defined by BBOP as ldquomeasurableconservation outcomes resulting from actions designed to compensatesignificant residual adverse impacts on biodiversity after appropriateprevention and mitigation measures have been takenrdquo The offsetmeasures should ldquoachieve no net loss and preferably a net gain of biodi-versity taking into account species composition habitat structureecosystem function and peoples use and cultural values associatedwith biodiversityrdquo (BBOP 2013 ten Kate et al 2011) To demonstrateno net loss or a net gain conservation action outcomes must demon-strate that biodiversity conserved is sufficient and of the same kind asthe biodiversity lost or degraded due to the projects impacts and thatbiodiversity persistence is not compromised or if possible enhanced(BBOP 2013 ten Kate et al 2011) For compensation there is no cleardefinition set by BBOP and the edge between these two concepts ismainly related with the capacity of a project to demonstrate that theconservation outcomes are enough to guarantee ldquono net loss or a netgainrdquo (BBOP 2013 ten Kate et al 2011)

Offsets are a relatively recent field of investigation (Hayes andMorrison-Saunders 2007) and the Business and Biodiversity OffsetsProgramme has developed and introduced the Standards on Biodiversi-ty Offsets These standards are based on 10 principles that provide aframework for the design and implementation of biodiversity offsetsand to verify its success (BBOP 2009a) (1) adherence to mitigationhierarchy (2) limits to what can be offset (3) landscape context(4) no net loss (5) additional conservation outcomes (6) stakeholderparticipation (7) equity (8) long-term outcomes (9) transparencyand (10) science and traditional knowledge

The compliance with these principles helps to ensure that adequateoffset programmes are created and implemented However there areseveral conservation programmes that for a variety of reasons aresimply unable to follow all these principles which is more evident inthe case of principle 4 mdash no net lossa net gain For some projects it isnot possible to prove no net loss because i) pre-impact data is lackingand it is impossible to know what was lost as a result of the projectandor ii) gains achievable by the conservation actions are not easilyquantified If so the programme in question should not be consideredas an offset but as a compensation programme Fig 2 illustrates thecontinuum from a very basic form of compensation to the type ofcompensation that is a full offset and may realistically be expected toachieve no net loss or even a net gain

Despite the recommendation to follow the mitigation hierarchymonitoring programmes in several Europeanwind farms have revealedthat in some situations significant impact over bat populations may beoccurring (EUROBATS 2013) So it is essential to guarantee that foreach wind energy facility the mitigation hierarchy is followed fromthe beginning and that this sensitive group is taken into account in allsteps In that context the implementation of the mitigation hierarchyshould start during the planning and design phase in order to avoidany important area such as breeding hibernating areas andor foraginghabitats of threatened bat species (EC 2010) However identifyingpotential impacts during the planning phase may be a difficult taskunless it is made in extreme circumstances with easily predictableimpacts or in the predictable absence of impacts (eg near an importantroost or at a hostile windy and cold site) Furthermore in some cases

Fig 2 Compensation-offset spectrum (from BBOP 2012d)

12 F Peste et al Environmental Impact Assessment Review 51 (2015) 10ndash22

the real effects are only indentified during the monitoring of the post-construction phase (eg Hein et al 2013) So an adaptive managementapproach should be followed in order to reconsider the mitigationhierarchy during the construction andor exploration phase based onmonitoring results to continually improve its performance (BBOP2009c) For unavoidable impacts minimisation measures for bat popu-lations usually include on-site efforts to remedy the effects of short-term damage Research on this subject has been significantly increasingin the last few years especially on ultrasound emissions as a way todeter bats from approaching wind turbines (Arnett et al 2013 Hornet al 2008 Johnson et al 2012 Spanjer 2006 Szewczak and Arnett2006a b 2007) Radar emissions also seem to negatively affect bat ac-tivity (Nicholls and Racey 2007 2009) However to our knowledgeuntil now no device was successfully developed or commercialisedNevertheless as bat mortality rates seem to be higher during lowwind nights (Amorim et al 2012 Kerns et al 2005 Rydell et al2010) the most effective mitigation measure seems to be the increaseof wind turbine cut-in speed (the velocity at which turbines start pro-ducing electricity) and changes in blade feathering (altering the angleof the blade preventing it from rotating on low wind situations) Thismeasure has been proven to reduce bat fatalities from 30 to 90(Arnett et al 2008 2011 Baerwald et al 2009)

If an adverse effect on the assemblage of bats cannot be definitelyeliminated or even reduced to acceptable levels through the above-mentioned measures and thus residual adverse effects on biodiversitystill remain offset or compensatory measures should then be considered(BBOP 2009a Darbi et al 2009 PricewaterhouseCoopers 2010) The ac-ceptable levels of impact referred above may vary between Europeanmember states in some countries the death of any individual bat of aprotected species is strictly forbidden while in others a reduced numberof fatalities is tolerated and evaluated on a case by case basis Howeverdespite that recommendation to our knowledge and to date no offsetor compensatorymeasures have been taken in Europe aimed at batmor-tality compensation (personal information obtained through inquiriesdone to the focal points of the EUROBATS Intersessional WorkingGroup on Bats and Wind Farms) It should be underlined however thatthe avoidance ofmortalitymust always be thefirst optionwhile compen-sationoffset of the acceptable impacts that remain after the implementa-tion of the mitigation hierarchy should be seen as the last resort

The lack of such measures is probably related to the lack of baselineknowledge on bat populations (eg Walters et al 2012) making it hardto assess the population affected and especially difficult withmigratingspecies (Voigt et al 2012) Actual knowledge on bat migration andmigratory paths is still scarce (eg Popa-Lisseanu and Voigt 2009)European bat species are classified into three migratory categories ac-cording to the distances recorded mdash long distance (N500 km) regional(100ndash500 km) and sedentary (b50 km) however not all populationsof known migratory species perform complete migrations and somemay even be sedentary along the range of occurrence of the species(Fleming and Eby 2003)

In this paper we reviewed a set of conservation measures that maybe applied and assessed in the context of compensation or offsettingthe impacts of wind farms on bat populations in particularly sedentaryor non-migrant species Although these measures were analysed underthe European land-use and policy context and considering the ecologi-cal requirements of the bat species that show higher mortality rates atEuropean wind farms the guidelines presented here are surely appro-priate elsewhere This review should be seen as a first approach to thesubject as in some cases the potential of the presented measures ismostly theoretical and it is crucial to investigate in more detail theirefficiency in different populations and regions

Review methodology and scope

Using a broad range of monitoring reports and other official docu-ments published between 2003 and 2013 we gathered information onthe species number of fatalities per species and seasonal trends in fatal-ities in European wind farms

To our knowledge no publication has addressed specific compensa-tory measures for bats at European wind farms so we investigated awide range of studies describing bat activity patterns taking intoaccount macro- meso- and micro-scale habitat features such as land-scape characteristics habitat forestryagricultural regime vegetationstructure and water and prey availability

Based on the review of i) the ecological requirements of the mostaffected bat species ii) the main threats to bat populations and iii)conservation strategies focused on bat populations we identified sever-al measures that could be used to compensate wind farm impact on batassemblages We focused on forest management actions to be imple-mented mostly in the surrounding area of the wind farms but distantenough to avoid the attraction of bats into their area of influence sothat by any means preventing an increase in fatalities numbers

Bat mortality in European wind farms

Presently only a few countries have published guidelines for themonitoring of bat fatalities at wind farms in the context of EIA(EUROBATS 2013) In most countries this monitoring is mandatoryonly in some situations and according to the potential impacts of thewind farm in question Even when monitoring schemes are in placethe results of those surveys are often not available or open to reviewor public access (Rydell et al 2010) which makes the evaluation ofthe patterns of bat fatalities in European wind farms quite difficult

The IntersessionalWorking Group onWind Turbines and Bat Popula-tions (EUROBATS) has however compiled information on this subject inthe European context Between 2003 and 2012 5139 dead bats weredetected either located accidentally or during post-construction moni-toring studies The report underlines that these numbers by no meansreflect the real extent of bat fatalities at wind farms even because many


infrastructures are not consistently monitored However these dataprobably represent the overall tendency in Europe (EUROBATS 2013)

Themajority of the fatalities occurred in Germany Spain France andPortugal but again this may be a consequence of the monitoringschemes being carried out in each country Between 2003 and 2012wind turbines in Europe killed at least 27 species of which the mostaffected were Pipistrellus pipistrellus (965 fatalities) Nyctalus noctula(704) P pipistrellusPipistrellus pygmaeus (597) Pipistrellus nathusii(593) and Nyctalus leisleri (383) These are all Least Concern (LC)species according to the IUCN Red List of Threatened Species althoughthe conservation status varies among the European countries For exam-ple in those four countries P pipistrellus and P pygmaeus are consideredleast concern species except in Germany where P pygmaeus is datadeficient N noctula is considered rare in Spain near threatened inFrance least concern in Germany and data deficient in Portugal andP nathusii is considered near threatened in France and least concern inGermany These differences in regional or national conservation statusof bat species imply that some measures may be priority in someareas but not in others and that compensatory programmes even iffollowing the general guidelines presented in this paper and elsewhere(eg Boye andDietz 2005 Entwistle et al 2001Meschede et al 2001)should be designed according to the regional and temporal context inwhich they are to be implemented

Ecological requirements of the most affected species

Table 1 summarises the ecological requirements of the five bat spe-ciesmost affected bywind energy facilities in Europe Information abouttheir distribution preferred foraging habitats flight paths and preyitems as well as breeding and hibernation requirements is presented

Those species that are rare or more threatened regionally such asN noctula N leisleri and P nathusii depend on wetlands and matureforests of deciduous trees to forage or roost indicating that the destruc-tion or degradation of these areas through cutting replacement byproduction forests or forest fires poses a negative impact for them

Potential offset and compensatory measures

In this work we bring together several measures that may be imple-mented to compensate the residual adverse effects of wind farms on batpopulations These measures are intended for the improvement ofecological conditions towards the increase of the carrying capacity forbat assemblages specifically for breeding and roosting conditions andthe increase of prey availability and accessibility These actions aremainly thought to be implemented in the surrounding area of windpower infrastructures but far enough to avoid the attraction of batsinto the wind farm area of influence Therefore measures related withroost and food availability have potentially larger scope andwill benefitboth sedentary andmigratory species otherswill mostly benefit seden-tary populations that use the vicinity of wind farms all year aroundWhenever there is bibliographic support of an increase in bat numbersor bat activity references are presented

As explained above bat populations are poorly known and presentseveral sampling constraints For instance for migratory bat species itis difficult to understandwhich populations are being affected and eval-uating the effects of the presented measures for those species is anextremely difficult task Despite the referred improving bats ecologicalrequirements in habitats that present limitations will certainly benefitthose populations at least at a local level So it is urgent to start studyingthis topic as it could be an important tool tomitigate residual impacts ofhuman infrastructures on bat populations

Management of autochthonous forests

Most native European forests are extremely important for a widespectrum of bat species especially ancient forests as opposed to even-

aged andmono-specific plantation forests due to their higher structuralcomplexity Bats usually prefer those habitats to forage and roost(Rainho 2007 Ruczyński et al 2010 Russ and Montgomery 2002Russo and Jones 2003 Waters et al 1999) though the specific struc-ture of each forest is closely linked to the array of bat species present(Ford et al 2005)

The maintenance and preservation of the existing conditions inmature autochthonous forests and the acceleration of the ecologicalsuccession of younger formations are crucial for bat conservationIn mature forests bats often use large trees and snags as roosts(Crampton and Barclay 1998 Hutson et al 2001 Kunz and Lumsden2003 Russo et al 2004) Simple actions such the preservation ofolder trees with cavities and well developed branches and the non-removal of standing or fallen dead trees should be adopted Theseactions are mostly relevant for the protection of tree-roosting batspecies and in the context of those more negatively affected by windfarms in Europe particularly N noctula and N leisleri Still besidesproviding roosts for bats these structures contribute to the enhance-ment of insect abundance and diversity increasing the availability ofpotential prey for bats (Dietz and Pir 2009 Guldin et al 2007 Russoand Jones 2003) However in some forest types branch thinning mayoccasionally be necessary in order to create flight corridors for batswith less manoeuvrable flights (eg Guldin et al 2007 Loeb andOKeefe 2006 Obrist et al 2011) creating vertical heterogeneity andpromoting the creation of niches that may be used by different species(Collins and Jones 2009 Plank et al 2012) Branch thinning may alsocontribute towards healthier tree development

Well-developed riparian galleries usually harbour great plant diver-sity and are frequently used as foraging grounds bymanybats includingspecies most affected by wind turbines in Europe (Table 1) Ripariangalleries act as a shield from the wind and are simultaneously home togreat diversity and abundance of arthropods (Peng et al 1992 Russoand Jones 2003Warren et al 2000) thus management actions aimingthe preservation or the restoration of those sites are fundamental Inmany areas these actions must include the removal of exotic invasiveplants because they override autochthonous vegetation together withthe plantation of native species (Guil and Moreno-Opo 2007Marchante et al 2005) Changes in trophic structures have alreadybeen shown for spiders in response to invasive plants (Petillon et al2005) Some exotic plants like Australian acacias which are amongthe most significant invaders worldwide (Richardson and Rejmaacutenek2011) have an aggressive invasive behaviour forming dense foreststands These dense stands block the development of native species(Marchante et al 2005) may change river-flow (Richardson et al2007) and fire regimes (Kull et al 2011) andmay also preclude the ac-cess of foraging bats to these areas due to high clutter For thewaterlineitself management actions should promote additional heterogeneity ofthewater flow The creation of backwater areas that endorse vegetationaccumulation favours i) species directly affected by wind farms asP pipistrellus (Warren et al 2000) ii) species least affected that huntin smooth water such as Myotis daubentonii (Warren et al 2000) andiii) species apparently not affected by wind farms such as Myotiscapaccinii considered vulnerable by IUCN (Biscardi et al 2007) whichmay result in an additional positive outcome in a compensatory schemefor awind farm Promoting rapid areas that allowwater oxygenation fa-vours breeding sites for several species of arthropods potentially in-creasing prey availability for bat species (Capinera 2010 Entwistleet al 2001)

In traditional agro-forestry European ecosystems such as Montadosor Dehesas (extensive silvo-pastoral agro-forestry systems consistingof grasslands with a tree cover of holm oak Quercus rotundifolia orcork oak Quercus suber) and extensive olive groves (Olea europaea) inthe Mediterranean and woodland pastures in Central and NorthernEurope management actions should aim at the maintenance of typicalextensive farming promoting the complexity of the vertical structureof the vegetation Rotational grazing fruit harvesting branch thinning

Table 1Ecological requirements of the five most affected bat species by wind farms in Europe

Species Common pipistrelle Pipistrelluspipistrellus

Soprano pipistrelle Pipistrelluspygmaeus

Nathusius pipistrellePipistrellus nathusii

Leislers bat Nyctalu leisleri Common noctule Nyctalus noctula

Distribution Distributed through Europe up to southernScandinavia and Baltic countries Occurringalso in some parts of Northwest Africa andSouthwest Asia to Central and Eastern AsiaP pipistrellus is one of the most commonspecies in many areas of its distributionrange(1 2 3)

All over Europe from Scotland andsouthern Scandinavia to Iberia andTurkey but records are missing fromsome regions like the northern Balkansand southernmost Italy(1 4)

P nathusii is a migratoryspeciesOccurs in Eastern Central andSouthern Europe(1 3 5 6)

Distributed all over E rope but absentfrom Scandinavia Es nia and NorthernRussia Missing in so hern Italy Sicilyand Crete Ranging to outh-western Asiaand also present in N rth-western Africa(1 5 7)

All over Europe except for IrelandScotland northern Scandinavia andSouthern parts of Greece and ItalyMostly absent from the MediterraneanIslands Ranging to Asia to southernSiberia north Vietnam Myanmar andTaiwan(1 3 5 8)

Foragingpreferentialhabitat

Hunts in several habitats although morecommon in wetlands and urban areas(3 9 10 11)

Hunts in several habitats from forestareas to wetlands agricultural and urbanareas Riparian areas and ponds withtrees or hedgerows in their marginsseem to be preferred especially duringthe breeding season(9 10 11 12 13)

Frequently found in riparianhabitats and wetlands Hunts4ndash15 m above ground onpaths and woodland edgesalso over water(3 9 11 13 14 15)

Forest species uses p eferentiallydeciduous forests bu can also be foundon resinous forests a urban parkshunting above tree t s forest roads andopen areas are also u d to hunt Feedingareas seem to chang ccording toseason age sex and ographical area(11 16 17)

Mostly a forest species hunts in openareas in forest and also frequent inlarge urban parks and gardensfrequently using artificial illuminatedareas as feeding grounds(3 11 13 17 18)

Usual commutingroutes

Linear landscape elements such ashedgerows forest edges and tree lines butalso open spaces(11 19 20 21)

Linear landscape elements such ashedgerows forest edges and tree linesbut also open spaces(11 20 21)

Follows landscape structuresas forest edges hedges roadsor forest aisles but also acrossopen fields(11 14 20)

Little is known but s ms to fly abovetree tops directly an ast to the feedinggrounds reaching up o 40 kmh(11 16 20)

Fast flying species known to travel asfar as 20 km to reach preferred foraginggrounds although individuals inmaternity colonies predominantlyforage within 2 km of the roost(11 20)

Diet Mosquitoes and other small flying insects(17 22 23)

Mostly Diptera(23 24)

Small to medium flyinginsects Mostly Chironomidae(14 22 24)

Lepidoptera Diptera nd Coleoptera(16 17 22 24)

Large sized insects as crickets andColeoptera But also small- tomedium-size prey as TrichopteraDiptera and Lepidoptera(17 22 24 25)

Breeding andhibernation

Uses virtually all kinds of natural andartificial structures as roosts though notcommom in caves Hibernates and breeds incolonies that can reach thousands ofindividuals(3 11 17 20)

Uses virtually all kinds of natural andartificial structures as roosts Hibernatesand breeds in colonies that can reachthousands of individuals(11 20 24)

Roosts in trees bat boxes andsometimes in buildingsHibernates in crevices cliffsbuildings and caves(5 11 15 14 20 26)

Seldom uses anthrop genic structures asshelter choosing pre rably tree cavitiesas roosts Migratory ecies hibernates inrelatively large grou also aggregatingin the roosts during e breeding season(11 16 17 20)

Roosts and hibernates in trees crevicesin rocks buildings and bridges incolonies that can reach thousands ofindividuals during hibernation(3 7 11 17 20 21)

Migration category Most populations are considered sedentarybut there is evidence of long distancemigratory behaviour(3 27)

Evidence of long distance migratorybehaviour(26 27)

Long distance(5 27)

Long distance(5 27)

Long distance(5 27)

References (1) Dietz and von Helversen 2004 (2) Hutson et al 2008a (3) Macdonald and Barrett 1993 (4) Hutson et al 2008b (5) Mitchell-Jones et al 99 (6) Hutson et al 2008c (7) Hutson et al 2008d (8)Csorba et al 2008 (9) Vaughan et al 1997 (10) Glendell and Vaughan 2002 (11) Boye and Dietz 2005 (12) Davidson-Watts and Jones 2005 3) Pocora and Pocora 2011 (14) Flaquer et al 2009 (15)Flaquer et al 2005 (16) Shiel et al 1999 (17) Mayle 1990 (18) Rydell 1992 (19) Verboom and Huitema 1997 (20) BCT 2007 (21) Downs a Racey 2006 (22) Vaughan 1997 (23) Barlow 1997 (24)Blanco 1998 (25) Gloor et al 1995 (26) Gelhaus and Zahn 2010 (27)Popa-Lisseanu and Voigt 2009

14FPeste

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and the creation of small clearings generate potential flight corridors forbat specieswith lowmanoeuvrable flight asN leisleri andN noctula andmedium manoeuvrable flight as P pipistrellus and P nathusii (Obristet al 2011) It will also enable access to food resources located on theground or in herbaceous vegetation which may benefit gleaning batseg genus Myotis and Plecotus (Rainho et al 2010) Additionally theseactions also may represent additional conservation outcomes whilecontributing to the reduction of vegetative surface fuels which is espe-cially relevant in Southern Europe where intensive and highly destruc-tive summer fires are frequent (Guil and Moreno-Opo 2007) Suchactions designed for bat population management that simultaneouslyreduce the risk of fire represent examples of actionsmeeting BBOP rec-ommendations on how to involve stakeholders in mitigation by show-ing how they can benefit with actions dedicated to biodiversitymanagement and conservation

Vegetation homogeneity may result in low availability of food re-sources for some bat species (Dodd et al 2008) So it may be necessaryto create small clearings or agricultural plots while avoiding pesticidetreatments in the surroundings of the wind energy facilities allowingsome diversification within the landscape and creating the conditionsfor greater diversity in food items (Wickramasinghe et al 2004) Thisis particularly evident in Southwest Mediterranean where many windfarms are located at hilltops of mountainous areas and where vast ex-panses of scrubland are common (Chauchard et al 2007 GallegoFernaacutendez et al 2004) In fact the creation of clearings and the subse-quent development of shoots and young plants and vegetation hetero-geneitymay increase both the accessibility (Rainho et al 2010) and theavailability of food items to arthropods that constitute the diet of allEuropean bats

The studies referred above focused mainly on the evaluation of batactivity in different management scenarios This means that there isstill a lack of studies specifically designed to evaluate if those measureshave promising results in bat population increase

Diversification of forest and agriculture monocultures

The diversification of agriculture and forest monocultures is closelyassociated with the measure described above In Europe intensive pro-duction forests are characterised by large areas covered with monocul-tures of the Pinaceae or Eucalyptus spp regarded as areas of poorquality in terms of food and roost availability for bats (Ciechanowski2005 Kusch and Schotte 2007 Rebelo and Rainho 2009 Salvo et al2009) These areas may also present higher susceptibility to fires thannative forests (Moreira et al 2009) so active management for firerestriction is essential including the creation of shaded fuelbreak stripswhere fuel reduction occurs through the cutting and removing of vege-tation (Agee et al 2000 Asociacioacuten Columbares 2009 Guil andMoreno-Opo 2007) and controlled grazing (Ruiz-Mirazo et al 2011)In specific cases prescribed burns may also be considered as theypromote fuel discontinuity and simultaneously maintain areas of vege-tation regeneration representing a significant decrease in fire occur-rence (Montiel and Kraus 2010) this is a high-risk activity and allprecautionary measures should be implemented in conformity withestablished security and legislation rules Prescribed burning andthinning have already been proved to benefit bats inhabiting forestpine stands in North America (Loeb and Waldrop 2008)

Because different species of bats use forests in different conditionsthe creation of spatial heterogeneity is desirable in those areas andcan be attained by the creation of clearings within the forest This willimprove the area as feeding ground and will contribute to the regener-ation of autochthonous understory vegetation (Guldin et al 2007) Inareas where this regeneration is difficult the plantation of autochtho-nous deciduous trees and shrubs should be considered in a long-termmanagement perspective At the same time particularly dense under-story areas may be managed through grazing It should be underlinedthat there is no generic habitat for forest-dwelling bats and different

habitats will favour different species (Guldin et al 2007) so the select-ed measures must consider the species most negatively affected bywind farms in each region

In intensively explored forests clear cuttings in large areas arecommon and this may represent the sudden loss of important foragingand roosting grounds for bats (Borkin et al 2011 Hutson et al 2001Russo et al 2010) Allowing some stands to grow older may attenuatesuch impacts while increasing spatial heterogeneity and the potentialdevelopment of roosting sites in cavities of bulkier older trees (Russoet al 2010) The installation of bat-boxes in younger forests shouldalso be taken into consideration (Ciechanowski 2005) and is specificallyrelevant for species of the genusNyctalus that present significant fatalitynumbers in European wind farms

In areas of intensive agriculture the planting of live fences andnative trees and shrubs provides additional refuge and breeding habitatfor many bat species In systems like Bocage (a habitat typically com-posed of very small parcels of land separated by hedgerows and ditchesfound in western Portugal and France) shrubs and trees alternate withagricultural fields promoting greater floristic diversity which potential-ly supports greater faunal diversity (Guil and Moreno-Opo 2007Haddad et al 2001 Knops et al 1999)

Preservation of existing roosts

The occurrence ofwildlife populations is limited by the availability ofrefuge and successful breeding places As referred above mature treesare prime roosts for forest bats all year long and may be especially rele-vant during the maternity season (Betts 1998 Carter and Feldhamer2005) So the maintenance of old trees and snags prime locationswhile natural shelters for forest bats must also be provided (egRuczyński et al 2010)

Roosts used by bats in the vicinity of wind farms whether of naturalor of anthropogenic origin may be improved or protected to optimiseroosting conditions It is well known that bats that roost in cavesmines and buildings are particularly vulnerable to anthropogenic dis-tress (Agosta 2002 Hutson et al 2001) and tend to abandon roostswhen these are frequently disturbed (Thomas 1995) Indeed severalimportant bat roosts are known to have been lost when caves wereopened to the public as show caves or used for sporting activities toooften (Ransome and Hutson 1999) Restricting human access to roostseither underground crevices or trees may be recommended in somecases For example setting adequately designed gates or fences in theentrances of caves andminesmay reduce human disturbance of impor-tant roosts (Rodrigues 1996 Tuttle 1977) Certainly neglecting thistype of maintenance or distress limitation may lead to the loss of localpopulations (Limpens et al 2000 Ransome and Hutson 1999)

The preservation of old buildings bridges and other anthropogenicstructures that are often used as roosts not only by Pipistrellus speciesbut also by species of the genus Nyctalus among others (eg Amorimet al 2013 BCT 2012) is also a key issue to bat conservation and canassume an important role in the wind farm context Special attentionshould also be given to building restoration and demolishing as distur-bances made in critical times of maternity and hibernation may causesevere mortality in bat populations (Ransome and Hutson 1999Sherwin et al 2000) Monitoring of any changes is important sinceaccess points to roosts used by bats may be blocked as for example bynesting birds or even destroyed by minor modifications (eg BCT2006 Kelleher andMarnell 2006 Mitchell-Jones 2004Waring 2011)

Provision of new roosts

Native mature forests had been showing a significant decrease inEurope in the last three decades (Gibbs and Greig 1997 Jung 2009Luisi et al 1993 Oleksyn and Przybyl 1987 Santos and Martins1993 Siwkcki and Ufnalski 1998 Sonesson and Drobyshev 2010Szepesi 1997 Thomas et al 2002) As a consequence many forest-


dwelling bats have lost their natural roosting habitats Even bat speciesadapted to artificial structures (eg walls and stone houses bridgesfences) had been losing potential roosts as these structures fell into dis-use and were gradually abandoned presenting risk of collapse or wereentirely destroyed

The creation of new artificial sites such as bat-boxes built with long-lasting materials (eg maritime plywood) is then of crucial importancefor European bats and should be implemented in areas where theavailability of natural roosts is low (Flaquer et al 2006) In factCiechanowski (2005) showed that the occupation of artificial roostsby P nathusii and Plecotus aurituswas significantly higher in pinemono-cultures than in deciduous forests because in the latter the availabilityof natural roosts is much higher The design and bat box placement-schemes should respect the ecological requirements and preferencesof the target-species For instance N leisleri and N noctula two ofthe most affected species by wind farms in Europe are quite selectivein their choice of natural roosts preferring high-located cavities(ca 19 m above the ground) in more open surroundings with smallerentrances that are consistently dry and at a safe distance frommartens(Ruczyński and Bogdanowicz 2005) While N noctula seems to prefercavities with wider inside cross section and with only one entranceN leisleri prefers cavities with more than one entrance (Ruczyńskiand Bogdanowicz 2005) N leisleri also seems to prefer roosts withentrances clear from dense vegetation in areas close to water linesand low tree density (Spada et al 2008)

Although bat boxes have been used for replacement of lost refugesor even for the purpose of providing new roosts or even as way offacilitating studies about bat ecology being one of the most adoptedconservation measures few studies have addressed the effectivenessof these structures (Arnett and Hayes 2000 Brittingham andWilliams 2000 Flaquer et al 2006 White 2004) Occupancy rates ofbat boxes seem to vary with factors such as geographic location typeof box and sunlight exposure (Mitchell-Jones 2004) Studies in theUnited States suggest increasing occupancy rates along the yearswhich vary with the placement site of the box trees mdash 20 poles mdash52 and buildingsmdash 64 (Kiser and Kiser 2004) In any case the occu-pation of bat boxes by batsmay take awhile so theymay needmonitor-ing for several years to assess their effectiveness

Creation of ponds

Bats constitute a groupwith unique natural history traits such as theability to fly and echolocate that make them particularly susceptible toenergy and water availability (Adams 2010 Arlettaz et al 2001Barclay 1994 Barclay and Harder 2003) In fact water availability rep-resents a limiting factor to the occurrence and foraging habitat selectionby many bats (Adams and Hayes 2008 Rainho and Palmeirim 20112013) especially during the summer in drier regions of Europe Howev-er global climate change will result in increasing average annualtemperatures and in a significant decrease in precipitation So water-limited environments are expected to increase worldwide (IPCC2008) By creating small ponds water may be available for bats allyear long Ideally to ensure the sustainability of these ponds in thelong term and to avoid the cost of artificially supplying water thesestructures should be placed in areas where rainfall naturally accumu-lates andor take advantage of the proximity of other sources of watersuch as wells and fountains Still in times of severe water scarcityponds could be supplied artificially A few studies provide supportfor the importance of artificial water sources for bats For exampleheliponds created for fire suppression in North American pine standswere considered important for bats to forage and drink (Vindigniet al 2009) a similar trend was found for retention-ponds created inagricultural landscapes (Sirami et al 2013 Stahlschmidt et al 2012)

In addition to providing water for bats and other wildlife ponds arefundamental systems for the emergence and development of someinsect taxa (Cayrou and Ceacutereacuteghino 2005) that can compose the diet of

bats Allowing and promoting the development of autochthonous vege-tation in the margins of the ponds not only provide favourable foragingand shelter habitat for other animal groups (Biggs et al 1994 Oertliet al 2002) but also promote the development of diverse insect assem-blages while simultaneously offering bats and other taxa for thatmatter protection against natural predators (Gee et al 1997) Pondcharacteristics may determine which bat species are privileged Thereis evidence that ponds located in open areas may benefit specieswith low flight manoeuvrability (eg Nyctalus spp and Eptesicus sppCiechanowski 2002) while those integrated with connectivity ele-ments such as treelines may favour species that follow linear landscapefeatures (eg Pipistrellus spp Downs andRacey 2006) A comprehensivecompilation of pond designs is available from the project Million Ponds(wwwfreshwaterhabitatsorgukprojectsmillion-ponds) Hopefullythe information gathered during the project and elsewhere willincrease the scientific knowledge about the most successful designsand benefited species

Selecting suitable conservationmeasures for wind farm offsetcom-pensation programmes

The selection of a specific conservation measure for a given windfarm requires a baseline study This study should contain informationon the most affected species but also on the ecological social and eco-nomical scenarios of the directly affected areas and of the borderingareas Only then it will be possible to adequately identify the mostsuitable measures for the particular residual effect to be compensated

In Table 2we present for each conservationmeasure detailed abovethe most suitable areas for implementation the bat species expected tobenefit the most with special emphasis on those showing higher fatal-ity rates at Europeanwind farms the expected outcomes an estimate ofhow long it may take for a visible offsetcompensation effect and aqualitative estimate on the implementation cost

Bat conservation and wind energy in Europe opportunitieschallenges and constraints

Despite the global financial crisis since 2008 the cumulativeinstalled wind power capacity worldwide had by May 2013 reached282 GW and is still increasing at a rapid pace (WWEA 2013) Europeis among the most dynamic markets with Germany Spain ItalyFrance UK and Portugal at the top of the installed capacity (WWEA2013) This means that the minimisation and compensation of negativeimpacts on European biodiversity associated with wind power infra-structures is crucial to reconciling the production of clean energy withnature and biodiversity conservation and management under thelight of sustainable development

Either directly associated with the offset or compensation of thedirect impacts of wind farm facilities or with the mitigation of otherindirect impacts of anthropogenic origin most of the measuressuggested in this paper entail management actions undertaken inprivate land that may not be and often are not owned by wind farmdevelopers This is surely one of themajor constraints in the applicationof many of the proposed measures the need for partnerships betweenprivate managers where there is little space for the intervention orfacilitation by government authorities with responsibility in the evalua-tion of the process of environmental impact assessment and of follow-upmonitoring programmes Indeed more than half of European forestsare privately owned (Schmithuumlsen and Hirsch 2010) and more than50 of Europes land surface is classified as agricultural land (CorineLand Cover 2013) In this scenario conflicts of interest may arise be-tween human economic activities and nature and biodiversity conser-vation in the same land (Breitenmoser 1998)

The establishment of i) local or regional reserves andor ii) agree-ments with landowners or managers may be essential to defineregimens of sustainable land-uses The definition and implementation

Table 2Offsetcompensatory measures for bat populations affected by residual adverse effects of wind farms including suitable areas for implementation target species expected outcomes estimated time period for the outcomes to show visible effects(short- medium- long-term) and qualitative estimate of the implementation cost of each measure (low medium high)

Offsetcompensatory measure Most suitable area Target bat species Expected outcomes Estimated time for visible effects Associated costs

Management of Autochthonous ForestPreservation of older trees withcavities

Patches and forests of autochthonousspeciesRiparian galleries

Especially N leisleri and N noctula Preservation of existing roostsIncrease in food availability

Short-term Low

Non-removal of standing or fallendead trees

All bat species but especially N leisleriand N noctula

Increase in food availabilityEnhancement of roost formation

Short-long-term Low

Branch thinning Pipistrellus sp Creation of flight corridorsEnhancement of vertical heterogeneityHealthier tree development

Short-term Medium

Maintenance of riparian galleries All bat species Creation of flight corridorsEnhancement of vertical heterogeneityIncrease in food availabilityEnhancement of foraging areas

Short-medium-term Lowmedium

Waterline management Watercourses All species but especially P nathusii Increase in food availabilityEnhancement of foraging areas

Short-medium-term Mediumhigh

Maintenance of the extensiveexploitation of traditionalagro-forestry European ecosystems

MontadosDehesasOlive grovesWoodland pastures

All bat species Creation of flight corridorsEnhancement of vertical heterogeneityReduction of the occurrence of large firesIncrease in food availability


Creating small clearings oragricultural plots

Scrubland areas All bat species Enhancement of spatial heterogeneityEnhancement of foraging areasIncrease in food availability

Short-medium-term Medium

Diversification of Forest and Agriculture MonoculturesCreation of clearings within theforest grazing and uneven stands

Production forests All bat species Enhancement of spatial heterogeneityEnhancement of vertical heterogeneityEnhancement of foraging areasIncrease in food availability


Plantation of live fences and nativetrees and shrubs

Areas of intensive agriculture All bats species especially from genusPipistrellus

Enhancement of spatial heterogeneityEnhancement of foraging areasIncrease in food availabilityIncrease in roost availabilityEnhancement of connectivity elements

Long-term Mediumhigh

Preservation of Existing RoostsMaintenance of old trees and snags Forested areas Especially N leisleri and N noctula Maintenance of roost availability Short-term LowMaintaining roost suitability Caves buildings bridges and other

artificial structures in the vicinity of thewind farm

All bat species Maintenance of roost availability Shortlong-term Lowmedium

Provision of New RoostsInstalling bat-boxes Production forests and agriculture areas All bat species Increase in roost availability Short-medium-term MediumCreation of Ponds Areas of water scarcity All bat species especially P nathusii Increase in water availability

Increase in food availabilityEnhancement of foraging areas


17FPeste

etalEnvironmentalIm

pactAssessm

entReview

51(2015)

10ndash22


of such regimens must contemplate the effective participation of stake-holders and should be well sustained by scientific technical and eventraditional knowledge so as to avoid conflicts that may ultimatelybecome an additional source of threat for wildlife

In the European Union the Birds Directive (79409EEC) and theHabitats Directive (9243EEC) are the two fundamental pillars of na-ture conservation legislation These directives use a twin track approachfor habitat and species protection and allowed the creation of an EU-wide network of protected areas known as Natura 2000 that coversabout 20 of the European territory The Habitats Directive in Article6(4) sets out the legal mechanism to protect Natura 2000 sites fromdamaging plans or projectswhich in theory should only proceed if con-sidered to be of overridingpublic interestwithno available alternativesguaranteeing effective compensatory measures and ensuring that theoverall coherence of the Natura 2000 network is maintained (Dodd2007) However the directive has serious implementation problemspresently as the network-designation process reaches its conclusionthe challenge lies in achieving effective management in each site(Pullin et al 2009) because there is still a large gap between the desig-nation of the Natura 2000 sites and the effective implementation of con-servationmeasures in these sites (eg Apostolopoulou and Pantis 2009)

Additionally several important areas for wildlife are still lackingany kind of protection policymechanism (Arauacutejo et al 2007Dimitrakopoulos et al 2004 Maiorano et al 2007 Saacutenchez-Fernaacutendezet al 2008) Because these areas potentially represent good foragingand roosting spots for bats they should be safeguarded especiallyduring the critical periods of the life-cycle of bats Despite theirimportance due to small size or spatial discontinuity many ofthese areas do not fulfil the necessary requirements to be estab-lished as formal protected areas by national or European legislationNevertheless they could benefit from the creation of local or regionalconservation regimens established by local governments or non-governmental organisations When managed properly public accessto these areas may be critically important to gaining public supportfor the classification of such local and regional conservation sites(Bauer et al 2009) Moreover public access together with environ-mental education and eco-tourism schemes may promote publicperception of and support for the conservation of biodiversity(Blangy and Mehta 2006 Eagles et al 2002 Kiss 2004)

Alternatively or in complement the establishment of agreementswith landowners andor managers restricting the timing of potentiallydisturbing activities may reduce or even completely circumvent batdisturbance during critical periods Still some agriculture and forestry ac-tivities like cork removal honey extraction crop harvest among othershave temporal specificities so an agreement between conservation ob-jectives and the requirements of the production systemmust be pursued

Therefore other non-ecological factors determining the practicalfeasibility of successful offsetting should be analysed under social cul-tural technical legal and financial headings (BBOP 2012c) In fact theproposed offsetcompensatory measures should take into account thesocial dimension and attempt to accomplish benefits for local communi-ties and owners in order to engage stakeholders in the implementationof the offsetcompensation actions Often the involvement of differentindividuals groups andor associations may be necessary to ensurebiodiversity offset fairness the success of the offsetcompensationprogrammes may also be dependent on reimbursements to indigenouspeople local communities and other directly affected stakeholders(BBOP 2009b)

Environmental education and raising awareness of communities andlocal stakeholders is a key issue in wildlife conservation in areas withhuman occupation In fact successful wildlife management is oftendependent on the level of engagement of the people living in or nearbyconservation areas Participative sessions should be promoted for thesecommunities especially involving land managers hunters loggerseither individually or in the form of associations and NGOs Freeworkshops on themes such as gardening management organic farming

andwaste disposal are desirable as these activities are directly related tothe creation of suitable conditions for native plants and the associated in-sect fauna (Asociacioacuten Columbares 2009 Guil and Moreno-Opo 2007)

In the European Union the potential conflict between humaneconomic activities and biodiversity conservation may also be reducedby the effective implementation of agro-environmental schemes fore-seen by the EU rural development policy These measures are indirectoffsets ie agreements with individuals to cede the right to convertland cover for profit (Quintero and Mathur 2011) More specificallythese schemes foresee payments to farmers who voluntarily sub-scribe to commitments related to environmental protection (httpeceuropaeu) Agro-environmental measures are compulsory for themember-states (Council Regulation on Rural Development 16982005EC) but there have been significant cuts in the budget for rural develop-ment in many European countries which have to co-fund those agro-environmental schemes mdash thus creating an additional constraint tothe application of many of the proposed measures

The European landscape entails an additionalmanagement problemas a significant percentage of privately owned rural areas are in the formof small-scale household land parcels and farms (Bowler 1985 Riddelland Rembold 2000 van Dijk 2003 2007) So even if a farmer andormanager comply with some kind of environmental scheme aimed atbat conservation or other component of biodiversity this does not nec-essarilymean that the neighbouring landwill follow In some cases thismay result in a very small area dedicated to the implementation of thecompensatory measures which is frequently ineffective in attainingthe conservation objectives proposed

According to the Business and Biodiversity Offsets Programme(BBOP 2012b) offsetscompensatory programmes that achieve lsquonetgainrsquo through additional conservation actions could contribute to batconservation Additionally a fraction of the revenues generated by pro-jects with negative impacts may be dedicated to co-fund agro-environmental schemes (Quintero and Mathur 2011) For example inPortugal this kind of financing towards conservation is already consid-ered through the creation of offset funds for nature and biodiversityconservation that result not only from the state budget but also fromen-vironmental compensation revenues of major private infrastructureprojects Another example comes from the USA where a kind of recla-mation fund paid by the promoters of hydroelectric and oil infrastruc-tures is in place to be used whenever damages to the environmentand biodiversity occur (Cole 2011)

Another important aspect of offset and compensatory programmesis that they should be based on adaptive management incorporatingmonitoring and evaluations with the objective of securing outcomesthat last at least as long as the project associated impacts and preferablyin perpetuity (Principle 8 BBOP 2012b) Based on that mandatoryprogrammes on i) bat mortality monitoring at wind farms ii) the as-sessment of the offsetcompensatory measure implementation and iii)the monitoring of effectiveness and success of the implemented mea-sures should be the rule in European countries (Baber 2012 BBOP2012b Quintero and Mathur 2011I) In fact even if a continued or pe-riodic evaluation of the effectiveness of the implemented compensatorymeasures is legally foreseen in some European countries ndash though oftenonly for specific projects and if included in the infrastructure permitconditions ndash no country seems to be actually implementing this obliga-tion (personal information obtained through inquiries done to the focalpoints of the EUROBATS Intersessional Working Group on Bats andWind Farms) This evaluation of the implementation of the offsetcom-pensatory measures especially those based on the improvement of theecological conditions for bats is essential to effectively assess theirbenefit to bat conservation

Concluding remarks

Our review indicates that in theory the residual impacts thatremain after avoidance and minimisation may potentially be offset or


at least compensated through the implementation of conservationmeasures that improve the ecological conditions for the bat speciesmost affected by wind farms The majority of the proposed measuresfocus especially on the enhancement of habitat heterogeneity at localand landscape scales For instance the maintenance of native forestsand the management of production forest should promote an increasein the availability of roosting and feeding grounds including theimprovement of foraging microhabitats

The creation of natural reserves the establishment of agreementsand partnerships with local owners and the development of environ-mental education sessions for local communities may also contributetowards the achievement of no net loss and in some cases a net gainfor bat populations

To our knowledge the measures we propose here have not beenpreviously used in offsetcompensation programmes for bat popula-tions affected by wind farm facilities and their efficiency was not thor-oughly assessed This is certainly the next step in this area of researchAdditionally the application of the measures we suggest should beconsistently adapted to each wind farm considering all the localspecificities ndash in particular the local bat assemblage and landscapeconfiguration ndash ensuring a monitoring scheme capable of detectingundesirable unexpected effects

Based on our review we found important knowledge gaps ini) methodologies to accurately assess bat fatalities atwind farms causesand fatality rates ii) local and regional specificities concerning themostaffected species and on the ecology of those species iii) the outcomesof management schemes specifically dedicated to bat populations thatcan be used as a basis to develop additional and complementarymeasures to those here presented

Role of the funding source

The work developed in this manuscript is part of the projectRampD project CENTRO-07-0202-FEDER-011541 Wind amp Biodiversityco-financed by the European Regional Development Fund (FEDER)under the Regional Operational Programme of Center (Mais Centro)This work was co-supported by European Funds through COMPETEand by National Funds through the Portuguese Science Foundation(FCT) within project PEst-CMARLA00172013

Acknowledgements

We would like to thank the focal points of the EUROBATSIntersessional Working Group on Bats and Wind Farms for theirkind and quick response to the inquiry on the implementation ofcompensatory measures in European countries

References

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Adams RA Hayes MA Water availability and successful lactation by bats as related toclimate change in arid regions of western North America J Anim Ecol 2008771115ndash21 httpdxdoiorg101111j1365-2656200801447x

Agee J Bahro B FinneyM Omi P Sapsis D Skinner C et al The use of shaded fuelbreaks inlandscape fire management For Ecol Manag 200012755ndash66

Agosta SJ Habitat use diet and roost selection by the big brown bat (Eptesicus fuscus) inNorth America a case for conserving an abundant species Mamm Rev 200232(3)179ndash98 httpdxdoiorg101046j1365-2907200200103x

Amorim F Rebelo H Rodrigues L Factors influencing bat activity and mortality at a windfarm in the Mediterranean Region Acta Chiropterol 201214(2)439ndash57 httpdxdoiorg103161150811012X661756

Amorim F Alves P Rebelo H Bridges over the troubled conservation of Iberian batsBarbastella 20136(1)3ndash12

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Arlettaz R Christe P Lugon A Perrin N Vogel P Food availability dictates the timing ofparturition in insectivorous mouse-eared bats Oikos 200195(1)105ndash11 httpdxdoiorg101034j1600-07062001950112x

Arnett E Hayes J Bat use of roosting boxes installed under flat-bottom bridges in westernOregon Wildl Soc Bull 200028(4)890ndash4

Arnett EB Brown WK Erickson WP Fiedler JK Hamilton BL Henry TH et al Patterns ofbat fatalities at wind energy facilities in North America J Wildl Manag 200872(1)61ndash78 httpdxdoiorg1021932007-221

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Ciechanowski M Utilization of artificial shelters by bats (Chiroptera) in three differenttypes of forest Folia Zool 20055431ndash7

Cole SGWind power compensation is not for the birds an opinion from an environmentaleconomist Restor Ecol 201119(2)147ndash53 httpdxdoiorg101111j1526-100X201000771x

Collins J Jones G Differences in bat activity in relation to bat detector height implicationsfor bat surveys at proposed windfarm sites Acta Chiropterol 200911(2)343ndash50httpdxdoiorg103161150811009X485576

Corine Land Cover 2013 httpwwweeaeuropaeudata-and-mapsdatacorine-land-cover-2006-raster-2 Acessed on March 2013

Crampton LH Barclay RMR Selection of roosting and foraging habitat stands by bats inAspen different-aged mixedwood stand Conserv Biol 199812(6)1347ndash58

Cryan P Barclay R Causes of bat fatalities at wind turbines hypotheses and predictions JMammal 200990(6)1330ndash40

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Darbi M Ohlenburg H Herberg A Wende W Skambracks D Herbert M Internationalapproaches to compensation for impacts on biological diversity Final Report 2009p 1ndash184

Davidson-Watts I Jones G Differences in foraging behaviour between Pipistrelluspipistrellus (Schreber 1774) and Pipistrellus pygmaeus (Leach 1825) J Zool 2005268(1)55ndash62 httpdxdoiorg101111j1469-7998200500016x

Dietz M Pir JB Distribution and habitat selection ofMyotis bechsteinii in Luxembourgimplications for forest management and conservation Folia Zool 200958(3)327ndash40

Dietz C von Helversen O Illustrated identification key to the bats of Europe Electronicpublication version 10 Released 15122004 Tuebingen amp Erlangen (Germany)2004

Dimitrakopoulos PG Memtsas D Troumbis AY Questioning the effectiveness of theNatura 2000 Special Areas of Conservation strategy the case of Crete Glob EcolBiogeogr 200413199ndash207 httpdxdoiorg101111j1466-822X200400086x

Dodd AM EU Habitats Directive and habitat compensation mdash spatial planning in Englandand implementing habitat compensation under Article 6 (4) of the Habitats Directive[dissertation] Oxford Brookes University 2007

Dodd LE Lacki MJ Rieske LK Variation in moth occurrence and implications for foraginghabitat of Ozark big-eared bats For Ecol Manag 20082553866ndash72 httpdxdoiorg101016jforeco200803034

Downs NC Racey PA The use by bats of habitat features in mixed farmland in ScotlandActa Chiropterol 20068(1)169ndash85 httpdxdoiorg1031611733-5329(2006)8[169TUBBOH]20CO2

Eagles P McCool S Haynes C Sustainable tourism in protected areas Guidelines forplanning and management Gland and Cambridge IUCN 2002 [183 pp]

EC EU guidance on wind energy development in accordance with the EU naturelegislation European Commission Luxembourg European Commission 2010httpdxdoiorg10277998894 [116 p]

Entwistle A Harris S Hutson A Racey P Walsh A Gibson S et al Habitat management forbats a guide for land managers land owners and their advisors Joint NatureConservation Committee UK 2001

Eurobats Report of the IWG on wind turbines and bat populations 17th Meeting of theAdvisory Committee Dublin 2012 [33 p]

Eurobats Progress report of the IWG onwind turbines and bat populations 18th Meetingof the Advisory Committee Sofia 2013 [30 p]

EWEA Thirty years growing together annual report 2011 The European Wind EnergyAssociation 2012 [47 p]

Flaquer C Ruiz-Jarillo R Torre I Arrizabalaga A First resident population of Pipistrellusnathusii (Keyserling and Blasius 1839) in the Iberian Peninsula Acta Chiropterol20057(1)183ndash8

Flaquer C Torre I Ruiz-Jarillo R The value of bat-boxes in the conservation of Pipistrelluspygmaeus in wetland rice paddies Biol Conserv 2006128223ndash30 httpdxdoiorg101016jbiocon200509030

Flaquer C Puig-Montserrat X Goiti U Vidal F Curcoacute A Russo D Habitat selection inNathusius pipistrelle (Pipistrellus nathusi) the importance of wetlands ActaChiropterol 200911(1)149ndash55 httpdxdoiorg103161150811009X465767

Fleming TH Eby P Ecology of bat migration In Kunz H Fenton MB editors Bat ecologyChicago The University of Chicago Press 2003 p 156ndash208

FordWMenzel M Rodrigue J Menzel J Johnson J Relating bat species presence to simplehabitat measures in a central Appalachian forest Biol Conserv 2005126528ndash39httpdxdoiorg101016jbiocon200507003

Gallego Fernaacutendez JB Mora MRG Novo FG Vegetation dynamics of Mediterraneanshrublands in former cultural landscape at Grazalema Mountains south SpainPlant Ecol 200417283ndash94

Gee JHR Smith BD Lee KM The ecological basis of freshwater pond management forbiodiversity Aquat Conserv Mar Freshwat Ecosyst 1997791ndash104

GelhausM Zahn A Roosting ecology phenology and foraging habitats of a nursery colonyof Pipistrellus nathusii in the southwestern part of its reproduction range Vespertilio201013ndash1493ndash102

Gibbs JN Greig BJW Biotic and abiotic factors affecting the dying back of pedunculate oakQuercus robur L Forestry 199770(4)399ndash406

Glendell M Vaughan N Foraging activity of bats in historic landscape parks in relation tohabitat composition and park management Anim Conserv 20025(4)309ndash16 httpdxdoiorg101017S1367943002004067

Gloor S Stutz HB Ziswiler V Nutritional habits of the noctule bat Nyctalus noctula(Shreber 1774) in Switzerland Myotis 199532ndash33231ndash42

Grodsky SM Behr MJ Gendler A Drake D Dieterle BD Rudd RJ et al Investigating thecauses of death for wind turbine-associated bat fatalities J Mammal 201192(5)917ndash25 httpdxdoiorg10164410-MAMM-A-4041

Guil F Moreno-Opo R Cataacutelogo de buenas praacutecticas para a gestioacuten del haacutebitat en RedNatura 2000 Bosque Y matorral mediterraacuteneos Una propuesta de actuacionesfinanciables en Red Natura 2000 Madrid Obra Social Caja Madrid-Fundacioacuten CBD-Haacutebitat 2007 [268 p Spanish]

Guldin JM EmminghamWH Carter SA Saugey DA Silvicultural practices andmanagementof habitat for bats In Lacki MJ Hayes JP Kurta A editors Bats in forests conservationand management Baltimore The Johns Hopkins University Press 2007 p 177ndash205

Haddad NM Tilman D Haarstad J Ritchie M Knops JMH Contrasting effects of plantrichness and composition on insect communities a field experiment Am Nat 2001158(1)17ndash35

Hayes N Morrison-Saunders A Effectiveness of environmental offsets in environmentalimpact assessment practitioner perspectives from Western Australia Impact AssessProj Apprais 200725(3)209ndash18 httpdxdoiorg103152146155107X227126

Hein C Gruver J Arnett E Relating pre-construction bat activity and post-construction batfatality to predict risk at wind energy facilities a synthesis A report submitted to theNational Renewable Energy Laboratory Austin (Tx) Bat Conservation International2013 [Available from httpmhkpnnlgovsitesdefaultfilespublicationsPre- Post-construction Synthesis_FINAL REPORTpdf]

Horn JW Arnett EB Jensen M Kunz TH Testing the effectiveness of an experimentalacoustic bat deterrent at the Maple Ridge wind farm The Bats and Wind EnergyCooperative and Bat Conservation International Austin (Tx) 2008 [Jun]

Hutson A Mickleburgh S Racey P Microchiropteran bats global status survey andconservation action plan IUCNSSC C Gland and Cambridge IUCN 2001 258 p

Hutson AM Spitzenberger F Aulagnier S Coroiu I Karataş A Juste J et al Pipistrelluspipistrellus The IUCN red list of threatened species 2008a [Version 20122 bwwwiucnredlistorgN Downloaded on 05 March 2013]

Hutson AM Spitzenberger F Aulagnier S Coroiu I Karataş A Juste J et al Pipistrelluspygmaeus The IUCN red list of threatened species 2008b [Version 20122 bwwwiucnredlistorgN Downloaded on 05 March 2013]

Hutson AM Spitzenberger F Juste J Aulagnier S Palmeirim J Karataş A et al Pipistrellusnathusii The IUCN red list of threatened species 2008c [Version 20142 bwwwiucnredlistorgN Downloaded on 22 October 2014]

Hutson AM Spitzenberger F Aulagnier S Juste J Karataş A Palmeirim J et al Nyctalusleisleri The IUCN red list of threatened species 2008d [Version 20122 bwwwiucnredlistorgN Downloaded on 05 March 2013]

IPCC Climate change and water resources in systems and sectors In Bates BC KundzewiczZWJ Wu S Palutiko P editors Climate change and water Technical paper of the Inter-governmental Panel on Climate ChangeGeneva IPCC Secretariat 2008 [53-76 p]

Jay S Jones C Slinn P Wood C Environmental impact assessment retrospect andprospect Environ Impact Assess Rev 200727(4)287ndash300 httpdxdoiorg101016jeiar200612001

Johnson G Erickson WP Strickland MD Shepherd M Shepherd D Mortality of bats at alarge-scale wind power development at Buffalo Ridge Minn Am Midl Nat 2003150(307)332ndash42 httpdxdoiorg1016740003-0031(2003)150[0332MOBAAL]20CO2

Johnson JB Ford WM Rodrigue JL Edwards JW Effects of acoustic deterrents on foragingbats Department of Agriculture Forest Service Northern Research Station Res NoteNRS-129 2012 [5 p]

Jung T Beech decline in Central Europe driven by the interaction between Phytophthorainfections and climatic extremes For Pathol 200939(2)73ndash94 httpdxdoiorg101111j1439-0329200800566x

Kelleher C Marnell F Bat mitigation guidelines for Ireland Dublin Ireland National Parksand Wildlife Service Department of Environment Heritage and Local Government2006

Kerns J EricksonWP Arnett EB Bat and bird fatality at wind energy facilities in Pennsylvaniaand West Virginia In Arnett EB editor Relationships between bats and wind turbinesin Pennsylvania and West Virginia an assessment of fatality search protocolspatterns of fatality and behavioural interactions with wind turbines Austin (Tx)Bat Conservation International 2005 p 24ndash95

Kiesecker JM Copeland H Pocewicz A McKenney B Development by design blendinglandscape-level planning with the mitigation hierarchy Front Ecol Environ 20108(5)261ndash6 httpdxdoiorg101890090005

Kiser M Kiser S A decade of bat house discovery Bat House Res 200412(1)1ndash12Kiss A Is community-based ecotourism a good use of biodiversity conservation funds

Trends Ecol Evol 200419(5)232ndash7 httpdxdoiorg101016jtree200403010Knops JMH Tilman D Haddad NM Naeem S Charles EM Haarstad J et al Effects of plant

species richness on invasion dynamics disease outbreaks insect abundances anddiversity Ecol Lett 19992286ndash93


Kull CA Shackleton CM Cunningham PJ et al Adoption use and perception of Australianacacias around the world Divers Distrib 201117(5)822ndash36 httpdxdoiorg101111j1472-4642201100783x

Kunz TH Lumsden LF Ecology of cavity and foliage roosting bats In Kunz TH Fenton MBeditors Bat ecology Chicago The University of Chicago Press 2003 p 3ndash89

Kusch J Schotte F Effects of fine-scale foraging habitat selection on bat communitystructure and diversity in a temperate low mountain range forest Folia Zool 200756(3)263ndash76

Ledec G Rapp K Aiello R Greening the wind environmental and social considerations forwind power development World Bank Studies Washington 2011

Leung DYC Yang Y Wind energy development and its environmental impact a reviewRenew Sustain Energy Rev 201216(1)1031ndash9 httpdxdoiorg101016jrser201109024

Limpens HJGA Lina P Hutson AM Action plan for the conservation of the pond bats(Myotis Dasycneme) in Europe Strasbourg Council of Europe Publishing 2000

Loeb SC OKeefe JM Habitat use by forest bats in South Carolina in relation to local standand landscape characteristics J Wildl Manag 200670(5)1210ndash8

Loeb SC Waldrop TA Bat activity in relation to fire and fire surrogate treatments insouthern pine stands For Ecol Manag 20082553185ndash92 httpdxdoiorg101016jforeco200710060

Luisi N Lerario P Vannini A Recent advances in studies on oak decline Proceedings of anInternational Congress Bari Italy Unione Fitopatologica 1993

Macdonald DW Barrett P Collins field guide to the mammals of Britain and EuropeLondon UK HarperCollinsPublishers 1993 312 p

Maiorano L Falcucci A Garton EO Boitani L Contribution of the Natura 2000 network tobiodiversity conservation in Italy Conserv Biol 200721(6)1433ndash44 httpdxdoiorg101111j1523-1739200700831x

Marchante H Marchante E Freitas H Plantas invasoras em Portugal - Fichas paraidentificaccedilatildeo e controlo Coimbra Portugal 2005 [Portuguese]

Marshall R Application of mitigation and its resolution within environmental impactassessment an industrial perspective Impact Assess Proj Apprais 200119(3)195ndash204 httpdxdoiorg103152147154601781767050

Mayle B A biological basis for bat conservation in British woodlandsmdasha review MammRev 199020(4)159ndash95

McKenney BA Kiesecker JM Policy development for biodiversity offsets a review of off-set frameworks Environmental Management 201045165ndash76

Meschede A Wolfram G Boye P Bats in forests mdash information and recomendations forforest managers Landschaft als Leb 4 2001 [18 p]

Mitchell-Jones A Conserving and creating bat roosts In Mitchell-jones A Mcleish Aeditors Bat workers manual JNCC 2004 p 111ndash33

Mitchell-Jones AJ Amori G Bogdanowicz W Krystufek B Reijnders PJH Spitzenberger Fet al The atlas of European mammals London UK Academic Press 1999

Montiel C Kraus D Best practices of fire use prescribed burning and suppression fireprogrammes in selected case-study regions in Europe European Forest InstituteJoensuu Finland 2010

Moreira F Vaz P Catry F Silva JS Regional variations in wildfire susceptibility ofland-cover types in Portugal implications for landscape management to minimizefire hazard Int J Wildl Fire 200918(5)563ndash74

Nicholls B Racey PA Bats avoid radar installations could electromagnetic fields deterbats from colliding with wind turbines PLoS ONE 20072(3)e297 httpdxdoiorg101371journalpone0000297

Nicholls B Racey PA The aversive effect of electromagnetic radiation on foraging bats apossible means of discouraging bats from approaching wind turbines PLoS ONE20094(7)e6246 httpdxdoiorg101371journalpone0006246

Obrist MK Rathey E Bontadina F Martinoli A Conedera M Christe P et al Response ofbat species to sylvo-pastoral abandonment For Ecol Manag 2011261789ndash98httpdxdoiorg101016jforeco201012010

Oertli B Joye DA Castella E Juge R Cambin D Lachavanne J-B Does size matter Therelationship between pond area and biodiversity Biol Conserv 2002104(1)59ndash70httpdxdoiorg101016S0006-3207(01)00154-9

Oleksyn J Przybyl K Oak decline in the Soviet Unionmdashscale and hypotheses Eur J ForPathol 198717321ndash36 httpdxdoiorg101111j1439-03291987tb01325x

Peng RK Sutton SL Fletcher CR Spatial and temporal distribution patterns of flyingDiptera J Zool 1992228(2)329ndash40 httpdxdoiorg101111j1469-79981992tb04612x

Petillon J Ysnel F Canard A Lefeuvre J Impact of an invasive plant (Elymus athericus) onthe conservation value of tidal salt marshes in western France and implications formanagement responses of spider populations Biol Conserv 2005126103ndash17httpdxdoiorg101016jbiocon200505003

Plank M Fiedler K Reiter G Use of forest strata by bats in temperate forests J Zool 2012286(2)154ndash62 httpdxdoiorg101111j1469-7998201100859x

Pocora I Pocora V The use by bats (Chiroptera Vespertilionidae) of various habitattypes in Moldova and the Danube delta (Romania) Trav Mus Natl Hist NatGrigore Antipa 201154(1)223ndash42 httpdxdoiorg102478v10191-011-0014-2

Popa-Lisseanu A Voigt C Bats on the move J Mammal 200990(6)1283ndash9PricewaterhouseCoopers Biodiversity offsets and the mitigation hierarchy a review of

current application in the banking sector London PricewaterhouseCoopers Businessand Biodiversity Offsets Programme and UN Environment Programme FinanceInitiative 2010

Pullin AS Baacuteldi A Can OE Dieterich M Kati V Livoreil B et al Conservation focus onEurope major conservation policy issues that need to be informed by conservationscience Conserv Biol 200923(4)818ndash24 httpdxdoiorg101111j1523-1739200901283x

Quintero JD Mathur A Biodiversity offsets and infrastructure Conserv Biol 201125(6)1121ndash3 httpdxdoiorg101111j1523-1739201101769x

Rainho A Summer foraging habitats of bats in a Mediterranean region of the IberianPeninsula Acta Chiropterol 20079(1)171ndash81

Rainho A Palmeirim JM The importance of distance to resources in the spatial modellingof bat foraging habitat PLoS ONE 20116(4)e19227 httpdxdoiorg101371jour-nalpone0019227

Rainho A Palmeirim JM Prioritizing conservation areas around multispecies bat coloniesusing spatial modeling Anim Conserv 201316(4)438ndash48 httpdxdoiorg101111acv12013

Rainho A Augusto AM Palmeirim JM Influence of vegetation clutter on the capacity ofground foraging bats to capture prey J Appl Ecol 201047(4)850ndash8 httpdxdoiorg101111j1365-2664201001820x

Rajvanshi A Mitigation and compensation in environmental assessment In Thomas BFGazzola P JHa-Thakur U Belčaacutekovaacute I AScheMann R editors Environmentalassessment lecturers handbook 2008 p 167ndash99

Ransome RD Hutson AM Action plan for conservation of the greater horseshoe bat(Rhinolophus ferrumequinum) in Europe 1999

Rebelo H Rainho A Bat conservation and large dams spatial changes in habitat usecaused by Europes largest reservoir Endanger Species Res 2009861ndash8 httpdxdoiorg103354esr00100

Richardson DM Rejmaacutenek M Trees and shrubs as invasive alien species mdash a globalreview Divers Distrib 201117788ndash809 httpdxdoiorg101111j1472-4642201100782x

Richardson DM Holmes PM Esler KJ Galatowitsch SM Stromberg JC Kirkman SP et alRiparian vegetation degradation alien plant invasions and restoration prospectsDivers Distrib 2007126ndash139 httpdxdoiorg101111j1472-4642200600314x

Riddell J Rembold F Social and economic impact of land fragmentation on rural society inselected EU accession countries Proceedings of the UDMS 2000 p 13ndash20

Rodrigues L Utilizaccedilatildeo de grades para proteccedilatildeo de abrigos de morcegos caverniacutecolas[dissertation] Lisbon FCUL 1996 81 p

Rodrigues L Bach L Dubourg-SavageMGoodwin J HarbuschC Guidelines for considerationof bats in wind farm projects Bonn Germany UNEPEUROBATS 2008 51 p

Rollins KE Meyerholz DK Johnson GD Capparella AP Loew SS A forensic investigationinto the etiology of bat mortality at a wind farm barotrauma or traumatic injuryVet Pathol 201249(2)362ndash71 httpdxdoiorg1011770300985812436745

Ruczyński I Bogdanowicz W Roost cavity selection by Nyctalus noctula and N leisleri(Vespertilionidae Chiroptera) in Białowieża primeval forest Eastern Poland JMammal 200586(5)921ndash30

Ruczyński I Nicholls B MacLeod CD Racey PA Selection of roosting habitats by Nyctalusnoctula and Nyctalus leisleri in Białowieża Forestmdashadaptive response to forestmanagement For Ecol Manag 20102591633ndash41 httpdxdoiorg101016jforeco201001041

Ruiz-Mirazo J Robles AB Gonzaacutelez-Rebollar JL Two-year evaluation of fuelbreaks grazedby livestock in the wildfire prevention program in Andalusia (Spain) Agric EcosystEnviron 2011141(1ndash2)13ndash22 httpdxdoiorg101016jagee201102002

Russ JM Montgomery WI Habitat associations of bats in Northern Ireland implicationsfor conservation Biol Conserv 200210849ndash58

Russo D Jones G Use of foraging habitats by bats in a Mediterranean area determined byacoustic surveys conservation implications Ecography (Cop) 200326197ndash209

Russo D Cistrone L Jones G Mazzoleni S Roost selection by barbastelle bats (Barbastellabarbastellus Chiroptera Vespertilionidae) in beech woodlands of central Italyconsequences for conservation Biol Conserv 2004117(1)73ndash81 httpdxdoiorg101016S0006-3207(03)00266-0

Russo D Cistrone L Garonna AP Jones G Reconsidering the importance of harvestedforests for the conservation of tree-dwelling bats Biodivers Conserv 201019(9)2501ndash15 httpdxdoiorg101007s10531-010-9856-3

Rydell J The exploitation of insects around street lamps by bats in Sweden FunctionalEcology 19926(6)744ndash55

Rydell J Bach L Dubourg-Savage M-J Green M Rodrigues L Hedenstroumlm A Bat mortalityat wind turbines in northwestern Europe Acta Chiropterol 201012(2)261ndash74httpdxdoiorg103161150811010X537846

Salvo I Russo DA Saragrave MA Habitat preferences of bats in a rural area of Sicily determinedby acoustic surveys Hystrix It J Mamm 200920(2)137ndash46 httpdxdoiorg104404hystrix-202-4444

Saacutenchez-Fernaacutendez D Bilton DT Abellaacuten P Ribera I Velasco J Millaacuten A Are the endemicwater beetles of the Iberian Peninsula and the Balearic Islands effectively protectedBiol Conserv 20081411612ndash27 httpdxdoiorg101016jbiocon200804005

Santos MNDS Martins AMM Cork oak decline Notes regarding damage and incidence ofHypoxylon mediterraneum In Luisi N Lerario P Vannini A editors Recent advancesin studies on oak decline Bari Italy Universita 1993 p 115ndash21

Schmithuumlsen F Hirsch F Private forest ownership in Europe Geneva United Nations2010

Sherwin R Stricklan D Rogers D Roosting affinities of Townsends big-eared bat(Corynorhinus townsendii) in northern Utah J Mammal 200081(4)939ndash47

Shiel C Shiel R Fairley J Seasonal changes in the foraging behaviour of Leislers bats(Nyctalus leisleri) in Ireland as revealed by radio‐telemetry J Zool 1999249347ndash58 httpdxdoiorg101111j1469-79981999tb00770x

Sirami C Jacobs DS Cumming GS Artificial wetlands and surrounding habitats provideimportant foraging habitat for bats in agricultural landscapes in the Western CapeS Afr Biol Conserv 201316430ndash8 httpdxdoiorg101016jbiocon201304017

Siwkcki R Ufnalski K Review of oak stand decline with special reference to the role ofdrought in Poland Eur J For Pathol 19982899ndash112 httpdxdoiorg101111j1439-03291998tb01171x

Sonesson K Drobyshev I Recent advances on oak decline in southern Sweden Ecol Bull201053197ndash207

Spada M Szentkuti S Zambelli N Mattei-Roesli M Moretti M Bontadina F et al Roostselection by non-breeding Leislers bats (Nyctalus leisleri) in montane woodlands


implications for habitat management Acta Chiropterol 200810(1)81ndash8 httpdxdoiorg103161150811008X331117

Spanjer G Responses of the big brown bat Eptesicus fuscus to a proposed acousticdeterrent device in a lab setting A report submitted to the Bats and Wind EnergyCooperative and the Maryland Department of Natural Resources Austin (Tx) BatConservation International 2006 p 1ndash12

Stahlschmidt P Paumltzold A Ressl L Schulz R Bruumlhl CA Constructed wetlands support batsin agricultural landscapes Basic Appl Ecol 201213(2)196ndash203 httpdxdoiorg101016jbaae201202001

Szepesi A Forest health status in Hungary Environ Pollut 199798(3)393ndash8Szewczak JM Arnett E Preliminary field test results of an acoustic deterrent with the

potential to reduce bat mortality from wind turbines Austin (Tx) Bat ConservationInternational 2006a 7 p

Szewczak J Arnett E Ultrasound emissions fromwind turbines as a potential attractant tobats a preliminary investigation An investigative report submitted to the Bats andWind Energy Cooperative Austin (Tx) Bat Conservation International 2006bp 1ndash11

Szewczak J Arnett E Field test results of a potential acoustic deterrent to reduce batmortality from wind turbines Bat Conservation International Austin (Tx) 2007[Available from httpbatsandwindorgpdf2007DeterrentPondStudyFinalpdf]

Ten Kate K von Hase A Boucher J Cassin J Victurine R Opportunities for environmentalfunds in compensation and offset schemes RedLAC capacity building project forenvironmental funds RedLAC Rio de Janeiro RedLAC 2011

Thomas D Hibernating bats are sensitive to nontactile human disturbance J Mammal199576(3)940ndash6 httpdxdoiorg1023071382764

Thomas FM Blank R Hartmann G Abiotic and biotic factors and their interactions ascauses of oak decline in Central Europe For Pathol 200232(4ndash5)277ndash307 httpdxdoiorg101046j1439-0329200200291x

Tuttle MD Gating as a means of protecting cave dwelling bats In Aley T Rhodes Deditors National Cave Management Symposium ProceedingsSpeleobooks 1977p 77ndash82

Van Dijk T Scenarios of Central European land fragmentation Land Use Policy 200320149ndash58 httpdxdoiorg101016S0264-8377(02)00082-0

Van Dijk T Complications for traditional land consolidation in Central Europe Geoforum200738505ndash11 httpdxdoiorg101016jgeoforum200611010

Vaughan N The diets of British bats (Chiroptera) Mamm Rev 199727(2)77ndash94 httpdxdoiorg101111j1365-29071997tb00373x

Vaughan N Jones G Harris S Habitat use by bats by means of a broad-band acousticmethod J Appl Ecol 199734716ndash30

Verboom B Huitema H The importance of linear landscape elements for the pipistrellePipistrellus pipistrellus and the serotine bat Eptesicus serotinus Landsc Ecol 199712(2)117ndash25

Vindigni MA Morris AD Miller DA Kalcounis-Rueppell MC Use of modified watersources by bats in a managed pine landscape For Ecol Manag 20092582056ndash61httpdxdoiorg101016jforeco200907058

Voigt CC Popa-Lisseanu AG Niermann I Kramer-Schadt S The catchment area of windfarms for European bats a plea for international regulations Biol Conserv 201215380ndash6 httpdxdoiorg101016jbiocon201204027

Walters CL Freeman R Collen A Dietz C Fenton BM Jones G et al A continental-scaletool for acoustic identification of European bats J Appl Ecol 201249(5)1064ndash74httpdxdoiorg101111j1365-2664201202182x

Waring P Snowdonia bat mitigation pilot project report Penrhyndeudraeth SnowdoniaNational Park Authority 2011 [Available from httproostbatsorguksitesdefaultfilespublicationsSNPA_Mitigation Report Final_2011pdf]

Warren RD Waters DA Altringham JD Bullock DJ The distribution of Daubentons bats(Myotis daubentonii) and pipistrelle bats (Pipistrellus pipistrellus) (Vespertilionidae)in relation to small-scale variation in riverine habitat Biol Conserv 20009285ndash91httpdxdoiorg101016S0006-3207(99)00062-2

Waters D Jones G Furlong M Foraging ecology of Leislers bat (Nyctalus leisleri) at twosites in southern Britain J Zool 1999249(2)173ndash80 httpdxdoiorg101017S0952836999010067

White EP Factors affecting bat house occupancy in Colorado Southwest Nat 200449(3)344ndash9

Wickramasinghe LP Harris S Jones G Vaughan Jennings N Abundance and speciesrichness of nocturnal insects on organic and conventional farms effects of agriculturalintensification on bat foraging Conserv Biol 200418(5)1283ndash92 httpdxdoiorg101111j1523-1739200400152x

WWEA The World Wind Energy Association annual 2012 report Bonn World WindEnergy Association 2013 p 1ndash22


among the scientific community Since the implementation of the firstwind farms in Europe and the USA it was assumed that bats could beaffected by collision with the moving turbines However this grouponly became a research focus when bat fatalities were documented aspotentially higher than bird fatalities (Cryan and Barclay 2009Rodrigues et al 2008 Rydell et al 2010)

Bat fatalities result from direct collision or from barotraumaie experiencing rapid pressure changes that cause severe internalorgan damage especially in the lungs (Baerwald et al 2008 Grodskyet al 2011 Rollins et al 2012) Bat fatality rates show significant vari-ation among sites and years and although there are general recommen-dations from EUROBATS for the monitoring and estimation of fatalities(eg Rodrigues et al 2008) the lack of standardised methods to esti-mate these rates hinders comparisons (EUROBATS 2012) Nonethelesssignificant fatality rates have been recorded in both theUSA and EuropeIn a review of the patterns of bat fatalities at wind energy facilities inNorth America (USA and Canada) Arnett et al (2008) present asmany as 696 bat fatalities per turbine per year In Europe although aglobal study has not been done yet it is known that fatality rates varylargely among sites and high numbers were also reported especiallyfrom Hohe Eck wind farm in southern Germany where rates of 411bat fatalities per turbine per year occurred (Rydell et al 2010)

In the European Union all wind energy developments that are likelyto have a significant impact on environment should be subjected to anenvironmental impact assessment (EIA) (Article 2 Directive 85337EEC) That is the formalised procedure that ensures that the likelyeffects of a new wind farm on the environment are fully understood(Jay et al 2007) and taken into account before the proposed project isgiven development consent For that reason they are a good decision-making tool on project viability (Rajvanshi 2008 McKenney andKiesecker 2010) and should identify and if possible quantify impactson biodiversity confirm the need for mitigation and set out the mitiga-tion required for the identified impacts (BBOP 2009a Marshall 2001)The negative impacts are mitigated through the implementation ofmeasures that aim at the reduction of those impacts to the pointwhere they have no adverse effects (BBOP 2012a) Within the EUthere are regulations that consider population effects and also regula-tions focusing on individual specimens of species that are strictlyprotected Ultimately both focus on negative effects that will occur atthe population level though considering that in threatened speciesthese effects are more severe so even a reduced number of fatalities isof great concern

Mitigation involves any process activity or action designed to avoidreduce or compensate those significant adverse impacts (Marshall2001) The mitigation measures are categorised according to theirgoals and following the mitigation hierarchy (a) avoid (b) reducemoderateminimise (c) offsetcompensate (Fig 1) (BBOP 2012dDarbi et al 2009 PricewaterhouseCoopers 2010) This hierarchy im-plies that avoidance strategies have priority over remedial solutions(Marshall 2001) and that those impacts that cannot be avoided orminimised must be addressed through biodiversity offsets or

Reduce Moderate Minimise

Avoid

Offset amp Compensate

Fig 1Mitigation hierarchy (adapted from PricewaterhouseCoopers 2010)

compensatory measures (BBOP 2009a PricewaterhouseCoopers2010) Strictly following the mitigation hierarchy it is important to un-derline that offsets or compensatory measures are the ldquolast resortrdquo andmust not provide a justification for proceeding with projects for whichthe residual impacts on biodiversity are unacceptable This means thatthe ldquono gordquo option has to be considered seriously and applied in caseswhere the destruction of unique habitats or irreversible loss wouldotherwise occur (BBOP 2012c Bishop 2006)

The last step of themitigation hierarchy the offset or compensationhas been acquiring importance and popularity among conservationists(McKenney and Kiesecker 2010 Kiesecker et al 2010) The clarifica-tion between those two concepts has been under discussion in recentyears and Biodiversity Offsets were defined by BBOP as ldquomeasurableconservation outcomes resulting from actions designed to compensatesignificant residual adverse impacts on biodiversity after appropriateprevention and mitigation measures have been takenrdquo The offsetmeasures should ldquoachieve no net loss and preferably a net gain of biodi-versity taking into account species composition habitat structureecosystem function and peoples use and cultural values associatedwith biodiversityrdquo (BBOP 2013 ten Kate et al 2011) To demonstrateno net loss or a net gain conservation action outcomes must demon-strate that biodiversity conserved is sufficient and of the same kind asthe biodiversity lost or degraded due to the projects impacts and thatbiodiversity persistence is not compromised or if possible enhanced(BBOP 2013 ten Kate et al 2011) For compensation there is no cleardefinition set by BBOP and the edge between these two concepts ismainly related with the capacity of a project to demonstrate that theconservation outcomes are enough to guarantee ldquono net loss or a netgainrdquo (BBOP 2013 ten Kate et al 2011)

Offsets are a relatively recent field of investigation (Hayes andMorrison-Saunders 2007) and the Business and Biodiversity OffsetsProgramme has developed and introduced the Standards on Biodiversi-ty Offsets These standards are based on 10 principles that provide aframework for the design and implementation of biodiversity offsetsand to verify its success (BBOP 2009a) (1) adherence to mitigationhierarchy (2) limits to what can be offset (3) landscape context(4) no net loss (5) additional conservation outcomes (6) stakeholderparticipation (7) equity (8) long-term outcomes (9) transparencyand (10) science and traditional knowledge

The compliance with these principles helps to ensure that adequateoffset programmes are created and implemented However there areseveral conservation programmes that for a variety of reasons aresimply unable to follow all these principles which is more evident inthe case of principle 4 mdash no net lossa net gain For some projects it isnot possible to prove no net loss because i) pre-impact data is lackingand it is impossible to know what was lost as a result of the projectandor ii) gains achievable by the conservation actions are not easilyquantified If so the programme in question should not be consideredas an offset but as a compensation programme Fig 2 illustrates thecontinuum from a very basic form of compensation to the type ofcompensation that is a full offset and may realistically be expected toachieve no net loss or even a net gain

Despite the recommendation to follow the mitigation hierarchymonitoring programmes in several Europeanwind farms have revealedthat in some situations significant impact over bat populations may beoccurring (EUROBATS 2013) So it is essential to guarantee that foreach wind energy facility the mitigation hierarchy is followed fromthe beginning and that this sensitive group is taken into account in allsteps In that context the implementation of the mitigation hierarchyshould start during the planning and design phase in order to avoidany important area such as breeding hibernating areas andor foraginghabitats of threatened bat species (EC 2010) However identifyingpotential impacts during the planning phase may be a difficult taskunless it is made in extreme circumstances with easily predictableimpacts or in the predictable absence of impacts (eg near an importantroost or at a hostile windy and cold site) Furthermore in some cases
































































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Creation of ponds
















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51(2015)

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Concluding remarks









Acknowledgements


References





































































































































































































































































Long distance(5 27)

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pactAssessm

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51(2015)

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utoutSo

rtndopsee age

eed ft

a

ofesppsth

19(1nd





















Creation of ponds
















Short-term Low




Short-long-term Low


Short-term Medium

























17FPeste

etalEnvironmentalIm

pactAssessm

entReview

51(2015)

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Concluding remarks









Acknowledgements


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Creation of ponds
















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Concluding remarks









Acknowledgements


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Short-term Low




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51(2015)

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Concluding remarks









Acknowledgements


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Concluding remarks









Acknowledgements


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Acknowledgements


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How to mitigate impacts of wind farms on bats? A review of potential conservation measures in the...

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Transcript of How to mitigate impacts of wind farms on bats? A review of potential conservation measures in the...