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How to mitigate impacts of wind farms on bats? A review of potential conservation measures in the European context Filipa Peste a,b, , Anabela Paula c , Luís P. da Silva a,b,d , Joana Bernardino e , Pedro Pereira e , Miguel Mascarenhas c , Hugo Costa e , José Vieira f , Carlos Bastos f , Carlos Fonseca a,b , Maria João Ramos Pereira a,g,h a Centre for Environmental and Marine Studies (CESAM), Portugal b Department of Biology, University of Aveiro, Portugal c Bioinsight - Ambiente e Biodiversidade, Lda. Lisboa, Portugal d MARE and CEF, Department of Life Sciences, University of Coimbra, Portugal e Bio3 - Estudos e Projectos em Biologia e Recursos Naturais, Lda. Almada, Portugal f Department of Electronics, Telecommunications and Informatics / IEETA, University of Aveiro, Portugal g PPGBAN, Department of Zoology, Institute of Biosciences, Federal University of Rio Grande do Sul, Brazil h PPGEC, Federal University of Mato Grosso do Sul, Brazil abstract article info Article history: Received 17 July 2014 Received in revised form 5 November 2014 Accepted 26 November 2014 Available online xxxx Keywords: Wind farms Impacts Bats Mitigation hierarchy Offsets/compensation measures Wind energy is growing worldwide as a source of power generation. Bat assemblages may be negatively affected by wind farms due to the fatality of a signicant number of individuals after colliding with the moving turbines or experiencing barotrauma. The implementation of wind farms should follow standard procedures to prevent such negative impacts: avoid, reduce and offset, in what is known as the mitigation hierarchy. According to this approach avoiding impacts is the priority, followed by the minimisation of the identied impacts, and nally, when residual negative impacts still remain, those must be offset or at least compensated. This paper presents a review on conservation measures for bats and presents some guidelines within the compensation scenario, focusing on negative impacts that remain after avoidance and minimisation measures. The conservation strategies presented aim at the improvement of the ecological conditions for the bat assemblage as a whole. While developed under the European context, the proposed measures are potentially applicable elsewhere, taking into consideration the specicity of each region in terms of bat assemblages present, landscape features and policy context regarding nature and biodiversity conservation and management. An analysis of potential opportunities and constraints arising from the implementation of offset/compensation programmes and gaps in the current knowledge is also considered. © 2014 Elsevier Inc. All rights reserved. Introduction In the last 20 years, wind energy became the fastest growing source of power generation in the world and it is expected to continue growing in Europe, North America and in the developing markets of China and India. There is also a growing trend in Latin America, new Asian and Eastern European markets and in some African countries (Ledec et al., 2011; WWEA, 2013), though in the past three years, due to the global economic crisis, the rate of growth has slowed down (WWEA, 2013). In Europe, during the last 30 years, wind energy has grown from 100 MW to over 100,000 MW (EWEA, 2012). Among European coun- tries, Germany, Spain, Italy, France, UK and Portugal have shown an extraordinary growth in wind energy in the last decade (WWEA, 2013). In fact, energy produced from renewable sources is a priority in the European Union (EU) agenda, especially after the implementation of the Renewable Energy Directive in 2009 (2009/28/EC) and subse- quent amending acts. This directive establishes mandatory targets for 2020, imposing a 20% share of energy from renewable sources by 2020 in all member states. As a consequence, several member states have seriously invested in the development of wind energy, as a crucial way to attain this goal. This goal shift towards a more sustainable production of energy to reduce the emission of greenhouse gases is certainly desirable, but the development of wind energy facilities does not come free of risk of negative impacts on biodiversity (Voigt et al., 2012), as well as noise and visual impacts for local human communities (Leung and Yang, 2012). Among vertebrates, bats are pointed out as one of the most affected groups (Arnett et al., 2011; Barclay et al., 2007; Johnson et al., 2003; Rydell et al., 2010). In the last few years, the concern about the negative impact of wind farms on bat assemblages has signicantly increased Environmental Impact Assessment Review 51 (2015) 1022 Corresponding author at: Centre for Environmental and Marine Studies (CESAM) & Department of Biology, University of Aveiro, Campus de Santiago, 3810-193, Aveiro, Portugal. Tel.: +351 234247138. E-mail addresses: [email protected], [email protected] (F. Peste). http://dx.doi.org/10.1016/j.eiar.2014.11.001 0195-9255/© 2014 Elsevier Inc. All rights reserved. Contents lists available at ScienceDirect Environmental Impact Assessment Review journal homepage: www.elsevier.com/locate/eiar

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  • Environmental Impact Assessment Review 51 (2015) 10–22

    Contents lists available at ScienceDirect

    Environmental Impact Assessment Review

    j ourna l homepage: www.e lsev ie r .com/ locate /e ia r

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

    Filipa Peste a,b,⁎, Anabela Paula c, Luís P. da Silva a,b,d, Joana Bernardino e, Pedro Pereira e, Miguel Mascarenhas c,Hugo Costa e, José Vieira f, Carlos Bastos f, Carlos Fonseca a,b, Maria João Ramos Pereira a,g,h

    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: [email protected], [email protected]

    http://dx.doi.org/10.1016/j.eiar.2014.11.0010195-9255/© 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 history:Received 17 July 2014Received in revised form 5 November 2014Accepted 26 November 2014Available online xxxx

    Keywords:Wind farmsImpactsBatsMitigation hierarchyOffsets/compensation 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 finally,when 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 scenario,focusing 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 whole.While developed under the European context, the proposed measures are potentially applicable elsewhere,taking 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 offset/compensation programmes and gapsin the current knowledge is also considered.

    © 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 al.,2011; 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 100,000 MW (EWEA, 2012). Among European coun-tries, Germany, Spain, Italy, France, UK and Portugal have shown an

    and Marine Studies (CESAM) &e Santiago, 3810-193, Aveiro,

    t (F. Peste).

    extraordinary growth in wind energy in the last decade (WWEA,2013). 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 (2009/28/EC) 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., 2003;Rydell et al., 2010). In the last few years, the concern about the negativeimpact of wind farms on bat assemblages has significantly increased

    http://crossmark.crossref.org/dialog/?doi=10.1016/j.eiar.2014.11.001&domain=pdfhttp://dx.doi.org/10.1016/j.eiar.2014.11.001mailto:[email protected]:[email protected]://dx.doi.org/10.1016/j.eiar.2014.11.001http://www.sciencedirect.com/science/journal/01959255www.elsevier.com/locate/eiar

  • 11F. Peste et al. / Environmental Impact Assessment Review 51 (2015) 10–22

    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, 2009;Rodrigues et al., 2008; Rydell et al., 2010).

    Bat fatalities result from direct collision or from barotrauma,i.e., 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(e.g. Rodrigues et al., 2008), the lack of standardised methods to esti-mate these rates hinders comparisons (EUROBATS, 2012). Nonetheless,significant fatality rates have been recorded in both theUSA and Europe.In a review of the patterns of bat fatalities at wind energy facilities inNorth America (USA and Canada), Arnett et al. (2008) present asmany as 69.6 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 41.1bat 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 85/337/EEC). 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 species,these effects are more severe, so even a reduced number of fatalities isof great concern.

    Mitigation involves any process, activity or action designed to avoid,reduce or compensate those significant adverse impacts (Marshall,2001). The mitigation measures are categorised according to theirgoals and following the mitigation hierarchy: (a) avoid, (b) reduce/moderate/minimise, (c) offset/compensate (Fig. 1) (BBOP, 2012d;Darbi 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 & Compensate

    Fig. 1.Mitigation hierarchy (adapted from PricewaterhouseCoopers, 2010).

    compensatory measures (BBOP, 2009a; PricewaterhouseCoopers,2010). Strictly following the mitigation hierarchy, it is important to un-derline that offsets or compensatory measures are the “last resort” andmust not provide a justification for proceeding with projects for whichthe residual impacts on biodiversity are unacceptable. This means thatthe “no go” 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 compensation,has 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 “measurableconservation outcomes resulting from actions designed to compensatesignificant residual adverse impacts on biodiversity, after appropriateprevention and mitigation measures have been taken”. The offsetmeasures should “achieve no net loss and preferably a net gain of biodi-versity taking into account species composition, habitat structure,ecosystem function and people's use and cultural values associatedwith biodiversity” (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 project's 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 “no net loss or a netgain” (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 — no net loss/a 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 project,and/or 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 hierarchy,monitoring 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 and/or foraginghabitats of threatened bat species (EC, 2010). However, identifyingpotential impacts during the planning phase may be a difficult task,unless it is made in extreme circumstances with easily predictableimpacts or in the predictable absence of impacts (e.g. 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) 10–22

    the real effects are only indentified during the monitoring of the post-construction phase (e.g. Hein et al., 2013). So, an adaptive managementapproach should be followed in order to reconsider the mitigationhierarchy during the construction and/or exploration phase based onmonitoring results, to continually improve its performance (BBOP,2009c). 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 Arnett,2006a, b, 2007). Radar emissions also seem to negatively affect bat ac-tivity (Nicholls and Racey, 2007, 2009). However, to our knowledge,until now, no device was successfully developed or commercialised.Nevertheless, as bat mortality rates seem to be higher during lowwind nights (Amorim et al., 2012; Kerns et al., 2005; Rydell et al.,2010) 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. However,despite 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-sation/offset 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 (e.g. 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 (e.g. Popa-Lisseanu and Voigt, 2009).European bat species are classified into three migratory categories ac-cording to the distances recorded — long distance (N500 km), regional(100–500 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, forestry/agricultural 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 place,the 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

  • 13F. Peste et al. / Environmental Impact Assessment Review 51 (2015) 10–22

    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 2012,wind turbines in Europe killed at least 27 species, of which the mostaffected were Pipistrellus pipistrellus (965 fatalities), Nyctalus noctula(704), P. pipistrellus/Pipistrellus 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(e.g. Boye andDietz, 2005; Entwistle et al., 2001;Meschede 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 around.Whenever 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, 2002;Russo 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 conservation.In mature forests, bats often use large trees and snags as roosts(Crampton and Barclay, 1998; Hutson et al., 2001; Kunz and Lumsden,2003; 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 (e.g. Guldin et al., 2007; Loeb andO'Keefe, 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, 2003;Warren 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, 2007;Marchante et al., 2005). Changes in trophic structures have alreadybeen shown for spiders in response to invasive plants (Petillon et al.,2005). Some exotic plants, like Australian acacias, which are amongthe most significant invaders worldwide (Richardson and Rejmánek,2011), 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 al.,2007) 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

    Leisler's 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 Asia.P. 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 migratoryspecies.Occurs 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 Ireland,Scotland, northern Scandinavia andSouthern parts of Greece and Italy.Mostly 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. Hunts4–15 m above ground, onpaths and woodland edges,also over water.(3, 9, 11, 13, 14, 15)

    Forest species, uses p eferentiallydeciduous forests, bu can also be foundon resinous forests a urban parks,hunting 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 gardens,frequently 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 structures,as 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 km/h.(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 Trichoptera,Diptera 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 buildings.Hibernates in crevices, cliffs,buildings, 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 sedentary,but 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

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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 bats,e.g. 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; GallegoFernández 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 (Ciechanowski,2005; Kusch and Schotte, 2007; Rebelo and Rainho, 2009; Salvo et al.,2009). 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; Asociación 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 conditions,the 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., 2001;Russo 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, 2007;Haddad 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 Feldhamer,2005). So, the maintenance of old trees and snags, prime locationswhile natural shelters for forest bats, must also be provided (e.g.Ruczyński 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 caves,mines 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 roosts,either 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 species,but also by species of the genus Nyctalus, among others (e.g. 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, 1999;Sherwin 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 (e.g. BCT,2006; Kelleher andMarnell, 2006; Mitchell-Jones, 2004;Waring, 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, 2009;Luisi et al., 1993; Oleksyn and Przybyl, 1987; Santos and Martins,1993; Siwkcki and Ufnalski, 1998; Sonesson and Drobyshev, 2010;Szepesi, 1997; Thomas et al., 2002). As a consequence, many forest-

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    dwelling bats have lost their natural roosting habitats. Even bat speciesadapted to artificial structures (e.g. walls and stone houses, bridges,fences) 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 (e.g. 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 fact,Ciechanowski (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 entrance,N. 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 refuges,or 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 years,which vary with the placement site of the box: trees — 20%, poles —52%, and buildings— 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., 2001;Barclay, 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, 2011,2013), 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 (IPCC,2008). 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, and/or take advantage of the proximity of other sources of watersuch as wells and fountains. Still, in times of severe water scarcity,ponds could be supplied artificially. A few studies provide supportfor the importance of artificial water sources for bats. For example,heliponds 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 Céréghino, 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 (e.g. Nyctalus spp. and Eptesicus spp.Ciechanowski, 2002), while those integrated with connectivity ele-ments such as treelines may favour species that follow linear landscapefeatures (e.g. Pipistrellus spp. Downs andRacey, 2006). A comprehensivecompilation of pond designs is available from the project Million Ponds(www.freshwaterhabitats.org.uk/projects/million-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 offset/com-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 above,the 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 offset/compensation effect, and aqualitative estimate on the implementation cost.

    Bat conservation and wind energy in Europe: opportunities,challenges 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, Italy,France, UK and Portugal at the top of the installed capacity (WWEA,2013). 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 (Schmithüsen and Hirsch, 2010), and more than50% of Europe's 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 and/or ii) agree-ments with landowners or managers may be essential to defineregimens of sustainable land-uses. The definition and implementation

    http://www.freshwaterhabitats.org.uk/projects/million-ponds/

  • Table 2Offset/compensatory 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).

    Offset/compensatory 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 Low/medium

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

    Short-/medium-term Medium/high

    Maintenance of the extensiveexploitation of traditionalagro-forestry European ecosystems

    Montados/DehesasOlive grovesWoodland pastures

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

    Short-/medium-term Low/medium

    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

    Short-/medium-term Medium

    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 Medium/high

    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 Short/long-term Low/medium

    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

    Short-/medium-term Medium/high

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    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, ultimately,become an additional source of threat for wildlife.

    In the European Union, the Birds Directive (79/409/EEC) and theHabitats Directive (92/43/EEC) 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 interest,withno available alternatives,guaranteeing effective compensatory measures, and ensuring that theoverall coherence of the Natura 2000 network is maintained (Dodd,2007). However, the directive has serious implementation problems;presently, as the network-designation process reaches its conclusion,the 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 (e.g. Apostolopoulou and Pantis, 2009).

    Additionally, several important areas for wildlife are still lackingany kind of protection policy/mechanism (Araújo et al., 2007;Dimitrakopoulos et al., 2004; Maiorano et al., 2007; Sánchez-Fernándezet 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 legislation.Nevertheless 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 and/or 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 others,have 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 offset/compensatory 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 offset/compensation actions. Often, the involvement of differentindividuals, groups and/or associations may be necessary to ensurebiodiversity offset fairness; the success of the offset/compensationprogrammes 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, loggers,either 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 (Asociación 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, i.e., agreements with individuals to cede the right to convertland cover for profit (Quintero and Mathur, 2011). More specifically,these schemes foresee payments to farmers who voluntarily sub-scribe to commitments related to environmental protection (http://ec.europa.eu). Agro-environmental measures are compulsory for themember-states (Council Regulation on Rural Development 1698/2005/EC) 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 — thus creating an additional constraint tothe application of many of the proposed measures.

    The European landscape entails an additionalmanagement problem,as 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 and/ormanager 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), offsets/compensatory programmes that achieve ‘netgain’ 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 offset/compensatory measure implementation and iii)the monitoring of effectiveness and success of the implemented mea-sures, should be the rule in European countries (Baber, 2012; BBOP,2012b; 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 – though oftenonly for specific projects and if included in the infrastructure permitconditions – 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 offset/com-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

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    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 offset/compensation 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 research.Additionally, the application of the measures we suggest should beconsistently adapted to each wind farm, considering all the localspecificities – in particular the local bat assemblage and landscapeconfiguration – ensuring a monitoring scheme capable of detectingundesirable unexpected effects.

    Based on our review, we found important knowledge gaps in:i) 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 projectR&D project, CENTRO-07-0202-FEDER-011541 Wind & Biodiversity,co-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-C/MAR/LA0017/2013.

    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.

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