L 158 - 2010-11 (1. samling) - Endeligt svar på spørgsmål 5: Spm. om, hvilken dokumentation der foreligger for, at dyrkning af flerårige energiafgrøder i de dyrkningsfrie randzoner vil føre til mere biodiversitet, til fødevareministeren

AbstractThe urgency for mitigation actions in response to climate change has stimulated policymakers to encourage the rapid expansion of bioenergy, resulting in major land-usechanges over short timescales. Despite the potential impacts on biodiversity and theenvironment, scientiﬁc concerns about large-scale bioenergy production have onlyrecently been given adequate attention. Environmental standards or legislative provi-sions in the majority of countries are still lagging behind the rapid development ofenergy crops. Ranging from the ﬁeld to the regional scale, this review (i) summarizes thecurrent knowledge about the impact of biomass crops on biodiversity in temperateregions, (ii) identiﬁes knowledge gaps and (iii) drafts guidelines for a sustainablebiomass crop production with respect to biodiversity conservation. The majority ofstudies report positive effects on biodiversity at the ﬁeld scale but impacts stronglydepend on the management, age, size and heterogeneity of the biomass plantations. Atthe regional scale, signiﬁcant uncertainties exist and there is a major concern thatextensive commercial production could have negative effects on biodiversity, in parti-cular in areas of high nature-conservation value. However, integration of biomass cropsinto agricultural landscapes could stimulate rural economy, thus counteracting negativeimpacts of farm abandonment or supporting restoration of degraded land, resulting inimproved biodiversity values. Given the extent of landconversion necessary to reach thebioenergy targets, the spatial layout and distribution of biomass plantations willdetermine impacts. To ensure sustainable biomass crop production, biodiversity wouldtherefore have to become an essential part of risk assessment measures in all thosecountries which have not yet committed to making it an obligatory part of strategiclandscape planning. Integrated environmental and economic research is necessary toformulate standards that help support long-term economic and ecological sustainabilityof biomass production and avoid costly mistakes in our attempts to mitigate climatechange.Keywords:bioenergy, biomass crops, ecosystem services, land-use change, policy guidelines, short-rotation coppice, spatial scale dependency, sustainability

290J . D A U B E Ret al.the environmental and socio-economic sustainability oflarge-scale energy crop production, as well as its effec-tiveness for reaching energy security and GHG mitiga-tion targets (e.g. Hillet al.,2006; Robertsonet al.,2008;Russi, 2008; Searchingeret al.,2008; Florin & Bunting,2009; Petrou & Pappis, 2009; Tilmanet al.,2009). Inorder to reach the benchmarks of energy productionfrom bioenergy, vast areas of land will have to beconverted to energy crop production, resulting in majorland-use changes over relatively short timescales(RCEP, 2004; EEA, 2006; Tucket al.,2006; Marland &Obersteiner, 2008; Fischeret al.,2010). Despite thespatial extent of this development and the potentialseverity of its impact on the environment, energy cropplanting in many countries is currently done withoutappraisal and with few environmental standards orlegislative provisions delineating principles of energycrop production (UN-Energy, 2007; Groomet al.,2008;but see Haughtonet al.,2009).Land-use change, in general, is considered one of themajor drivers of biodiversity loss (Salaet al.,2005).Therefore, although indirect positive effects of energycrop production on biodiversity through potential halt-ing of climate change are acknowledged, there is con-cern about the direct effects that expansion of energycrop production could have on biodiversity (Huston &Marland, 2003; Robertsonet al.,2008; Eggerset al.,2009).Already, the cultivation of energy crops has a signiﬁcantimpact on land use. Out of the total area of arable landin 25 European Union countries in 2005 (97 Mha), about1.8 Mha were used for producing raw materials forbioenergy (Commission of the European Communities,2005). At national levels, for instance in England, thearea of land planted with biomass crops such asMis-canthus(predominantlyMiscanthusÂgiganteus)andshort rotation coppice (SRC) willow (Salix spp.) hasincreased more than seven times since 2003 to anestimated area of 15 000 ha (Haughtonet al.,2009). TheUK government’s Biomass Strategy (Defra, 2007); how-ever, suggests that the area occupied by bioenergycrops, grown for heat and power generation, couldreach 1.1 million ha by 2020. Similarly, in Germany,the land area used for production of energy crops, inparticular of maize for biogas, quadrupled during the10 years to 2008, to cover ca. 17% of agricultural land(Wieheet al.,2009).There is, therefore, an urgent need for well-struc-tured, conceptual frameworks that connect scientiﬁcknowledge with policy making and action, to establishenvironmental and biofuel certiﬁcation standards forenergy crop production (Groomet al.,2008; Meinkeet al.,2009). Drafting such standards is a challengingtask because the primary objectives of energy cropcultivation are climate change mitigation and energysecurity and not the support of wildlife-friendly farm-ing systems. Nevertheless, preliminary studies showthat economically viable and environmentally sustain-able, integrated food and energy agro-ecosystems mightbe feasible (Porteret al.,2009). The wide scope for land-use planning which includes energy crops could pre-sent an opportunity for novel agricultural landscapes ofhigher economic viability and environmental sustain-ability, provided that holistic, knowledge-based plan-ning concepts are developed and applied (Scherr &McNeely, 2008; Kohet al.,2009). Application of scientiﬁcexpertise on how energy crop cultivation affectsbiodiversity, ecosystem services, economic viabilityand ecological sustainability of natural habitats andagricultural lands can contribute to evaluation andplanning standards that help in achieving win–winsolutions for biodiversity conservation, GHG controland energy security (Huston & Marland, 2003; Groomet al.,2008).In this context it is important to differentiate betweenﬁrst and second generation energy crops as manage-ment intensity, implications for land-use change and, asa result, impacts on biodiversity differ among the cropsinvolved (UN-Energy, 2007; UNEP, 2009). In contrast toﬁrst generation biofuels, which are currently grown asarable food crops rich in sugar, starch or vegetable oil(such as maize, soybean or rape seed), but can be usedfor ethanol and biodiesel production, second generationfeedstock are perennial ligno-cellulosic crops such asfast growing trees (SRC) or grasses used for combustionor ethanol production (see Karp & Shield, 2008 for anoverview). Compared with arable crops, ligno-cellulo-sic biomass crops have the potential for positive effectson soil carbon sequestration and soil properties ingeneral, GHG emissions, biodiversity and energy bal-ance (Styles & Jones, 2008; Roweet al.,2009). The majorfocus of this review is on second generation biomasscrops, in particular on SRC crops and perennial grasses,because they are currently considered to be the mostefﬁcient and sustainable feedstock for bioenergy pro-duction in temperate regions (Adleret al.,2007; Karp &Shield, 2008; Russi, 2008; Williamset al.,2009; UNEP,2009).The aims of this review are (i) to summarize thecurrent knowledge about the impact of biomass cropproduction on biodiversity in temperate regions with anemphasis on the major producers, Europe and NorthAmerica, (ii) to identify knowledge gaps and (iii) todraft guidelines for a sustainable energy crop produc-tion with respect to biodiversity conservation, coveringa range of spatial and temporal scales.The effects of biomass crop production on biodiver-sity and associated ecosystem services depend greatlyon the respective crop and its management, howr2010 Blackwell Publishing Ltd,GCB Bioenergy,2,289–309

BIOMASS CROPS AND BIODIVERSITYproduction is integrated into existing landscapes andfarming systems, how much land is converted andwhether intensively managed agricultural land, mar-ginal agricultural land or natural areas are affected (e.g.Ranney & Mann, 1994). As a consequence, impacts ofbiomass crops on biodiversity operate on a wide rangeof spatial scales. In this review, we have separatedimpacts of biomass crops at the ﬁeld/crop, landscapeand regional scale because this distinction facilitatesisolating particular pressures and impacts and howthey might be assessed (Firbank, 2008). At the ﬁeldscale, we look at the intrinsic biodiversity value of thebiomass crops in comparison with the crops replacedand to alternative ﬁeld usages. We review the intensityof management required for biomass crop cultivation,the structural habitat quality and effects of secondaryland use of energy crops such as waste water disposal.At the landscape scale, we examine the spatial structureand turnover of habitats within a landscape (homoge-nization vs. increased heterogeneity), the type or com-bination of biomass crops planted and the potentialinvasiveness of the crops and genetic contamination ofwild plants. At the regional scale, we compare prog-noses for future land area demanded by biomass cropsand respective effects of the crops across regions and forareas of different nature conservation value.

Field-scale studies on biomass crops and biodiversityAn intensive literature search provided us with a totalof 47 publications and reports from nine Europeancountries and the USA which studied the impacts ofbiomass crop production on biodiversity (Table 1 andAppendix S1). The majority of biomass crops studiedwere SRC crops in particular willow, poplar (Populusspp.) or mixed plantations, and the perennial grassesMiscanthusspp., reed canary grass (Phalarisarundinacea)and switchgrass (Panicumvirgatum).Most of the Eur-opean studies, both on SRC and perennial grasses, wereconducted in the UK and Germany. The North Amer-ican studies focussed primarily on willow, poplar andswitchgrass.It is likely that this list of studies is biased towardsstudies written in English and German because theauthors were able to intensively search library data-bases and internet resources in those languages. Cross-references only rarely directed us to studies from non-English- or non-German-speaking countries. 43% of thestudies we found were not published in internationaland/or easily accessible journals but were reports (3),conference proceedings (2) or publications in smaller,national journals (15). It is likely that several moreEuropean studies do exist, but results are hidden inreports or conference proceedings. Studies focussing onr2010 Blackwell Publishing Ltd,GCB Bioenergy,2,289–309

weed or pest control in energy crops were not includedin the list as they provided very limited informationabout the biodiversity in the crops but the implicationsfor biodiversity arising from crop management wereincluded in the discussion of ﬁeld-scale impacts.Most of the studies on SRC crops focused on birds,both breeding and winter birds (Table 1). Some of theNorth American studies also included mammals andvery few looked at soil fauna. Many European studies,both on SRC and perennial grass crops, focused on, orincluded in addition to birds, vegetation and variousgroups of canopy-, ground- and soil-living inverte-brates (Table 1 and Appendix S1). The comprehensive-ness of the studies varies considerably in terms ofnumber of sites surveyed, age of sites and samplingstrategy used (see also the section on ‘Knowledge gapsat the ﬁeld scale’).The vast majority of studies compared species rich-ness, abundance and species composition in energy cropplantations to other types of land use, either of thesurrounding landscape or land use replaced by therespective plantations (Table 2). The land use most fre-quently compared with both SRC and perennial grasseswas arable land (in particular land used for winterwheat, maize, barley and oilseed rape) and the SRCplantations were compared with natural woodlands ormanaged forests. Few studies compared biomass cropswith grassland, set-aside or noncultivated land.The number of studies comparing different types ofenergy crops are also limited (Table 2). Three studiescompare reed canary grass with eitherMiscanthusÂgiganteus(Semere & Slater, 2007a, b) or with other fastgrowing perennial grasses (Jahnova & Bohac, 2009). ASwiss study comparedMiscanthus sinensiswith hemp(Cannabis sp.) and kenaf (Hibiscuscannabinus)and avariety of other renewable primary products (Loeffel& Nentwig 1997). In the USA, willow was comparedwith poplar (Dhondtet al.,2004) and SRC sweetgum(Liquidambarstyraciﬂua)with switchgrass (Ward &Ward, 2001). Several studies did not compare the re-spective energy crops with any other type of land usebut instead compared age structure, plant height ordifferent clones within the energy crops (e.g. Coates &´ˇSay, 1999; Berg, 2002; Dhondtet al.,2004; Bohacet al.,2007; Gru & Schulz, 2008). Nevertheless, those studiesprovide valuable information about the importance ofenergy crop management, heterogeneity, canopy struc-ture and harvesting patterns for various species orspecies groups (Appendix S1).

biodiversity compared with cultivated areas of arablefood crops because, in general, biomass crops havelonger rotation periods, low fertilizer and pesticiderequirements, provide better soil protection, a greaterrichness of spatial structures, are exposed to fewerdisturbances during the growing period, andharvesting is carried out in winter or can be doneafter the breeding period of birds, which again causesless disturbance (EEA, 2007; Haughtonet al.,2009;Roweet al.,2009). Indeed, when compared with arableﬁelds, all types of biomass crop plantations showed apositive effect on species richness for almost all taxastudied (Table 2). Only ground beetles (Coleoptera:Carabidae), and, in some of the studies, rove beetles(Coleoptera: Staphylinidae) were found to have higherspecies richness in arable land than in SRC crops(Liesebach & Mecke 2003; Ulrichet al.,2004; Brittet al.,2007). Weihet al.(2003) reported a similarnumber of plant species across all sites of poplarstands and arable ﬁelds but a small number of specieswere shared between both types of land use.In contrast, most studies comparing SRC crops andwoodland habitats reported lower species richness inthe energy crops or no signiﬁcant differences. Positiveeffects were only recorded for ground beetles and otherground living invertebrates. The most importantﬁndings of these studies, in particular when focussingon birds, was that the species composition of the SRCcrops did not resemble forest bird communities butopen farmland or transitional scrubland communities(Hanowskiet al.,1997; Liesebach & Mulsow, 2003;Reddersen & Petersen, 2004). Plots planted with fastgrowing trees are extremely dynamic and within 4years they can change from being open habitat tobeing young forest-like habitat, with trees reaching10–15 m in height. Consequently, with increasing ageof the plantations, forest elements of the bird faunabecome more common in the SRC plots (Goransson,�1994; Gru & Schulz, 2008; Kroiheret al.,2008). In thecontext of pastoral landscapes, SRC crops create apseudo-arable environment for weeds during theestablishment phase but create early successionwoodland conditions when mature (Fry & Slater, 2008;Valentineet al.,2009). Accordingly, the number ofwoodland indicator plant species increases in poplarplantations compared with agricultural surroundings(Brittet al.,2007). When compared with forests, SRCplantations may contain higher plant species richnessthan coniferous forests, but poorer than in old-growthmixed deciduous forests (Baumet al.,2009).Compared with uncultivated land, the few studieswhich included set-aside land reported higher birdspecies richness in SRC willow plantations but nodifferences for small mammals (Reddersenet al.,2001;r2010 Blackwell Publishing Ltd,GCB Bioenergy,2,289–309

BIOMASS CROPS AND BIODIVERSITYReddersen & Petersen, 2004; Reddersenet al.,2005).Similarly, higher species richness was found for birds,spiders and ground invertebrates inMiscanthusÂgiganteuscompared with uncultivated stands ofPhragmites australis(Jodlet al.1998, 2004), but nodifferences were found in bird species richnessbetween SRC willow and uncultivated fens(Reddersen & Petersen, 2004). Mammals had lowerspecies richness in SRC willow than in small biotopessuch as shelterbelts, grassy ditches or canal banks(Reddersenet al.,2005).Findings reported from the few studies thatcompared species richness of biomass crops withgrasslands were ambiguous. For woody crops, nodifferences were found in earthworms in SRC willowcompared with grasslands (Tischeret al.,2006); willowand poplar had either positive or no effects on birds(Christianet al.,1997; Reddersen & Petersen, 2004); andfewer spider families were recorded in a poplarplantation compared with a ley (an arable ﬁeld beingtemporarily used as a pasture) (Brittet al.,2007). Plantspecies richness and proportions of annuals and short-lived perennials was higher in recently planted SRCwillow ﬁelds compared with grasslands, but declinedagain with increasing age of the plantations (Fry &Slater, 2008). For perennial grass crops, the abundanceof individual birds was higher inMiscanthusÂgiganteusthan in unimproved grassland but there was nodifference in the number of bird species (Clapham &Slater, 2008); and more ground beetle species werefound inM. sinensisthan in managed grassland(Loeffel & Nentwig, 1997).The comparisons among different biomass cropsshowed higher species richness of birds and canopyinvertebrates in SRC willow than in SRC poplarplantations (Sage & Robertson, 1996) but breedingbird density was higher in mixed plantations than inpure willow stands (Kavanagh, 1990). This indicatesthat the physical structure of the vegetation is animportant factor (Sage & Robertson, 1996; Schulzet al.,2009). Higher species richness was reported for birds,plantsandseveralinvertebrategroupsinMiscanthusÂgiganteusthan in reed canary grass(Semere & Slater, 2007a, b), but differences betweenthe crops for birds and mammals were lesspronounced and weed species richness was evenhigher in reed canary grass than inMiscanthusÂgiganteusin the study of Clapham & Slater (2008).Species richness of ground beetles was higher inDactylis glomeratagrassland than in reed canary grassﬁelds (Jahnova & Bohac, 2009).Biomass crop management, age and heterogeneity.Ingeneral, positive effects of biomass crop cultivation onr2010 Blackwell Publishing Ltd,GCB Bioenergy,2,289–309

biodiversity are expected in the long term mainly due tothe reduced soil tillage and use of agrochemicals and tothe increased input of litter (Borjesson, 1999; Smeets�et al.,2009). However, many studies have reportedconsiderable differences in biodiversity amongbiomass crop plantations, mainly due to differences inweed control measures, vegetation structure andheterogeneity and harvesting patterns (e.g. Goransson,�1994; Hanowskiet al.,1997; Dhondtet al.,2004; Minoret al.,2004).The development of ground vegetation within theplantations is of great importance for the richness ofthe associated invertebrate communities and for thefood availability and shelter for birds (Ward & Ward,2001; Sageet al.,2006; Semere & Slater, 2007a, b; Fry& Slater, 2008; Bellamyet al.,2009; Valentineet al.,2009). As commercial biomass crops are developed asmonocultures which are managed mainly for maximumyield rather than biodiversity, weed control to avoidyield suppression and secure crop establishment isessential for SRC crops during establishment (Clay &Dixon, 1995) and for perennial grass crops such asMiscanthusduring establishment and annual regrowth(Bullardet al.,1995; see also Baumet al.,2009 for areview on site preparation). As weed problems becomeless severe with maturation of the crops (Bullardet al.,1995; Baumet al.,2009), a succession or introduction of astable perennial ground ﬂora in biomass crops may bedesirable, both from an ecological and economicalviewpoint (Sage, 1999), and mechanical treatments forweed control may be preferable (Baumet al.,2009).SRC plantations support a diverse community ofinvertebrate species (Sage & Tucker, 1997). However,many of those species are pest species such as leaf-eating beetles (Coleoptera: Chrysomelidae) which canreach damaging numbers in the plantations (Sage,2008). In plantations of perennial grass crops, whichoften are nonnative species, impacts of invertebratepests are less severe. To prevent yield losses, pestcontrol in SRC plantations could become necessarywhich would also suppress the nonpest invertebrates.Considering the negative effects on biodiversity butalso the small economic proﬁt margins of biomasscrop cultivation, application of insecticides might notbe a sensible option in SRC crops (Bjorkmanet al.,2004).�As the leaf-eating beetles colonize the crops from theedge in each year, insecticide application in the edgesonly and during beetle colonization could be aneffective, cost efﬁcient and more biodiversity friendlymethod of pest control (Sage, 2008). Bjorkmanet al.�(2004) state that biological control is the only realisticway for pest management in SRC crops. Yet, biologicalcontrol is disrupted by harvesting in winter asgeneralist predators, in contrast to many herbivores,

296J . D A U B E Ret al.overwinter within the crops and take longer to recoverfrom the disturbance than the pest species do.Therefore, in order to support the biocontrol agents, alonger period between harvests that enables them tofully respond numerically and/or to disperse fromrefuges during harvest, or harvesting neighbouringplantations asynchronously would be necessarymanagement strategies (Bjorkmanet al.,2004).�Harvesting times and patterns have been reported tobe of importance for other species groups as well.Harvested ﬁelds of switchgrass support a differentgrassland bird community than nonharvested ﬁeldsdue to a higher and denser vegetation structure (Rothet al.,2005). Harvesting of some ﬁelds and leaving otherﬁelds unharvested would increase the heterogeneity ofvegetation structure and hence the overall birddiversity (Rothet al.,2005). Also in SRC crops,different species prefer different growth stages and asuccession from harvested to mature crops can beobserved (Goransson, 1994; Kroiheret al.,2008). In�general, high-structural complexity enhances thespecies richness and abundance of birds within´plantations (Najera & Simonetti, 2009). Recom-mendations regarding the length of periods betweenharvests are conﬂicting and depend on the speciesgroups in question. As many bird species prefer tallwillow plants for nesting, relatively long periodsbetween harvests would be beneﬁcial for many birdspecies (Berg, 2002), whereas short periods would bebeneﬁcial from a plant conservation point of viewbecause of the reduced light intensity in older stands(Gustafsson, 1987). InMiscanthusplantations, beneﬁtsfor biodiversity were found in the ﬁrst ﬁve years duringcrop establishment but declined when the crop becamedenser (Bellamyet al.,2009). Altogether, irregularharvest and/or establishment patterns of both SRCand grass crops would increase habitat diversity andspecies turnover and therefore the overall biodiversity.In addition, planting more than one clone and, ifpossible, species in a SRC stand would also increasethe vegetation heterogeneity and hence the diversity ofstructural niches for a variety of species (Gustafsson,1987; Dhondtet al.,2004; Londoet al.,2005), as wellas increase the resistance of the plantations to leafeating insects and diseases such as rust (Peacocket al.,1999; McCrackenet al.,2005). Planting of willow speciesand clones with varying ﬂowering times would extendthe ﬂowering season and may provide a morecontinuous resource for ﬂower visiting insects(Reddersen, 2001). Furthermore, planting both maleand female plants provides a more diverse SRCwillow biotope, as males will produce both nectar andpollen while females produce nectar and eventuallyseeds (Reddersen, 2001).In SRC andMiscanthusplantations, headlands andrides provide access to crops for harvesting and othermanagement operations. Those small noncrop areas inthe ﬁelds are an important feature for biodiversity. Inintensively managed farmland they present anopportunity for rough grassland and wood-edgecommunities to exist (Sage, 1998). In particular,butterﬂy abundance and occurrence have been shownto be positively inﬂuenced by biomass crop headlandsand margins (Sage, 1998; Andersonet al.,2004;Haughtonet al.,2009). Among the butterﬂies,numbers of browns (Lepidoptera, Satyrinae) andskippers (Lepidoptera, Hesperiidae), both of whichare associated with speciﬁc larval food plants, werehigher in SRC headlands than in arable headlandsand those two groups were also positively affected byincreasing width of the headlands (Sageet al.,2008).Edges of hybrid poplar plantations located inagricultural land showed strong edge effects forbutterﬂies with high numbers of individuals found inthe plantations resembling open woodland edges (Brittet al.,2007). The number of plant species, in particularof perennials, was greater in SRC headlands than inarable headlands (Sageet al.,2008). An activemanagement of headlands to maximize plant speciesrichness, a diverse vegetation structure and ﬂoralrichness could support a species-rich invertebratecommunity providing ecosystem services such aspollination and biocontrol for the biomass cropsthemselves and/or the arable crops in the vicinity(Sage, 1998; Sageet al.,2008; Bellamyet al.,2009; seealso Marshallet al.,2006).Plantation size and edge effects.The absolute size of thestand can affect the number of taxa present in biomassplantations, for example, plant species richnessincreased with increasing size of a SRC plantation butonly until a size of 0.1–0.3 ha was reached (Kroiheret al.,2008). In addition, the shape of a stand and the relativeedge-to-stand area relationship can affect biodiversity.Plant species richness decreases from the edges towardsthe central parts of poplar stands (Weihet al.,2003) andthe possibility of plant propagules entering a SRCplantation does to some extent depend on the shapeof the stand, with long, narrow stands having longeredges into which seeds could enter via wind or animaldispersal (Gustafsson, 1987). Also, species diversity ofsmall mammals and birds was found to be higher in theborders ofMiscanthusﬁelds compared with the centres(Semere & Slater, 2007a). On large poplar plantations,lower overall bird densities were observed in plantationinteriors than on edges (Christianet al.,1998). In SRCplantations, an edge effect on birds became apparentwith increased time since last harvest (Cunninghamr2010 Blackwell Publishing Ltd,GCB Bioenergy,2,289–309

BIOMASS CROPS AND BIODIVERSITYet al.,2004). The edges of the SRC crops containedhigher bird abundance and the hedgerow boundariescontained higher bird abundance and higher diversitythan hedgerows around arable crops.Multifunctional land use: waste and wastewater application.The rapid growth and relatively frequent harvests ofSRC crops remove nutrients from the soil. Therefore, tomaintain soil productivity, nutrients have to beartiﬁcially applied in similar quantities to thoseremoved during harvest. Because these crops are notfor human consumption, waste organic material in formof municipal wastewater, landﬁll leachate and sewagesludge, can be applied to the plantations instead ofindustrial fertilizer. SRC crops such as willow andpoplar transpire large volumes of water, have anextensive root system and a long growing seasonwhich makes them ideal candidates for irrigatedvegetation ﬁlter systems (Berndeset al.,2008). Amultifunctional land use of biomass production andwaste disposal secures the return of nutrients into thesoil, irrigates the plantations and further enhances theeconomic feasibility of the system (Abrahamsonet al.,1998). Although the application of waste materials tobiomass crops, such as SRC andMiscanthus,might beexpected to have signiﬁcant effects on the ﬂora andfauna, an extensive literature review by Britt (2002)revealed almost no evidence of research that lookeddirectly at the ecological effects of applying farm, urbanor industrial waste products to biomass crops. Thickapplications of waste materials may have a netdetrimental ‘mulching’ effect and suppress the groundﬂora, whilst organic wastes may provide a valuableadditional food source for soil and ground-dwellingmicroorganisms and invertebrates with a generallypositive effect and both would have ‘knock-on’ effectsup through the food chain (Britt, 2002). Thebioaccumulation of heavy metals, organic toxins,polycyclic aromatic hydrocarbons in animal tissuesand increased exposure risk to pathogens are ofimportant concern but generally not well studiedwithin the biomass crop context (Bainet al.,1999;Britt, 2002; Minor & Norton, 2004).In some countries (e.g. Sweden), the willowvegetation ﬁlter system has become established on alarge scale and its potential for phytoremediation ismostly regarded as beneﬁcial, from a wastemanagement point of view (Berndeset al.,2008). Froma biodiversity and sustainability point of view, concernsregarding the generalization of beneﬁcial effects ofthe vegetation ﬁlter systems are: (i) the nutrientcomposition in waste products is often different to therequirements of the plants and (ii) the removal ofnutrients from the system by harvests is limited. Tor2010 Blackwell Publishing Ltd,GCB Bioenergy,2,289–309

avoid leaching of nutrients, amounts and compositionof wastewater should be regulated accordingly(Nielsen, 1994).Persistent organic contaminants may transferthrough the food chains and cause adverse effects onhuman health or on soil fauna and ﬂora after long-termapplication (Chenet al.,2005). Bioactive substances suchas antibiotics, as well as resistant microorganisms fromcontaminated excrements, can cause resistance in soilmicroorganisms, directly or via gene transfer. Thisincreases the risk of infections in humans and animalsthat can not be treated with pharmaceuticals (Thiele-Bruhn, 2003; Carlanderet al.,2009). Anthelmintics werereported to increase mortality in springtails and inhibitnematodes and earthworms in soil (Thiele-Bruhn,2003).Knowledge gaps at the ﬁeld scale.As the compilation ofstudies and observations shows (Tables 1 and 2),negative, neutral and positive impacts of biomasscrops on biodiversity at the ﬁeld scale exist and thedirection of the impact strongly depends on therespective crop, the land use replaced, the landscapesand biogeographical context in which the plantationsare embedded and of course on the group of organismsconsidered.Given the scale of biomass production anticipatedwithin temperate regions of Europe and North America(Graham, 2007; Hellmann & Verburg, 2008), the numberof published studies on potential effects on biodiversityis very small. What is further limiting our knowledgeabout effects on biodiversity and the ability to come to ageneral conclusion is that the number of studies withcomprehensive and scientiﬁcally sound study designs islimited; 14 out of 36 studies on SRC crops and eight outof 11 studies on perennial grass crops were based onfewer than ﬁve replicate sites and lacked proper controlsin some cases (Appendix S1). Therefore, many of theﬁndings are based on singular observations and aredifﬁcult to generalize. In many countries only a fewcommercially used ﬁelds of biomass crops exist. Inconsequence, about half of the existing studies wereconducted on experimental SRC or grass plots and theinferences that can be drawn for extensive commercialproduction of these crops are limited as differentpictures might emerge for full-commercial SRCproduction (Andersonet al.,2004). Fortunately, theimportance of more thorough and interdisciplinaryprojects on environmental impacts of biomass cropshas recently been recognized by national andinternational funding bodies and outputs from theestablished projects can be expected in the coming years.Since the age and maturity of the energy crop is ofgreat importance for the patterns of species richness

298J . D A U B E Ret al.found within the crop (Bellamyet al.,2009; Schulzet al.,2009), crop age needs to be considered within studydesigns. However, for the perennial grass crops inparticular, only a few studies were able to include oldplantations as production in many countries only starteda few years ago and no mature crops were available forthe studies. Ecological studies are further constrainedby the limited spectrum of ages, the small size ofmost available plantations, poor establishment ofsome younger plantations, the lack of statisticalindependence between age and plantation size, and bya limited replication of landscape contexts (Christianet al.,1998; Roweet al.,2009). Caution is advisedfor extrapolating conclusions about habitat orbiodiversity value of biomass plantations from onelandscape to another particularly as there is atendency for different responses in forested asopposed to agricultural regions (Christianet al.,1997).Contradictory results may also arise from comparisonsof biomass plantations located in different bio-geographical regions. For example, in the AmericanNorth-West, large plantations of SRC poplar werefound to decrease ﬂoristic diversity comparedwith old-growth forest, whereas small-scale SRCwillow cultures in Sweden were found to increasebiodiversity compared with coniferous forests (Weihet al.,2003).An assessment of the impacts on biodiversity isfurther hampered by the fact that it is currently notclear which types of land use and habitats would bereplaced by full-scale commercial production of energycrops. Only a few studies analysing the implications ofland allocation to biomass cropping which incorporatedyield variations and other land-use characteristics exist(Lovettet al.,2009). As any change of land use will affectsome species positively and others negatively, it isimportant to identify the priorities for biodiversityconservation with respect to expected landscapechange (Firbank, 2008).The identiﬁcation of useful biodiversity indicators foragricultural landscapes is currently an important topicin biodiversity research (Buchs, 2003; Billeteret al.,2008).�Findings about the usefulness of certain species groupsas indicators are; however, contradictory and theconcept of using indicator taxa has been questioned ingeneral (Wolterset al.,2006; Wugt Larsenet al.,2009).Therefore, a more thorough consideration about thebiodiversity indicators surveyed in biomass cropsshould perhaps be a priority for future studies.Haughtonet al.(2009) have suggested butterﬂies as anappropriate ecological indicator for biomass crops butthis would need further conﬁrmation for widespreaduse as their study was conﬁned to ﬁeld margins ofbiomass crops in England.

Interactions between energy crops and surroundinglandscapesSpecies interchanges between energy crops and surroundingland use.The importance of size and shape of plantationsfor biodiversity at the ﬁeld scale has been discussedabove. Looking beyond the ﬁeld scale, size and shape ofplantations are important factors for the interactionsbetween biomass crops and other land use in thevicinity. For example, in small SRC plantations, a highportion of animals moved from adjacent habitats intothe plantations (Christianet al.,1997; Hanowskiet al.,1997) although colonization of poplar plantations bywoodland carabids was only observed when dispersalfrom surrounding woodlands is possible (Allegro &Sciaky, 2003). Also, a high number of arthropods fromsurrounding arable crops, among them potentialbiocontrol agents, were found overwintering inM.sinensisplantations (Loeffel & Nentwig, 1997) andlocating perennial grass ﬁelds of optimal size close todifferent types of vegetation increases their biodiversity(Smeetset al.,2009). These examples indicate thatspecies communities on plantations are inﬂuencedfundamentally by the surrounding landscape (e.g.Christianet al.,1998). In turn, as biomass crops mightact as temporal habitat or shelter for species, theplantations could also have a positive feedback effecton landscape scale biodiversity and on ecosystemservice performance in neighbouring habitats (e.g.EEA, 2007; Porteret al.,2009). An optimization ofbiomass crop ﬁeld sizes with a larger number ofsmaller plantations interspersed in the landscape maytherefore be desirable from a biodiversity and ecosystemservice perspective (Gustafsson, 1987; Wissinger, 1997;Perttu, 1998; Smeetset al.,2009). This perspective;however, is likely to resurrect the SLOSS debate (aresingle large areas better for biodiversity conservationthan several small areas?) by introducing biomass cropsinto the equation.Invasiveness and genetic pollution.Currently, perennialrhizomatous grasses are among the leading candidatesfor biomass energy production. They are selected andbred for desirable agronomic traits such as tolerance todrought and low soil fertility, as well as highaboveground biomass and enhanced competitiveability against weeds, making a reduction in fertilizerand pesticide applications possible (Barney &diTomaso, 2008). Those plant traits that characterizean ideal energy crop; however, also contribute to ahigher probability of naturalization and invasiveness(Barney & diTomaso, 2008; Buddenhagenet al.,2009).Indeed, some of the most promising biomass crops arenonnative to Europe and North America, hence holdingr2010 Blackwell Publishing Ltd,GCB Bioenergy,2,289–309

BIOMASS CROPS AND BIODIVERSITYthe potential risk of future invasions. By applying aweed risk assessment system for screening outpotentially invasive species, Buddenhagenet al.(2009)found that energy crops, in comparison with nonenergycrops, were two to four times more likely to benaturalized or invasive. Subjecting switchgrass, giantreed (Arundodonax),andM.spp. to a weed riskassessment protocol, which took biogeography,history, biology, and ecology into account, revealedswitchgrass to have a high invasive potential inCalifornia, giant reed to have a high invasive potentialin Florida, andMiscanthusÂgiganteus(a sterile hybrid)to pose little threat of escape in the USA (Barney &diTomaso, 2008). Some small-scale escapes of fertileornamentalMiscanthusgenotypes have been reportedfrom Ohio and Indiana, USA, and therefore it wasrecommended that newMiscanthusgenotypes shouldbe sterile (e.g. triploid) hybrids as a precaution againstthem becoming invasive weeds (Lewandowskiet al.,2000). As there has been little success so far ineradicating or even controlling invading grasses, theecological risks of introducing biomass crops must berigorously assessed before starting their cultivation(Raghuet al.,2006). Barney & diTomaso (2008) suggesta genotype-speciﬁc preintroduction screening for atarget region, consisting of risk analysis, climatematching modelling, and ecological studies of ﬁtnessresponses to various environmental scenarios. The riskof invasiveness also needs to be addressed when, afterthe introduction of the species, land users are planningthe location of the energy crop in a landscape. It wouldfor example be inappropriate to plant giant reedadjacent to high-quality wetlands as it is known toinvade riparian habitats (Firbank, 2008).Genetic contamination of wild native species throughhybridization with nonnative crop species is another riskassociated with large-scale introduction of biomass cropcultivation (Firbank, 2008). Solutions to this problemcould be the development of sterile clones of nonnativespecies or using female clones only, or the use of nativespecies as it is practised with willow species in Sweden(Borjesson, 1999). This would minimize the movement of�genes from crops into native gene pools and avoidgenetic pollution of native taxa. The impact of genetransfer to wild relatives is considered an importantrisk to biodiversity should the crop be geneticallymodiﬁed or should the crop be located in an area ofgenetic diversity (Firbank, 2008).

taking place across ﬁeld boundaries, altering speciesinteractions and responses of populations and commu-nities (Christianet al.,1998; Firbank, 2008). Biomasscrops could destroy seminatural habitats but they couldalso act as buffer areas, shelters or ecotones, hence theycould increase or decrease habitat fragmentation andavailability. Understanding impacts of land-use changeon biodiversity requires developing information andperspectives at broader spatial scales than the planta-tions themselves (Christianet al.,1998; Tscharntkeet al.,2005). This means that for an impact assessment, themainly positive effects of biomass crop plantations onspecies richness, reported by the majority of surveysundertaken at the scale of individual ﬁelds (Table 2),would require an upscaling by taking landscape scaleecological processes into account.Biomass crop production has the potential to changethe diversity of land use making it either more uniformin the case of extensive, large-scale monocultures (seesection on ‘Regional effects’) or more diverse in the caseof smaller polyculture plantations interspersed in apreviously homogeneous landscape (Firbank, 2008; Wil-liamset al.,2009). Its impact also depends on whetherthe landscape is characterized by annual or perennialcropping systems. Biomass crops are likely to increasebiodiversity in areas dominated by agriculture or con-iferous forests but they are not likely to provide wildlifehabitats of major signiﬁcance because the plantationsrarely harbour species that would not be found else-where in the surrounding landscape (Brittet al.,2007;Baumet al.,2009; Schulzet al.,2009). In consequence,biomass plantations could potentially have adverseeffects in landscapes of high conservation value (An-derson & Fergusson, 2006; Schulzet al.,2009).Habitat heterogeneity at a range of spatial scales hasbeen identiﬁed as one key issue for maintenance offarmland biodiversity (Bentonet al.,2003). The intro-duction of biomass crops in farmed landscapes couldimprove habitat heterogeneity, thereby preserving nat-ural biodiversity and simultaneously diversifying theincome mix of landowners (Cook & Beyea, 2000), pos-sibly sustaining farming in marginal high nature valuefarmlands (cf. Bignal, 1998) or helping to restore de-graded land (UNEP, 2009). However, whether produc-tion of biomass crops on marginal or degraded landwould be possible and economically sustainable isquestionable (Howarthet al.,2009). If productivity islower, then a larger land area would be required to meetspeciﬁc targets, and it is more likely there will beconﬂicts with other landscape functions and ecosystemservices (Berndeset al.,2003; Huston & Marland, 2003).Currently, we have limited understanding of theproportion of land covered by biomass crops thatwould signiﬁcantly affect species richness or survival

300J . D A U B E Ret al.of wildlife populations in landscapes. A proportion of10–20% SRC crops in open farmland has been estimatedto be optimal for bird species number (Goransson,�1994). In general, it has been suggested that a thresholdof 20% represents a minimum amount of habitat neededin a landscape, below which effects on populationpersistence become evident (Fahrig, 1998). For example,it has been shown that proportion of parasitism of rapepollen beetles drops below a level necessary for efﬁcientbiocontrol of the beetle when the percentage of noncroparea drops below 20% (Tscharntkeet al.,2002). Observa-tions of limiting thresholds of habitat cover exist forvarious species groups (e.g. Garaffaet al.,2009; Utzet al.,2009). Therefore, future studies should verifywhether such thresholds apply for perennial grassplantations or SRC cropping systems.Habitat heterogeneity of a landscape, in the light ofbiomass crop cultivation, depends not only on theproportion and the diversity of the crops but also onthe turnover of the biomass crop ﬁelds. Owing to thelong rotation periods of 20 plus years, the 2–3 yearestablishment phases of perennial grasses during whichthe ﬁelds are patchy in terms of crop development andthe 3–5 year harvest cycles of SRC crops, biomass cropsprovide transitional habitats which vary considerably invegetation structure and habitat quality. When plantingand harvesting is done asynchronously on a landscape-wide rotating routine, the resulting spatio-temporalmosaic of sites could provide high structural diversityfor a variety of species (Sage & Robertson, 1996; Tolbert& Wright, 1998; Borjesson, 1999; Smeetset al.,2009). An�irregular harvest pattern of switchgrass ﬁelds, for ex-ample, provides habitat for a larger number of birdspecies than if all ﬁelds are harvested simultaneously(Rothet al.,2005). Large-scale SRC plantations contain-ing ﬁelds of different age classes and a variety of cropspecies or clones support a more diverse community ofspecies (Sage & Robertson, 1996; Dhondtet al.,2007;Baumet al.,2009). Furthermore, cultivating a variety ofenergy feedstock could increase habitat diversity inagricultural landscapes and enhance arthropod-mediated ecosystem services (Landiset al.,2008).Biomass crops, in particular SRC crops with highvegetation ﬁlter potential, could be planted as bufferstrips along streams or other (semi-) aquatic habitats tomaintain good water quality and hence aquatic biodi-versity in agriculturally dominated landscapes (Abra-hamsonet al.,1998; Borjesson, 1999). As about 70% of�the water’s nitrogen content is estimated to be remo-vable by willow strips of 25–50 m width, a 50 m widebuffer, where half of the width is harvested at a time,could provide a continuous high uptake of nutrients(Berndeset al.,2008). This service of water puriﬁcationcould; however, compete with the conservation value ofsome riparian sites which is linked with the openness ofthe habitat (Berg, 2002).SRC crops could also be planted along sharp edgesbetween coniferous plantations and open farmlandwhere they function as ecotones in order to increasethe complexity of the forest margins (Berg, 2002). Incontrast, plantations in forest-dominated landscapescould have negative effects, since the mosaic structureof open and forest habitats, which is positive for mostfarmland birds, would disappear, and only a few forestbird species are favoured by SRC plantations (Berg,2002). To improve quality of remnants of natural habi-tats for native wildlife, perennial biomass crops couldalso be integrated with annual crops as buffers aroundnatural areas or woody crops around forest remnants(Cook & Beyea, 2000). Suggestions that SRC plantationsmight enhance connectivity of forest habitats should betreated with caution because SRC plantations do notrepresent forest habitat for many taxa and better evi-dence of their use as dispersal corridors would beneeded (Christianet al.,1997). Porteret al.(2009) sug-gest using biomass belts, i.e. 11 m wide rows of clonallymixed fast-growing bush willows (Salix spp.) with tworows of alder trees (Alnusrubrawhich ﬁxes N) on oneside and two rows of hazel bushes (Corylus spp. whichare attractive to predatory insects) on the other side, toincrease ecosystem services such as biological pestcontrol in arable crop/pasture systems. The biodiver-sity value of such biomass belts would have to becompared with the value of traditional hedgerows ifthey were to replace them. Such mapping exercises ofbiomass crop positioning are however only realistic ifthe demand from biomass crops for land area wouldallow an integration of biomass crops into landscapesand not dictate an overall conversion of land to biomasscrops as discussed in the following section on regionaleffects.

BIOMASS CROPS AND BIODIVERSITYhigh-quality land for agricultural production is limited,energy crops will most likely compete with food andfeed production, urban development, forestry and nat-ure conservation (Salaet al.,2009). The potential offuture biomass production and distribution has beencalculated based on various combinations of feedstockand materials, socio-economic and land-cover scenariosand future climate conditions resulting in a wide rangeof estimates (Berndeset al.,2003; van Damet al.,2007;Bustamanteet al.,2009). No matter which estimate ofthe extent of biomass crop development is correct, evenmeeting the lowest targets would result in majorchanges of land use (Hellmann & Verburg, 2010).According to modelling approaches conducted at thescale of European biogeographical regions and based onland-use sensitivity of a set of 754 species, comprisingmammals, reptiles, amphibians, birds, butterﬂies andvascular plants (Eggerset al.,2009; Louetteet al.,2010),large-scale woody biomass crop production may have anegative net effect on the species considered (Louetteet al.,2010). In this analysis, the individual speciesgroups did show considerable differences in their re-sponse to the assumed land-use change, with negativeeffects being strongest for reptiles, butterﬂies and birds,whereas plant species would proﬁt from the biomasscrop production (Louetteet al.,2010). These results haveto be interpreted with caution because the generalizedand coarse-scale approach chosen can only report rela-tively broad impact patterns. The major impacts andpressures of biomass-induced land-use change willhowever operate on the ﬁner spatial scales of land-scapes or regions and therefore such modelling ap-proaches would have to be down-scaled in order tobecome more accurate by taking patterns of spatialdistribution of biomass plantations and habitat replace-ment in the regions and the associated ecological pro-cesses into account.When utilizing biomass feedstock for coﬁring forexample, locations of existing power plants, distanceto markets or heat generating facilities, minimization oftransport distances to maximize the economic beneﬁt ofthe crop and the net reductions of GHG emissions,create economic pressures for processing or combustionplants to be surrounded by large areas of biomassfeedstock (RCEP, 2004; Anderson & Fergusson, 2006).This could result in a spatial aggregation of energy cropplantations in regions providing appropriate infrastruc-tural conditions (Hellmann & Verburg, 2010).The distances for economic collection of biomasscrops range from 45 to 90 km for SRC willow and30 km forMiscanthus(RCEP, 2004). Consequently, thisis reﬂected in the UK grant funding for biomass cropcultivation, which speciﬁes that the crops should begrown within 40 km of the end user (Wildlife & Coun-r2010 Blackwell Publishing Ltd,GCB Bioenergy,2,289–309

tryside Link, 2007). Examples for such aggregationprocesses are 1300 ha of SRC established in a 75 kmradius of a biomass gasiﬁcation plant close to York inthe UK (Pitcher & Everard 2001) and 16 000 ha of willowSRC in the vicinity of four coal-ﬁred power plants in thestate of New York in the USA (Dhondtet al.,2007).According to Grahamet al.(1996), an efﬁcient biomasspower plant would require between 200 and 400 ha ofbiomass crops (depending on the yield) per MW ofbaseload power. A 2000 MW power station coﬁring25% of its fuel from dedicated energy crops, at currentyields of SRC willow in the United Kingdom, wouldrequire the willow biomass from ca. 1500 ha of land(RCEP, 2004). Given an approximate farm size of 150 hafor mixed farms in the United Kingdom, this wouldequal a total of 10 farms in the vicinity of the powerplant to convert all their land to SRC plantations. InFinland, farmers have entered into contracts withpower plants to grow reed canary grass for coﬁring. Asurvey of 74 farms (i.e. 47% of all contracted farms)showed that on average an area of 14 ha, being morethan one-third of the ﬁelds on a farm, were planted withreed canary grass and maximum transport distance ofthe crop was 80 km (Pahkalaet al.,2008).These trends of centralized biomass crop cultivationcould result in large-scale monocultures in the mostsuitable locations and a segregation of landscapes forenergy production from landscapes for food productionand landscapes for nature conservation. Given such ascenario, ideas for strategic landscape design, usingbiomass crops as elements to increase structural diver-sity (Bellamyet al.,2009), ecotones or buffer zones toimprove landscape quality for wildlife would be futile.Whether biomass crops have signiﬁcant potential to beintegrated into multifunctional landscapes that simul-taneously advance production, conservation and liveli-hood goals (Berndeset al.,2008; Porteret al.,2009)depends on the markets and the structure of the infra-structure involved. One way to integrate biomass cropsinto agricultural landscapes is in the context of small-holder production for local use (Milderet al.2008) andthe development of local markets (Andersonet al.,2004). Efforts are underway at the US Department ofAgriculture to evaluate biomass crops as an alternativeto Conservation Reserve Program (CRP) set-asides(Cook & Beyea, 2000) and it might be worthwhile takingthem into consideration in the framework of agri-environment schemes in the EU as well to encouragesmaller plantings, the splitting of blocks by rides andhedges, and rotational harvesting in mixed age-classblocks (Sageet al.,2006). A scenario of land segregationbetween intensive food production, intensive biomasscrop production, urban development and natureconservation, reduced to whatever land is left, would

302J . D A U B E Ret al.be a worst case situation for biodiversity. There isroom for a rational and efﬁcient use of biomass at therural level and research into prospects of biomassproduction should be based on holistic and multiscaleapproaches.Application of wastewater or other waste materialsto the crops must comply with the nutrient uptakeof the crop variety, the soil and hydrological situa-tion of the site.Efforts of farmers for biodiversity friendly productionof biomass crops have to be supported by policy ma-kers, landscape planners and by further research. Astrategic regional speciﬁc landscape planning would bedesirable to locate biomass plantations in such a waythat they maximize variation in habitat type and canfunction as buffer, corridor or stepping stone habitat.This would have to go hand in hand with research onplantation–landscape interactions. Furthermore, re-search needs to investigate production methods thatmay enhance biodiversity and ecosystem services overtime. Also impacts of secondary land-use of biomasscrops such as waste application would require a betterknowledge-base so that speciﬁc local management re-commendations could be provided.Developing strategies for the landscape and regional scale.Amatter of particular concern is the likelihood of large-scale land-use change induced by bioenergyproduction. A general recommendation is therefore toselect feedstock with high conversion efﬁciencies tominimize land area needed to produce biofuels andonly produce feedstock that are proven to be net carbonneutral or that sequester carbon (Groomet al.,2008). Asstated before, the primary target of bioenergyproduction is, or should be, climate change mitigation.From a biodiversity conservation perspective, thereason behind this is that climate change is expectedto drive a large number of species into extinction(Pimm, 2008). The dilemma that biodiversityconservation is facing with bioenergy production isthat either species could be lost due to climate changemitigation actions now, if biodiversity friendlycultivation of energy crops is not applied or is notpossible, or species are lost later due to climatechange if the mitigation was not successful becauseproduction necessary to reduce GHG emissions wasnot achieved. It is therefore important for biodiversityresearchers to work closely together with otherdisciplines and decision makers to turn a potential lose–lose into a win–win situation. Given the importance ofclimate change mitigation, but also the extent of theimpacts of bioenergy production, society can neitherafford nor accept impacts of bioenergy cultivation gonewrong (Tilmanet al.,2009). The challenge for scientists isto investigate the potentials and risks of bioenergyand for decision makers to give consideration torecommendations in order to implement policies andencourage developments that ensure the full potentialr2010 Blackwell Publishing Ltd,GCB Bioenergy,2,289–309

Strategies for biodiversity friendly energy crop productionWith policy-makers deciding on targets to increase theproduction and use of biomass resources before soundscientiﬁc knowledge about the risks of bioenergy pro-duction are understood (Florin & Bunting, 2009), thereis an urgent need for recommendations on sustainableand biodiversity friendly production of biomass cropswhich range from the ﬁeld via the landscape andregional scale to national and international policy level.Recommendations for the ﬁeld scale.Based on theknowledge gained from studies undertaken at theﬁeld scale, several publications list recommendationsfor biodiversity friendly and sustainable bioenergyproduction (e.g. Sage, 1998; Firbank, 2008; Groomet al.,2008; Baumet al.,2009; Roweet al.,2009).General guidelines for biomass production addressingin particular farm- and ﬁeld-scale management are:Grow energy crops that require low fertilizer, pes-ticide, and energy inputs in most settings (i.e.biomass crops such as SRC crops or perennialgrasses).Minimize pesticide impacts on the nontarget inver-tebrate population and promote biocontrol agents.Grow native species or varieties.Promote polyculture and/or use a mix of varieties(preferably of different gender and different growthstructure) to increase within crop heterogeneity.Use willow clones with a range of ﬂowering times topromote resource availability for ﬂower visitinginsects.Design plantations with large edge to interior ratioand incorporate rides and headland of at least 6 m inwidth.Introduce nectar sources into rides and headlandsfor ﬂower-visiting insects.Intersperse blocks of biomass crops with otherfarmed habitats and keep plots’ size below 15 ha.In large plantations, apply varying harvest cycles toindividual plots and establish plots in different yearsto diversify the age structure (mixed-age stands).Encourage growth of weed species in crops after theestablishment phase of the crop.

BIOMASS CROPS AND BIODIVERSITYof bioenergy is realized without causing the associatedrisks to occur (Florin & Bunting, 2009).In contrast to the ﬁeld scale, no clear-cutrecommendations for coarse scale management ofbiomass cultivation exist. As the perspectives of biomassproduction are varied across regions of Europe and NorthAmerica, it will not be possible to apply a ‘one size ﬁts all’approach. In intensive agricultural regions for instance,introduction of biomass crops will most likely not imposeadditional pressures on biodiversity (Biemanset al.,2008),but might even improve their state. In high nature valuefarming systems, which are characterized by lowintensity farming and high abundance of abandonedland (EEA, 2004), biomass production could in contrastpose a signiﬁcant threat to biodiversity (Biemanset al.,2008; Hellmann & Verburg, 2010). Nevertheless,production of biomass crops or use of biomass fromexisting low-input grasslands could also potentiallystimulate the economic proﬁtability of farming withinmarginal regions and hence beneﬁt biodiversity bycounteracting abandonment of farming and loss of highnature value habitats (e.g. Hennenberget al.,2009).Restoration of highly degraded land through productionof biomass crops (Groomet al.,2008) as well as payinglandowners to maintain environmentally sensitive landout of row crop production and under permanent grasscover and harvesting biomass from those lands mightprovide environmental beneﬁts (Paineet al.,1996).Biodiversity beneﬁts will only arise as long assustainability principles are applied and novel farmingactivities are compliant with the overall conservationvision for the respective regions (Biemanset al.,2008).As the existence of the vast majority of species,including endangered species, at least within Europe,depends on areas managed for agriculture and forestry(Tscharntkeet al.,2005), prohibiting bioenergy productionin protected and nature conservation areas alone wouldnot be sufﬁcient as a strategy to prevent negative effectsof biomass crop cultivation on biodiversity at thelandscape or regional scale. Strategies for sustainablecultivation of biomass crops within productionlandscapes are therefore needed. An important questionin this context, that needs to be addressed by research, isto what degree is biomass production in a certain arearelated to the (potential) biodiversity value of the samearea if reserved for nature or managed by high naturevalue farming (Dornburget al.,2010)?One of the essential prerequisites for formulatingrecommendations are assessments of realistic capacitiesof landscapes to produce domestic bioenergy feedstockfor bioenergy and to avoid over-optimistic projectionsabout the potential contribution of biomass to theenergy mix (Florin & Bunting, 2009). Biemanset al.(2008) recommended making land inventories whichr2010 Blackwell Publishing Ltd,GCB Bioenergy,2,289–309

explore the opportunities and necessary restrictionsconcerning the cultivation of biomass for bioenergypurposes. Equally important for projecting futureregional distribution of biomass crops is an under-standing of the development of the bioenergy marketsand the context of energy production, i.e., smallholderproduction for local use as against large-scale centralizedproduction for transregional use. Cross-disciplinaryresearch, development of environmental metrics, closingthe knowledge gaps regarding positive or negativeimpacts on biodiversity and integrated modellingapproaches are necessary to evaluate sustainability andeconomic and environmental tradeoffs (Graham, 2007;Firbank, 2008; Groomet al.,2008).The national and international policy dimension.If the fullpotential of bioenergy is to be realized without causingthe associated risks to biodiversity and the environmentto occur, there is a pressing need to better understandthe full environmental impact throughout the life cycleof bioenergy utilization (Florin & Bunting, 2009;Hennenberget al.,2009). Given the shortcomings ofexisting sustainability standards in Europe and theUSA (see Hennenberget al.,2009 for an overview)development and implementation of mandatorystandards and certiﬁcation systems are needed.However, for the coarse scale impacts in particular,signiﬁcant uncertainties exist. Risk-based approachesto decision-making, full life-cycle assessments (LCA)or environmental impact assessments (EIA) to assessthe net direct and indirect impacts of land-use changecould be helpful tools for the development of legallybinding regulations (Firbank, 2008; Biemanset al.,2008;Florin & Bunting, 2009). As impacts of energy cropproduction vary on spatial scales ﬁner than the onesusually considered in LCAs, some challenges regardingthe implementation of spatially explicit information inorder to integrate biodiversity aspects into LCAs haveto be overcome (Urbanet al.,2008). To meet thosechallenges and to reduce uncertainties, biodiversityresearch has to contribute knowledge to the riskassessment and decision-making process. In order tomake risk and/or sustainability assessments ofbioenergy production operable, it is crucial to identifycritical criteria, but at the same time keep the numberand measurement at a reasonable level (Donnellyet al.,2006; Buchholzet al.,2009). Otherwise, the aim tointegrate biomass crops into agricultural landscapesfor stimulating beneﬁcial effects on biodiversity andecosystem services might be at risk as small andindependent producers could be locked out and themarket for sustainable biofuels would be thendominated by international investors, most probablyresulting in large-scale plantations (Zahet al.,2009).

304J . D A U B E Ret al.Existing subsidy programmes and incentives forbioenergy and for agri-environment schemes need tobe re-evaluated and perhaps integrated for the purposeof sustainable energy crop production (Paineet al.,1996). The efﬁciency of standards, when appliedvoluntarily or only referring to cross-compliance andgood agricultural practice, have fundamental limits intheir contribution to sustainable production and instopping the loss of biodiversity in agriculturalproduction areas (Henleet al.,2008; Kaphengstet al.,2009). Therefore, governance structures that set clearrules and incentives for biomass crop production anduse of natural resources are essential for a moresustainable development (Kaphengstet al.,2009). Atthe same time, risk-mitigation strategies should ideallyremain ﬂexible with regard to the various geographicalpeculiarities, feedstock produced and technologiesapplied and should use the principles of adaptivemanagement so that policies can be revised as newscientiﬁc knowledge emerges (Florin & Bunting, 2009;Hennenberget al.,2009).crop production. Taking regional peculiarities into ac-count, risk assessment would have to include coarsescale ecological patterns and processes. To facilitate this,interdisciplinary research and integrated modelling ofenvironmental and economic issues would be necessaryto formulate standards that help to support long-termeconomic and ecological sustainability of bioenergyproduction and to avoid costly mistakes in our attemptsto mitigate global climate change.

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