Structurally rich dry grasslands – Potential stepping stones for bats in open farmland

Agricultural intensification has caused decrease and fragmentation of European semi-natural dry grasslands. While a high biodiversity value of dry grasslands is acknowledged for plants and insects, locally and on landscape level, their relevance for mobile species, such as bats, is unknown. Here we investigate the use of dry grassland fragments by bats in an agriculturally intensified region in Germany and evaluate local and landscape factors influencing bat activity and assemblages. Specifically, we predicted that a combination of local dry grassland structural richness and landscape features as well as their interactions affect bat activity and foraging above dry grasslands. We also expected that these features influence compositions of local bat assemblages. We repeatedly sampled at 12 dry grassland plots with acoustic monitoring and assessed activity and foraging of bat species/sonotypes, which we grouped into guilds known for foraging in open land, at vegetation edges and in narrow spaces. We determined structural richness of the dry grassland plots in field and derived landscape features from digital landscape data. A relatively high proportion of bat species/sonotypes used dry grasslands regularly. The edge space foragers responded positively to higher local structural richness. Their dry grassland use increased when surrounding forests and woody features were less available, but they foraged more on dry grasslands closer to water bodies. Narrow space bat activity on dry grasslands decreased with less landscape connectivity. Open and narrow space foragers responded to local structural richness only in landscape context. For all bat guilds we found increased use of structurally richer dry grasslands when there was more open farmland in the surroundings. This was also the case for edge space foragers, when landscapes were more homogeneous. Lastly, with increasing structural richness, bat assemblages were more dominated by edge space foragers. We show the importance of European dry grassland fragments for the highly mobile group of bats under certain local structural and landscape compositional conditions. Our results underline the value of heterogeneous dry grassland fragments as potential stepping stones in intensively used farmland areas and contribute to evidence based decision making in dry grassland management and bat conservation.

[1]  Kirsty J. Park,et al.  Tree size, microhabitat diversity and landscape structure determine the value of isolated trees for bats in farmland , 2022, Biological Conservation.

[2]  R. Wolf Rezension von: Rote Liste und Gesamtartenliste der Säugetiere (Mammalia) Deutschlands , 2021, Schwäbische Heimat.

[3]  Jacqueline Loos,et al.  Local and landscape responses of biodiversity in calcareous grasslands , 2021, Biodiversity and Conservation.

[4]  Ella Browning,et al.  Drivers of European bat population change: a review reveals evidence gaps , 2021, Mammal Review.

[5]  P. Raven,et al.  Agricultural intensification and climate change are rapidly decreasing insect biodiversity , 2021, Proceedings of the National Academy of Sciences.

[6]  B. Deák,et al.  Fragmented dry grasslands preserve unique components of plant species and phylogenetic diversity in agricultural landscapes , 2020, Biodiversity and Conservation.

[7]  L. Fahrig,et al.  Bats respond negatively to increases in the amount and homogenization of agricultural land cover , 2019, Landscape Ecology.

[8]  N. Buchmann,et al.  Multiple plant diversity components drive consumer communities across ecosystems , 2019, Nature Communications.

[9]  U. Zeller,et al.  Bat Community Responses to Structural Habitat Complexity Resulting from Management Practices Within Different Land Use Types — A Case Study from North-Eastern Germany , 2019, Acta Chiropterologica.

[10]  Unai Pascual,et al.  Summary for policymakers of the global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services-ADVANCE UNEDITED VERSION , 2019 .

[11]  Alexander C. Diener,et al.  Diversity of Flower Visiting Insects in Dry Grasslands and Vineyards Close to the City of Vienna with Special Focus on Wild Bees. , 2018, Sociobiology.

[12]  S. Philpott,et al.  Agroecological farming practices promote bats , 2018, Agriculture, Ecosystems & Environment.

[13]  C. Threlfall,et al.  Trait-dependent tolerance of bats to urbanization: a global meta-analysis , 2018, Proceedings of the Royal Society B: Biological Sciences.

[14]  Amanda E. Martin,et al.  Farmland heterogeneity benefits bats in agricultural landscapes , 2018 .

[15]  K. Jung,et al.  The relevance of vegetation structures and small water bodies for bats foraging above farmland , 2017 .

[16]  Casper W. Berg,et al.  glmmTMB Balances Speed and Flexibility Among Packages for Zero-inflated Generalized Linear Mixed Modeling , 2017, R J..

[17]  K. Jung,et al.  Landscape and scale-dependent spatial niches of bats foraging above intensively used arable fields , 2017, Ecological Processes.

[18]  C. Brühl,et al.  Nocturnal Risks-High Bat Activity in the Agricultural Landscape Indicates Potential Pesticide Exposure , 2017, Front. Environ. Sci..

[19]  Jakub Stoklosa,et al.  Terrestrial laser scanning reveals below-canopy bat trait relationships with forest structure , 2017 .

[20]  V. Nardone,et al.  Effects of free-ranging cattle and landscape complexity on bat foraging: implications for bat conservation and livestock management. , 2017 .

[21]  E. Arnett,et al.  Reducing bat fatalities at wind facilities while improving the economic efficiency of operational mitigation , 2017, Journal of Mammalogy.

[22]  Christoph Leuschner,et al.  Ecology of Central European Non-Forest Vegetation: Coastal to Alpine, Natural to Man-Made Habitats , 2017, Springer International Publishing.

[23]  C. Fonseca,et al.  Bat richness and activity in heterogeneous landscapes: guild-specific and scale-dependent? , 2017, Landscape Ecology.

[24]  R. Dirzo,et al.  Patterns, Causes, and Consequences of Anthropocene Defaunation , 2016 .

[25]  K. Jung,et al.  Seasonal activity patterns of European bats above intensively used farmland , 2016 .

[26]  Christian C. Voigt,et al.  The use of automated identification of bat echolocation calls in acoustic monitoring: A cautionary note for a sound analysis , 2016 .

[27]  M. Tschapka,et al.  The effect of local land use and loss of forests on bats and nocturnal insects , 2016, Ecology and evolution.

[28]  K. Walker,et al.  Agricultural Management and Climatic Change Are the Major Drivers of Biodiversity Change in the UK , 2016, PloS one.

[29]  Florian Zellweger,et al.  From field surveys to LiDAR: Shining a light on how bats respond to forest structure , 2016 .

[30]  Roberto Toffoli The Importance of Linear Landscape Elements for Bats in a Farmland Area: The Influence of Height on Activity , 2016 .

[31]  G. McCracken,et al.  The importance of natural habitats to Brazilian free-tailed bats in intensive agricultural landscapes in the Winter Garden region of Texas, United States , 2015 .

[32]  M. Knörnschild,et al.  The Importance of Landscape Elements for Bat Activity and Species Richness in Agricultural Areas , 2015, PloS one.

[33]  T. Tscharntke,et al.  Biodiversity conservation across taxa and landscapes requires many small as well as single large habitat fragments , 2015, Oecologia.

[34]  J. Liira,et al.  Multi-scale ecology of insectivorous bats in agricultural landscapes , 2015 .

[35]  J. Liira,et al.  Multi-scale ecology of woodland bat the role of species pool, landscape complexity and stand structure , 2015, Biodiversity and Conservation.

[36]  U. Toelch,et al.  Seasonal Bat Activity in Relation to Distance to Hedgerows in an Agricultural Landscape in Central Europe and Implications for Wind Energy Development , 2014 .

[37]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[38]  R. Lindborg,et al.  Function of small habitat elements for enhancing plant diversity in different agricultural landscapes , 2014 .

[39]  T. Wrbka,et al.  Species richness in dry grassland patches of eastern Austria: A multi-taxon study on the role of local, landscape and habitat quality variables , 2014 .

[40]  Hans Pretzsch,et al.  From ground to above canopy—Bat activity in mature forests is driven by vegetation density and height , 2013 .

[41]  J. Dengler,et al.  European grassland ecosystems: threatened hotspots of biodiversity , 2013, Biodiversity and Conservation.

[42]  Kirsty J. Park,et al.  Fragmented woodlands in agricultural landscapes: The influence of woodland character and landscape context on bats and their insect prey , 2013 .

[43]  Volker C. Radeloff,et al.  Image Texture Predicts Avian Density and Species Richness , 2013, PloS one.

[44]  M. Obrist,et al.  Landscape connectivity, habitat structure and activity of bat guilds in farmland-dominated matrices , 2013 .

[45]  Péter Török,et al.  The European Dry Grassland Group (EDGG): stewarding Europe’s most diverse habitat type , 2013 .

[46]  Gareth Jones,et al.  Home range use and habitat selection by barbastelle bats (Barbastella barbastellus): implications for conservation , 2012 .

[47]  J. Hanspach,et al.  Using trait-based filtering as a predictive framework for conservation: a case study of bats on farms in southeastern Australia , 2012 .

[48]  M. Pärtel,et al.  Plant species richness: the world records , 2012 .

[49]  C. Brühl,et al.  Bats at risk? Bat activity and insecticide residue analysis of food items in an apple orchard , 2012, Environmental toxicology and chemistry.

[50]  Jens Nieschulze,et al.  Moving in three dimensions: effects of structural complexity on occurrence and activity of insectivorous bats in managed forest stands , 2012 .

[51]  C. Brühl,et al.  Constructed wetlands support bats in agricultural landscapes , 2012 .

[52]  J. Dengler,et al.  Festuco-Brometea communities of the Transylvanian Plateau (Romania) - a preliminary overview on syntaxonomy, ecology, and biodiversity , 2012 .

[53]  M. D. Dixon Relationship between land cover and insectivorous bat activity in an urban landscape , 2012, Urban Ecosystems.

[54]  T. Hothorn,et al.  Aggregative response in bats: prey abundance versus habitat , 2012, Oecologia.

[55]  P. Dolman,et al.  Effects of landscape-scale broadleaved woodland configuration and extent on roost location for six bat species across the UK , 2011 .

[56]  P. Dolman,et al.  Improving the biodiversity benefits of hedgerows: How physical characteristics and the proximity of foraging habitat affect the use of linear features by bats , 2011 .

[57]  L. Fahrig,et al.  Positive effects of forest fragmentation, independent of forest amount, on bat abundance in eastern Ontario, Canada , 2011, Landscape Ecology.

[58]  B. Law,et al.  A preliminary assessment of the impact of forest thinning on bat activity: Towards improved clutter-based hypotheses , 2011 .

[59]  Nick C. Downs,et al.  Do Bats Forage Over Cattle Dung or Over Cattle? , 2010 .

[60]  Mollie E. Brooks,et al.  Generalized linear mixed models: a practical guide for ecology and evolution. , 2009, Trends in ecology & evolution.

[61]  M. WallisDeVries,et al.  Grasslands as habitats for butterflies in Europe , 2009 .

[62]  J. Vandermeer,et al.  Bats Limit Insects in a Neotropical Agroforestry System , 2008, Science.

[63]  E. Kalko,et al.  Bats Limit Arthropods and Herbivory in a Tropical Forest , 2008, Science.

[64]  Beat Naef-Daenzer,et al.  A predictive model of the density of airborne insects in agricultural environments , 2008 .

[65]  B. Verboom,et al.  The importance of linear landscape elements for the pipistrellePipistrellus pipistrellus and the serotine batEptesicus serotinus , 1997, Landscape Ecology.

[66]  Gareth Jones,et al.  Differential habitat selection by Pipistrellus pipistrellus and Pipistrellus pygmaeus identifies distinct conservation needs for cryptic species of echolocating bats , 2006 .

[67]  Jason W. Horn,et al.  Economic value of the pest control service provided by Brazilian free-tailed bats in south-central Texas , 2006 .

[68]  P. Racey,et al.  The use by bats of habitat features in mixed farmland in Scotland , 2006 .

[69]  D. Lindenmayer,et al.  Biodiversity, ecosystem function, and resilience: ten guiding principles for commodity production landscapes , 2006 .

[70]  E. Kalko,et al.  Gleaning bats as underestimated predators of herbivorous insects: diet of Micronycteris microtis (Phyllostomidae) in Panama , 2005, Journal of Tropical Ecology.

[71]  Carsten Thies,et al.  REVIEWS AND SYNTHESES Landscape perspectives on agricultural intensification and biodiversity - ecosystem service management , 2005 .

[72]  J. P. Grime,et al.  The impacts of agricultural change (1963–2003) on the grassland flora of Central England: processes and prospects , 2005 .

[73]  O. Honnay,et al.  Conservation and restoration of calcareous grasslands: a concise review of the effects of fragmentation and management on plant species , 2005 .

[74]  M. Obrist,et al.  Variability in echolocation call design of 26 Swiss bat species: consequences, limits and options for automated field identification with a synergetic pattern recognition approach , 2004 .

[75]  S. Gehrt,et al.  SPECIES‐SPECIFIC PATTERNS OF BAT ACTIVITY IN AN URBAN LANDSCAPE , 2004 .

[76]  Birgitta Svensson,et al.  Plants, insects and birds in semi-natural pastures in relation to local habitat and landscape factors , 2001, Biodiversity & Conservation.

[77]  C. Weber,et al.  Foraging habitat preferences of bats in relation to food supply and spatial vegetation structures in a western European low mountain range forest , 2004 .

[78]  J. Kusch,et al.  Structure and variability of bat social calls: implications for specificity and individual recognition , 2003 .

[79]  T. Benton,et al.  Farmland biodiversity: is habitat heterogeneity the key? , 2003 .

[80]  M. Obrist,et al.  Regional biodiversity in an agricultural landscape: the contribution of seminatural habitat islands , 2003 .

[81]  Gareth Jones,et al.  Identification of twenty‐two bat species (Mammalia: Chiroptera) from Italy by analysis of time‐expanded recordings of echolocation calls , 2002 .

[82]  P. Poschlod,et al.  The historical and socioeconomic perspective of calcareous grasslands—lessons from the distant and recent past , 2002 .

[83]  Carsten Thies,et al.  CONTRIBUTION OF SMALL HABITAT FRAGMENTS TO CONSERVATION OF INSECT COMMUNITIES OF GRASSLAND–CROPLAND LANDSCAPES , 2002 .

[84]  Rob H. G. Jongman,et al.  Homogenisation and fragmentation of the European landscape: ecological consequences and solutions , 2002 .

[85]  N. Boatman,et al.  Ecological impacts of arable intensification in Europe. , 2001, Journal of environmental management.

[86]  H. Schnitzler,et al.  Echolocation by Insect-Eating Bats , 2001 .

[87]  Brian G. Wolff,et al.  Forecasting Agriculturally Driven Global Environmental Change , 2001, Science.

[88]  Marti J. Anderson,et al.  A new method for non-parametric multivariate analysis of variance in ecology , 2001 .

[89]  Bruce W. Miller,et al.  A method for determining relative activity of free flying bats using a new activity index for acoustic monitoring , 2001 .

[90]  S. Parsons,et al.  Acoustic identification of twelve species of echolocating bat by discriminant function analysis and artificial neural networks. , 2000, The Journal of experimental biology.

[91]  Barry R. Noon,et al.  Biological Corridors: Form, Function, and Efficacy , 1997 .

[92]  W. Parton,et al.  Agricultural intensification and ecosystem properties. , 1997, Science.

[93]  J. Speakman,et al.  Habitat Exploitation by a Gleaning Bat, Plecotus auritus , 1996 .

[94]  M. Brock Fenton,et al.  The foraging behaviour and ecology of animal-eating bats , 1990 .

[95]  Allan R. Wilks,et al.  The new S language: a programming environment for data analysis and graphics , 1988 .

[96]  J. Rayner,et al.  Ecological Morphology and Flight in Bats (Mammalia; Chiroptera): Wing Adaptations, Flight Performance, Foraging Strategy and Echolocation , 1987 .

[97]  H. Aldridge,et al.  Morphology echolocation and resource partitioning in insectivorous bats , 1987 .

[98]  R. Macarthur,et al.  On Bird Species Diversity , 1961 .