Foraging guild modulates insectivorous bat responses to habitat loss and insular fragmentation in peninsular Malaysia

Despite mounting evidence on the ecological impacts of damming for biodiversity, little is known regarding its consequences in the hyper-diverse Southeast Asian tropical forests. Here we assess the effects of habitat loss and fragmentation on the diversity and activity of insectivorous bats within the hydroelectric Kenyir Lake in peninsular Malaysia. We surveyed bat assemblages on 26 islands and two mainland continuous forest sites using passive acoustic monitoring. Echolocation calls were classified into sonotypes, each corresponding to either one or multiple species, and grouped into foraging guilds. We then examined bat overall assemblage (sonotype richness, activity, and composition), guild- and sonotype-specific activity. From 9360 hours of recordings, we identified 16 bat sonotypes, including 10 forest (2854 bat passes), three edge (13 703) and three open-space foragers (3651). Sonotype richness increased towards denser forest structures (higher Normalized Difference Vegetation Index - NDVI), while species composition varied across the gradient of forest area. Forest foragers were positively affected by NDVI and negatively affected by distance to the closest neighbour, whereas edge foragers’ activity increased in smaller islands. Of the six sonotypes analysed, the activity of one forest sonotype increased with forest area, while that of one edge sonotype decreased. Ensuring habitat quality within insular forest remnants, in addition to their functional connectivity, maximises bat diversity, including the persistence of forest foraging species. Future hydropower development should therefore avoid the creation of a myriad of small, isolated, and habitat-degraded islands further characterised by altered levels of bat diversity and guild-level activity. Highlights We assessed the diversity of insectivorous bats in dam-induced islands in Malaysia Species persistence was modulated by island size and habitat quality Forest foragers were negatively affected by island isolation and degradation Edge foragers benefited from fragmentation, increasing in activity on smaller islands By creating multiple small, isolated, degraded islands, damming erodes bat diversity

[1]  C. Peres,et al.  Emergent properties of species-habitat networks in an insular forest landscape , 2022, Science advances.

[2]  C. Voigt,et al.  Activity of forest specialist bats decreases towards wind turbines at forest sites , 2022, Journal of Applied Ecology.

[3]  C. Peres,et al.  Functional diversity and trait filtering of insectivorous bats on forest islands created by an Amazonian mega dam , 2022, Functional Ecology.

[4]  C. Peres,et al.  Invasive rat drives complete collapse of native small mammal communities in insular forest fragments , 2022, Current Biology.

[5]  C. Peres,et al.  Habitat Quality, Not Patch Size, Modulates Lizard Responses to Habitat Loss and Fragmentation in the Southwestern Amazon , 2022, Journal of Herpetology.

[6]  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.

[7]  Jake E. Bicknell,et al.  A machine learning framework to classify Southeast Asian echolocating bats , 2022, Ecological Indicators.

[8]  Sándor Zsebők,et al.  ChiroVox: a public library of bat calls , 2022, PeerJ.

[9]  T. Aide,et al.  The effect of artificial light on bat richness and nocturnal soundscapes along an urbanization gradient in an arid landscape of central Peru , 2021, Urban Ecosystems.

[10]  D. Armstrong,et al.  Using experimental reintroductions to resolve the roles of habitat quality and metapopulation dynamics on patch occupancy in fragmented landscapes , 2021, Conservation biology : the journal of the Society for Conservation Biology.

[11]  P. Ding,et al.  Passive acoustic monitoring reveals the role of habitat affinity in sensitivity of sub‐tropical East Asian bats to fragmentation , 2021, Remote Sensing in Ecology and Conservation.

[12]  C. Peres,et al.  Avian extinctions induced by the oldest Amazonian hydropower mega dam: evidence from museum collections and sighting data spanning 172 years , 2021, PeerJ.

[13]  C. Peres,et al.  Forest area predicts all dimensions of small mammal and lizard diversity in Amazonian insular forest fragments , 2021, Landscape Ecology.

[14]  C. Peres,et al.  Phylogenetic homogenization of Amazonian tree assemblages in forest islands after 26 years of isolation , 2021, Applied Vegetation Science.

[15]  J. M. Palmeirim,et al.  Optimising bat bioacoustic surveys in human-modified neotropical landscapes. , 2021, Ecological applications : a publication of the Ecological Society of America.

[16]  Indrajeet Patil,et al.  performance: An R Package for Assessment, Comparison and Testing of Statistical Models , 2021, J. Open Source Softw..

[17]  Y. Bas,et al.  An automatic classifier of bat sonotypes around the world , 2021, Methods in Ecology and Evolution.

[18]  C. Peres,et al.  Using Relict Species–Area Relationships to Estimate the Conservation Value of Reservoir Islands to Improve Environmental Impact Assessments of Dams , 2021, The Species–Area Relationship.

[19]  G. Kerth,et al.  Consequences of fragmentation for Neotropical bats: The importance of the matrix , 2020 .

[20]  C. Peres,et al.  Determinants of population persistence and abundance of terrestrial and arboreal vertebrates stranded in tropical forest land‐bridge islands , 2020, Conservation biology : the journal of the Society for Conservation Biology.

[21]  V. D. Chamizo,et al.  Spatial Orientation , 2019, Encyclopedia of Animal Cognition and Behavior.

[22]  L. C. Terribile,et al.  Effects of landscape and patch attributes on the functional diversity of medium and large-sized mammals in the Brazilian Cerrado , 2019, Mammal Research.

[23]  Jakub Nowosad,et al.  landscapemetrics : an open‐source R tool to calculate landscape metrics , 2019, Ecography.

[24]  T. Kingston,et al.  Echolocation and roosting ecology determine sensitivity of forest‐dependent bats to coffee agriculture , 2019, Biotropica.

[25]  Alice C Hughes,et al.  Top 100 research questions for biodiversity conservation in Southeast Asia , 2019, Biological Conservation.

[26]  Shengwen Tang,et al.  Current and future hydropower development in Southeast Asia countries (Malaysia, Indonesia, Thailand and Myanmar) , 2019, Energy Policy.

[27]  I. Saiful,et al.  Canopy gap dynamics and effects of selective logging: a study in a primary hill dipterocarp forest in Malaysia , 2019, JOURNAL OF TROPICAL FOREST SCIENCE.

[28]  T. Maraseni,et al.  Evolutionary dynamics of selective logging in the tropics: A systematic review of impact studies and their effectiveness in sustainable forest management , 2018, Forest Ecology and Management.

[29]  Kate E. Jones,et al.  Emerging opportunities and challenges for passive acoustics in ecological assessment and monitoring , 2018, Methods in Ecology and Evolution.

[30]  M. Abdullah,et al.  Checklist of Small Mammals of Hulu Terengganu, Terengganu , 2018, Greater Kenyir Landscapes.

[31]  T. Fartmann,et al.  Patch occupancy of grassland specialists: Habitat quality matters more than habitat connectivity , 2018, Biological Conservation.

[32]  C. F. Meyer,et al.  The importance of lakes for bat conservation in Amazonian rainforests: an assessment using autonomous recorders , 2018 .

[33]  C. Peres,et al.  Small mammal responses to Amazonian forest islands are modulated by their forest dependence , 2018, Oecologia.

[34]  Julian D. Olden,et al.  Global proliferation of small hydropower plants – science and policy , 2018 .

[35]  Marcela Suarez-Rubio,et al.  Insectivorous bats respond to vegetation complexity in urban green spaces , 2018, Ecology and evolution.

[36]  Danilo Russo,et al.  Bats are still not birds in the digital era: echolocation call variation and why it matters for bat species identification , 2018 .

[37]  Alex Rogers,et al.  AudioMoth: Evaluation of a smart open acoustic device for monitoring biodiversity and the environment , 2018 .

[38]  W. Laurance,et al.  How Green is 'Green' Energy? , 2017, Trends in ecology & evolution.

[39]  C. Peres,et al.  Non-random lizard extinctions in land-bridge Amazonian forest islands after 28 years of isolation , 2017 .

[40]  Izaya Numata,et al.  Landsat-based analysis of mega dam flooding impacts in the Amazon compared to associated environmental impact assessments: Upper Madeira River example 2006–2015 , 2017 .

[41]  J. M. Palmeirim,et al.  Consequences of a large-scale fragmentation experiment for Neotropical bats: disentangling the relative importance of local and landscape-scale effects , 2016, Landscape Ecology.

[42]  C. Peres,et al.  Extinction debt on reservoir land-bridge islands , 2016 .

[43]  H. Jactel,et al.  Bat and bird diversity along independent gradients of latitude and tree composition in European forests , 2016, Oecologia.

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

[45]  K. Y. Foo A vision on the opportunities, policies and coping strategies for the energy security and green energy development in Malaysia , 2015 .

[46]  J. Petinrin,et al.  Renewable energy for continuous energy sustainability in Malaysia , 2015 .

[47]  M. Willig,et al.  Responses of Tropical Bats to Habitat Fragmentation, Logging, and Deforestation , 2015, Bats in the Anthropocene: Conservation of Bats in a Changing World.

[48]  C. Peres,et al.  Predicting local extinctions of Amazonian vertebrates in forest islands created by a mega dam , 2015 .

[49]  T. Sattler,et al.  Mobility explains the response of aerial insectivorous bats to anthropogenic habitat change in the Neotropics , 2015 .

[50]  C. Peres,et al.  Edge‐mediated compositional and functional decay of tree assemblages in Amazonian forest islands after 26 years of isolation , 2015 .

[51]  Z. Buřivalová,et al.  Thresholds of Logging Intensity to Maintain Tropical Forest Biodiversity , 2014, Current Biology.

[52]  S. Rossiter,et al.  Diversity of Malaysian insectivorous bat assemblages revisited , 2014, Journal of Tropical Ecology.

[53]  M. Fortin,et al.  EDITOR'S CHOICE: Stepping stones are crucial for species' long‐distance dispersal and range expansion through habitat networks , 2014 .

[54]  M. Struebig,et al.  Quantifying the Biodiversity Value of Repeatedly Logged Rainforests: Gradient and Comparative Approaches from Borneo , 2013 .

[55]  William F. Laurance,et al.  Near-Complete Extinction of Native Small Mammal Fauna 25 Years After Forest Fragmentation , 2013, Science.

[56]  Hans-Ulrich Schnitzler,et al.  Bat guilds, a concept to classify the highly diverse foraging and echolocation behaviors of microchiropteran bats , 2013, Front. Physiol..

[57]  J. Mora Bats, from Evolution to Conservation , 2011 .

[58]  T. Lee,et al.  Dung beetle assemblages on tropical land‐bridge islands: small island effect and vulnerable species , 2011 .

[59]  Ivette Perfecto,et al.  Ensemble Composition and Activity Levels of Insectivorous Bats in Response to Management Intensification in Coffee Agroforestry Systems , 2011, PloS one.

[60]  L. P. Koh,et al.  Do insectivorous bird communities decline on land-bridge forest islands in Peninsular Malaysia? , 2010, Journal of Tropical Ecology.

[61]  Matthew E. Watts,et al.  Conserving biodiversity in production landscapes. , 2010, Ecological applications : a publication of the Ecological Society of America.

[62]  E. Kalko,et al.  Assemblage‐level responses of phyllostomid bats to tropical forest fragmentation: land‐bridge islands as a model system , 2008 .

[63]  Stephen J. Rossiter,et al.  Conservation value of forest fragments to Palaeotropical bats , 2008 .

[64]  I. Cuthill,et al.  Effect size, confidence interval and statistical significance: a practical guide for biologists , 2007, Biological reviews of the Cambridge Philosophical Society.

[65]  E. Kalko,et al.  Ecological correlates of vulnerability to fragmentation in Neotropical bats , 2007 .

[66]  Anne-Béatrice Dufour,et al.  The ade4 Package: Implementing the Duality Diagram for Ecologists , 2007 .

[67]  J. Malcolm,et al.  Effects of Selective Logging on Bat Communities in the Southeastern Amazon , 2006, Conservation biology : the journal of the Society for Conservation Biology.

[68]  M. Saleem Environmental Issues in a Federation: The Case of Malaysia , 2005 .

[69]  L. P. Koh,et al.  Southeast Asian biodiversity: an impending disaster. , 2004, Trends in ecology & evolution.

[70]  G. Kerth,et al.  A Comparative Analysis of Specialization and Extinction Risk in Temperate‐Zone Bats , 2004 .

[71]  M. Willig,et al.  LANDSCAPE RESPONSES OF BATS TO HABITAT FRAGMENTATION IN ATLANTIC FOREST OF PARAGUAY , 2004 .

[72]  H. Schnitzler,et al.  From spatial orientation to food acquisition in echolocating bats , 2003 .

[73]  David R. Anderson,et al.  Model Selection and Multimodel Inference , 2003 .

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

[75]  B. Harvey,et al.  Effects of mechanized careful logging on natural regeneration and vegetation competition in the southeastern Canadian boreal forest , 2002 .

[76]  Kevin McGarigal,et al.  COMPARATIVE EVALUATION OF EXPERIMENTAL APPROACHES TO THE STUDY OF HABITAT FRAGMENTATION EFFECTS , 2002 .

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

[78]  J. Hayes,et al.  Temporal Variation in Activity of Bats and the Design of Echolocation-Monitoring Studies , 1997 .

[79]  D A Waters,et al.  Echolocation call structure and intensity in five species of insectivorous bats. , 1995, The Journal of experimental biology.

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

[81]  M. Brock Fenton,et al.  A technique for monitoring bat activity with results obtained from different environments in southern Ontario , 1970 .

[82]  R. Macarthur,et al.  The Theory of Island Biogeography , 1969 .

[83]  Dung Beetle , 2021, Encyclopedia of Social Insects.

[84]  Mohamed,et al.  Greater Kenyir Landscapes: Social Development and Environmental Sustainability: From Ridge to Reef , 2019 .

[85]  D. Yong PERSISTENCE OF PRIMATE AND UNGULATE COMMUNITIES ON FORESTED ISLANDS IN LAKE KENYIR IN NORTHERN PENINSULAR MALAYSIA , 2016 .

[86]  J. M. Palmeirim,et al.  Consequences of a large-scale fragmentation experiment for Neotropical bats: disentangling the relative importance of local and landscape-scale effects , 2016, Landscape Ecology.

[87]  Damaris Zurell,et al.  Collinearity: a review of methods to deal with it and a simulation study evaluating their performance , 2013 .

[88]  T. Kingston Response of Bat Diversity to Forest Disturbance in Southeast Asia: Insights from Long-Term Research in Malaysia , 2013 .

[89]  C. L. Meneses-Tovar NDVI as indicator of degradation , 2012 .

[90]  Roy Want,et al.  How Green Is Green? , 2009, IEEE Pervasive Comput..

[91]  T. Kingston Research priorities for bat conservation in Southeast Asia: a consensus approach , 2008, Biodiversity and Conservation.

[92]  R. Axelrod,et al.  Evolutionary Dynamics , 2004 .

[93]  J. Terborgh,et al.  1 Maintenance of Tree Diversity in Tropical Forests , 2002 .

[94]  J. Hayes,et al.  Assumptions and practical considerations in the design and interpretation of echolocation-monitoring studies , 2000 .

[95]  Gregory Taylor,et al.  Current and future , 1998 .

[96]  RockOn Team,et al.  Re: Attenuation compensation in single-photon emission tomography: a comparative evaluation. , 1983, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[97]  Gareth Jones,et al.  ECHOLOCATION CALL STRUCTURE AND INTENSITY IN , 1994 .