CONSERVATION ECOLOGY Extinction filters mediate the global effects of habitat fragmentation on animals Matthew G. Betts 1 *†, Christopher Wolf 1 *†, Marion Pfeifer 2 , Cristina Banks-Leite 3 , Víctor Arroyo-Rodríguez 4 , Danilo Bandini Ribeiro 5 , Jos Barlow 6,7 , Felix Eigenbrod 8 , Deborah Faria 9 , Robert J. Fletcher Jr. 10 , Adam S. Hadley 1 , Joseph E. Hawes 11 , Robert D. Holt 12 , Brian Klingbeil 13 , Urs Kormann 1,14,15 , Luc Lens 16 , Taal Levi 1 , Guido F. Medina-Rangel 17 , Stephanie L. Melles 18 , Dirk Mezger 19 , José Carlos Morante-Filho 9,20 , C. David L. Orme 3 , Carlos A. Peres 21 , Benjamin T. Phalan 22 , Anna Pidgeon 23 , Hugh Possingham 24,25 , William J. Ripple 1 , Eleanor M. Slade 26 , Eduardo Somarriba 27 , Joseph A. Tobias 3 , Jason M. Tylianakis 28 , J. Nicolás Urbina-Cardona 29 , Jonathon J. Valente 1,30 , James I. Watling 31 , Konstans Wells 32 , Oliver R. Wearn 33 , Eric Wood 34 , Richard Young 35 , Robert M. Ewers 3 Habitat loss is the primary driver of biodiversity decline worldwide, but the effects of fragmentation (the spatial arrangement of remaining habitat) are debated. We tested the hypothesis that forest fragmentation sensitivity— affected by avoidance of habitat edges—should be driven by historical exposure to, and therefore species’ evolutionary responses to disturbance. Using a database containing 73 datasets collected worldwide (encompassing 4489 animal species), we found that the proportion of fragmentation-sensitive species was nearly three times as high in regions with low rates of historical disturbance compared with regions with high rates of disturbance (i.e., fires, glaciation, hurricanes, and deforestation). These disturbances coincide with a latitudinal gradient in which sensitivity increases sixfold at low versus high latitudes. We conclude that conservation efforts to limit edges created by fragmentation will be most important in the world’s tropical forests. G lobal biodiversity loss is occurring at more than 100 times the prehuman background extinction rate (1), and there is general consensus among scientists that most species’ declines can be at- tributed to habitat loss (2, 3). Nevertheless, the degree to which habitat fragmentation, defined as the spatial arrangement of remaining hab- itat, influences biodiversity loss has been a source of contention for over 40 years (4–7). Resolving this debate is important to conser- vation planning, which can entail designing the configuration of landscapes as well as spatially prioritizing areas for conservation (8). Forest fragmentation is particularly pres- sing given that 70% of Earth’s remaining forest is within 1 km of the forest edge (9) and that fragmentation of the world’ s most intact forest landscapes—the tropics—is predicted to accel- erate over the coming five decades (10). The variation across taxa and regions in species’ responses to fragmentation and edge effects in particular is central to the fragmen- tation debate (6, 11, 12). It is well known that life history and other ecological traits mediate species’ responses to habitat edges (13), but the degree to which there are predictable geo- graphical patterns in species’ sensitivity has yet to be quantified across multiple taxa on a global scale. Species’ evolutionary histories can shape their capacity to respond to novel stressors. The extinction filter hypothesis predicts that spe- cies that have evolved and survived in high- disturbance environments should be more likely to persist in the face of new distur- bances, including those of habitat loss and fragmentation (14). Further, more frequent disturbances could act as a barrier to sensi- tive species, preventing them from colonizing disturbance-prone regions. Disturbances often create edges, and in environments with fre- quent and large-scale disturbances, persistent species are more likely to be adapted to ubiqui- tous edge habitats. The extinction filter hypoth- esis is at least several decades old and has been suggested to apply in forest (15, 16) and grass- land systems (14). Both natural disturbances (such as wildfires and glaciation) and anthro- pogenic ones (such as logging, burning, and hunting) are thought to exert such evolutionary pressures (14). Nevertheless, there has been no global test of whether historical disturbance regimes can explain fragmentation effects. We used 73 datasets collected worldwide containing 4489 species from four major taxa [2682 arthropods, 1260 birds, 282 herptiles (reptiles and amphibians), and 265 mammals] (Fig. 1, fig. S1, and tables S1 and S2) to provide a global test of the extinction filter hypothesis in forest ecosystems (17). In the presence of an extinction filter, species inhabiting a filtered landscape with high levels of disturbances over historical (evolutionary) time scales should be resilient to new disturbances—either because sensitive species have been driven locally ex- tinct or because extant species have adapted to disturbance. Either mechanism would lead to a reduced prevalence of fragmentation- sensitive species in regions of the globe where disturbance has been historically common. We used a recently developed approach to quantify the landscape-scale impacts of forest edges on biodiversity ( 13, 18). By definition, hab- itat fragmentation for a given habitat amount leads to more, smaller patches, with a greater proportion of edge. We focus on landscape- scale variation in edge effects rather than the number of patches, because edge effects have long been known to have widespread effects on RESEARCH Betts et al., Science 366, 1236–1239 (2019) 6 December 2019 1 of 4 1 Forest Biodiversity Research Network, Department of Forest Ecosystems and Society, Oregon State University, Corvallis, OR 97331, USA. 2 School of Natural and Environmental Sciences, Newcastle University, Newcastle Upon Tyne NE1 7RU, UK. 3 Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot SL5 7PY, UK. 4 Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México (UNAM), Campus Morelia, Antigua Carretera Patzcuaro no. 8701, Ex-Hacienda de San José de la Huerta, 58190 Morelia, Michoacán, Mexico. 5 Instituo de Biociências, Universidade Federal de Mato Grosso do Sul, Caixa Postal 549, 79070-900 Campo Grande, Brazil. 6 Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK. 7 Setor Ecologia, Departamento de Biologia, Universidade Federal de Lavras, 37200-000, Lavras, MG, Brazil. 8 Geography and Environmental Sciences, University of Southampton, Southampton SO17 1BJ, UK. 9 Applied Conservation Ecology Lab, Programa de Pós-graduação em Ecologia e Conservação, da Biodiversidade, Universidade Estadual de Santa Cruz, Rodovia Ilhéus-Itabuna, km 16, Salobrinho, 45662- 000 Ilhéus, Bahia, Brazil. 10 Department of Wildlife Ecology and Conservation, University of Florida, Gainesville, FL 32611, USA. 11 Applied Ecology Research Group, School of Life Sciences, Anglia Ruskin University, Cambridge CB1 1PT, UK. 12 Department of Biology, University of Florida, Gainesville, FL 32611, USA. 13 School of Forestry and Wildlife Sciences, Auburn University, Auburn, AL 36849, USA. 14 Swiss Ornithological Institute, Sempach, Switzerland. 15 Division of Forest Sciences, School of Agricultural, Forest and Food Sciences HAFL, Bern University of Applied Sciences, Zollikofen, Switzerland. 16 Ghent University, Department of Biology, K.L. Ledeganckstraat 35, B-9000 Gent, Belgium. 17 Groupo de Biodiversidad y Conservación, Reptiles, Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Ciudad Universitaria, Edificio 425, Bogotá, Distrito Capital, Colombia. 18 Department of Chemistry and Biology, Ryerson University, 350 Victoria Street, Toronto, ON M5B 2K3, Canada. 19 Department of Science and Education, Field Museum of Natural History, Chicago, IL 60605, USA. 20 Departamento de Ciências Biológicas, Universidade Estadual de Feira de Santana, Avenida Transnordestina, s/n - Novo Horizonte, 44036-900 Feira de Santana, Bahia, Brazil. 21 Centre for Ecology, Evolution and Conservation, School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, UK. 22 Instituto de Biologia, Universidade Federal da Bahia, Salvador, 40170-115 Bahia, Brazil. 23 Department of Forest and Wildlife Ecology, University of Wisconsin–Madison, 1630 Linden Drive, Madison, WI 53706, USA. 24 School of Biological Sciences, University of Queensland, St Lucia, Queensland, Australia. 25 The Nature Conservancy, Arlington, VA 22203, USA. 26 Asian School of the Environment, Nanyang Technological University, 62 Nanyang Dr., 637459 Singapore. 27 Centro Agronómico Tropical de Investigación y Enseñanza, Turrialba, Costa Rica. 28 School of Biological Sciences, University of Canterbury, Private bag 4800, Christchurch 8140, New Zealand. 29 Department of Ecology and Territory, School of Rural and Environmental Studies, Pontificia Universidad Javeriana, Bogota, Colombia. 30 Smithsonian Conservation Biology Institute, Migratory Bird Center, National Zoological Park, Washington, DC 20013, USA. 31 Department of Biology, John Carroll University, University Heights, OH 44118, USA. 32 Department of Biosciences, Swansea University, Swansea SA2 8PP, Wales, UK. 33 Institute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, UK. 34 Department of Biological Sciences, California State University Los Angeles, 5151 State University Drive, Los Angeles, CA 90032, USA. 35 Durrell Wildlife Conservation Trust, Les Augres Manor, Trinity, Jersey JE3 5BP, UK. *Corresponding author. Email: matt.betts@oregonstate.edu (M.G.B); wolfch@oregonstate.edu (C.W) †These authors contributed equally to this work. on December 5, 2019 http://science.sciencemag.org/ Downloaded from