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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Habitat fragmentation and its lasting impact on Earth’s ecosystems</title><author><name sortKey="Haddad, Nick M" sort="Haddad, Nick M" uniqKey="Haddad N" first="Nick M." last="Haddad">Nick M. Haddad</name><affiliation><nlm:aff id="aff1">Department of Biological Sciences, North Carolina State University, Raleigh, NC 27695, USA.</nlm:aff></affiliation></author><author><name sortKey="Brudvig, Lars A" sort="Brudvig, Lars A" uniqKey="Brudvig L" first="Lars A." last="Brudvig">Lars A. Brudvig</name><affiliation><nlm:aff id="aff2">Department of Plant Biology, Michigan State University, East Lansing, MI 48824–1312, USA.</nlm:aff></affiliation></author><author><name sortKey="Clobert, Jean" sort="Clobert, Jean" uniqKey="Clobert J" first="Jean" last="Clobert">Jean Clobert</name><affiliation><nlm:aff id="aff3">Station d’Ecologie Expérimentale du CNRS a Moulis USR 2936, Moulis, 09200 Saint-Girons, France.</nlm:aff></affiliation></author><author><name sortKey="Davies, Kendi F" sort="Davies, Kendi F" uniqKey="Davies K" first="Kendi F." last="Davies">Kendi F. Davies</name><affiliation><nlm:aff id="aff4">Department of Ecology and Evolutionary Biology, UCB 334, University of Colorado, Boulder, CO 80309, USA.</nlm:aff></affiliation></author><author><name sortKey="Gonzalez, Andrew" sort="Gonzalez, Andrew" uniqKey="Gonzalez A" first="Andrew" last="Gonzalez">Andrew Gonzalez</name><affiliation><nlm:aff id="aff5">Department of Biology, McGill University, Montreal, Quebec H3A 1B1, Canada.</nlm:aff></affiliation></author><author><name sortKey="Holt, Robert D" sort="Holt, Robert D" uniqKey="Holt R" first="Robert D." last="Holt">Robert D. Holt</name><affiliation><nlm:aff id="aff6">Department of Biology, University of Florida, Gainesville, FL 32611, USA.</nlm:aff></affiliation></author><author><name sortKey="Lovejoy, Thomas E" sort="Lovejoy, Thomas E" uniqKey="Lovejoy T" first="Thomas E." last="Lovejoy">Thomas E. Lovejoy</name><affiliation><nlm:aff id="aff7">Department of Environmental Science and Policy, George Mason University, Fairfax, VA 22030, USA.</nlm:aff></affiliation></author><author><name sortKey="Sexton, Joseph O" sort="Sexton, Joseph O" uniqKey="Sexton J" first="Joseph O." last="Sexton">Joseph O. Sexton</name><affiliation><nlm:aff id="aff8">Global Land Cover Facility, Department of Geographical Sciences, University of Maryland, College Park, MD 20702, USA.</nlm:aff></affiliation></author><author><name sortKey="Austin, Mike P" sort="Austin, Mike P" uniqKey="Austin M" first="Mike P." last="Austin">Mike P. Austin</name><affiliation><nlm:aff id="aff9">CSIRO Land and Water Flagship, GPO Box 1700, Canberra, Australian Capital Territory 2601, Australia.</nlm:aff></affiliation></author><author><name sortKey="Collins, Cathy D" sort="Collins, Cathy D" uniqKey="Collins C" first="Cathy D." last="Collins">Cathy D. Collins</name><affiliation><nlm:aff id="aff10">Department of Biology, Colby College, 5746 Mayflower Hill, Waterville, ME 04901, USA.</nlm:aff></affiliation></author><author><name sortKey="Cook, William M" sort="Cook, William M" uniqKey="Cook W" first="William M." last="Cook">William M. Cook</name><affiliation><nlm:aff id="aff11">Department of Biological Sciences, St. Cloud State University, St. Cloud, MN 56301, USA.</nlm:aff></affiliation></author><author><name sortKey="Damschen, Ellen I" sort="Damschen, Ellen I" uniqKey="Damschen E" first="Ellen I." last="Damschen">Ellen I. Damschen</name><affiliation><nlm:aff id="aff12">Department of Zoology, University of Wisconsin, Madison, WI 53706, USA.</nlm:aff></affiliation></author><author><name sortKey="Ewers, Robert M" sort="Ewers, Robert M" uniqKey="Ewers R" first="Robert M." last="Ewers">Robert M. Ewers</name><affiliation><nlm:aff id="aff13">Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire SL5 7PY, UK.</nlm:aff></affiliation></author><author><name sortKey="Foster, Bryan L" sort="Foster, Bryan L" uniqKey="Foster B" first="Bryan L." last="Foster">Bryan L. Foster</name><affiliation><nlm:aff id="aff14">Department of Ecology and Evolutionary Biology and Kansas Biological Survey, University of Kansas, 2101 Constant Avenue, Lawrence, KS 66047–3759, USA.</nlm:aff></affiliation></author><author><name sortKey="Jenkins, Clinton N" sort="Jenkins, Clinton N" uniqKey="Jenkins C" first="Clinton N." last="Jenkins">Clinton N. Jenkins</name><affiliation><nlm:aff id="aff15">Instituto de Pesquisas Ecológicas, Rod. Dom Pedro I, km 47, Caixa Postal 47, Nazaré Paulista, São Paulo 12960-000, Brazil.</nlm:aff></affiliation></author><author><name sortKey="King, Andrew J" sort="King, Andrew J" uniqKey="King A" first="Andrew J." last="King">Andrew J. King</name><affiliation><nlm:aff id="aff9">CSIRO Land and Water Flagship, GPO Box 1700, Canberra, Australian Capital Territory 2601, Australia.</nlm:aff></affiliation></author><author><name sortKey="Laurance, William F" sort="Laurance, William F" uniqKey="Laurance W" first="William F." last="Laurance">William F. Laurance</name><affiliation><nlm:aff id="aff16">Centre for Tropical Environmental and Sustainability Science and College of Marine and Environmental Sciences, James Cook University, Cairns, Queensland 4878, Australia.</nlm:aff></affiliation></author><author><name sortKey="Levey, Douglas J" sort="Levey, Douglas J" uniqKey="Levey D" first="Douglas J." last="Levey">Douglas J. Levey</name><affiliation><nlm:aff id="aff17">National Science Foundation, Arlington, VA 22230, USA.</nlm:aff></affiliation></author><author><name sortKey="Margules, Chris R" sort="Margules, Chris R" uniqKey="Margules C" first="Chris R." last="Margules">Chris R. Margules</name><affiliation><nlm:aff id="aff18">Centre for Tropical Environmental and Sustainability Science, School of Earth and Environmental Sciences, James Cook University, Cairns 4878, Australia.</nlm:aff></affiliation><affiliation><nlm:aff id="aff19">Research Center for Climate Change, University of Indonesia, Kota Depok, Java Barat 16424, Indonesia.</nlm:aff></affiliation></author><author><name sortKey="Melbourne, Brett A" sort="Melbourne, Brett A" uniqKey="Melbourne B" first="Brett A." last="Melbourne">Brett A. Melbourne</name><affiliation><nlm:aff id="aff4">Department of Ecology and Evolutionary Biology, UCB 334, University of Colorado, Boulder, CO 80309, USA.</nlm:aff></affiliation></author><author><name sortKey="Nicholls, A O" sort="Nicholls, A O" uniqKey="Nicholls A" first="A. O." last="Nicholls">A. O. Nicholls</name><affiliation><nlm:aff id="aff9">CSIRO Land and Water Flagship, GPO Box 1700, Canberra, Australian Capital Territory 2601, Australia.</nlm:aff></affiliation><affiliation><nlm:aff id="aff20">The Institute for Land, Water and Society, Charles Sturt University, Thurgoona Campus, Albury, New South Wales 2640, Australia.</nlm:aff></affiliation></author><author><name sortKey="Orrock, John L" sort="Orrock, John L" uniqKey="Orrock J" first="John L." last="Orrock">John L. Orrock</name><affiliation><nlm:aff id="aff12">Department of Zoology, University of Wisconsin, Madison, WI 53706, USA.</nlm:aff></affiliation></author><author><name sortKey="Song, Dan Xia" sort="Song, Dan Xia" uniqKey="Song D" first="Dan-Xia" last="Song">Dan-Xia Song</name><affiliation><nlm:aff id="aff8">Global Land Cover Facility, Department of Geographical Sciences, University of Maryland, College Park, MD 20702, USA.</nlm:aff></affiliation></author><author><name sortKey="Townshend, John R" sort="Townshend, John R" uniqKey="Townshend J" first="John R." last="Townshend">John R. Townshend</name><affiliation><nlm:aff id="aff8">Global Land Cover Facility, Department of Geographical Sciences, University of Maryland, College Park, MD 20702, USA.</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26601154</idno><idno type="pmc">4643828</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4643828</idno><idno type="RBID">PMC:4643828</idno><idno type="doi">10.1126/sciadv.1500052</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000384</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000384</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Habitat fragmentation and its lasting impact on Earth’s ecosystems</title><author><name sortKey="Haddad, Nick M" sort="Haddad, Nick M" uniqKey="Haddad N" first="Nick M." last="Haddad">Nick M. Haddad</name><affiliation><nlm:aff id="aff1">Department of Biological Sciences, North Carolina State University, Raleigh, NC 27695, USA.</nlm:aff></affiliation></author><author><name sortKey="Brudvig, Lars A" sort="Brudvig, Lars A" uniqKey="Brudvig L" first="Lars A." last="Brudvig">Lars A. Brudvig</name><affiliation><nlm:aff id="aff2">Department of Plant Biology, Michigan State University, East Lansing, MI 48824–1312, USA.</nlm:aff></affiliation></author><author><name sortKey="Clobert, Jean" sort="Clobert, Jean" uniqKey="Clobert J" first="Jean" last="Clobert">Jean Clobert</name><affiliation><nlm:aff id="aff3">Station d’Ecologie Expérimentale du CNRS a Moulis USR 2936, Moulis, 09200 Saint-Girons, France.</nlm:aff></affiliation></author><author><name sortKey="Davies, Kendi F" sort="Davies, Kendi F" uniqKey="Davies K" first="Kendi F." last="Davies">Kendi F. Davies</name><affiliation><nlm:aff id="aff4">Department of Ecology and Evolutionary Biology, UCB 334, University of Colorado, Boulder, CO 80309, USA.</nlm:aff></affiliation></author><author><name sortKey="Gonzalez, Andrew" sort="Gonzalez, Andrew" uniqKey="Gonzalez A" first="Andrew" last="Gonzalez">Andrew Gonzalez</name><affiliation><nlm:aff id="aff5">Department of Biology, McGill University, Montreal, Quebec H3A 1B1, Canada.</nlm:aff></affiliation></author><author><name sortKey="Holt, Robert D" sort="Holt, Robert D" uniqKey="Holt R" first="Robert D." last="Holt">Robert D. Holt</name><affiliation><nlm:aff id="aff6">Department of Biology, University of Florida, Gainesville, FL 32611, USA.</nlm:aff></affiliation></author><author><name sortKey="Lovejoy, Thomas E" sort="Lovejoy, Thomas E" uniqKey="Lovejoy T" first="Thomas E." last="Lovejoy">Thomas E. Lovejoy</name><affiliation><nlm:aff id="aff7">Department of Environmental Science and Policy, George Mason University, Fairfax, VA 22030, USA.</nlm:aff></affiliation></author><author><name sortKey="Sexton, Joseph O" sort="Sexton, Joseph O" uniqKey="Sexton J" first="Joseph O." last="Sexton">Joseph O. Sexton</name><affiliation><nlm:aff id="aff8">Global Land Cover Facility, Department of Geographical Sciences, University of Maryland, College Park, MD 20702, USA.</nlm:aff></affiliation></author><author><name sortKey="Austin, Mike P" sort="Austin, Mike P" uniqKey="Austin M" first="Mike P." last="Austin">Mike P. Austin</name><affiliation><nlm:aff id="aff9">CSIRO Land and Water Flagship, GPO Box 1700, Canberra, Australian Capital Territory 2601, Australia.</nlm:aff></affiliation></author><author><name sortKey="Collins, Cathy D" sort="Collins, Cathy D" uniqKey="Collins C" first="Cathy D." last="Collins">Cathy D. Collins</name><affiliation><nlm:aff id="aff10">Department of Biology, Colby College, 5746 Mayflower Hill, Waterville, ME 04901, USA.</nlm:aff></affiliation></author><author><name sortKey="Cook, William M" sort="Cook, William M" uniqKey="Cook W" first="William M." last="Cook">William M. Cook</name><affiliation><nlm:aff id="aff11">Department of Biological Sciences, St. Cloud State University, St. Cloud, MN 56301, USA.</nlm:aff></affiliation></author><author><name sortKey="Damschen, Ellen I" sort="Damschen, Ellen I" uniqKey="Damschen E" first="Ellen I." last="Damschen">Ellen I. Damschen</name><affiliation><nlm:aff id="aff12">Department of Zoology, University of Wisconsin, Madison, WI 53706, USA.</nlm:aff></affiliation></author><author><name sortKey="Ewers, Robert M" sort="Ewers, Robert M" uniqKey="Ewers R" first="Robert M." last="Ewers">Robert M. Ewers</name><affiliation><nlm:aff id="aff13">Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire SL5 7PY, UK.</nlm:aff></affiliation></author><author><name sortKey="Foster, Bryan L" sort="Foster, Bryan L" uniqKey="Foster B" first="Bryan L." last="Foster">Bryan L. Foster</name><affiliation><nlm:aff id="aff14">Department of Ecology and Evolutionary Biology and Kansas Biological Survey, University of Kansas, 2101 Constant Avenue, Lawrence, KS 66047–3759, USA.</nlm:aff></affiliation></author><author><name sortKey="Jenkins, Clinton N" sort="Jenkins, Clinton N" uniqKey="Jenkins C" first="Clinton N." last="Jenkins">Clinton N. Jenkins</name><affiliation><nlm:aff id="aff15">Instituto de Pesquisas Ecológicas, Rod. Dom Pedro I, km 47, Caixa Postal 47, Nazaré Paulista, São Paulo 12960-000, Brazil.</nlm:aff></affiliation></author><author><name sortKey="King, Andrew J" sort="King, Andrew J" uniqKey="King A" first="Andrew J." last="King">Andrew J. King</name><affiliation><nlm:aff id="aff9">CSIRO Land and Water Flagship, GPO Box 1700, Canberra, Australian Capital Territory 2601, Australia.</nlm:aff></affiliation></author><author><name sortKey="Laurance, William F" sort="Laurance, William F" uniqKey="Laurance W" first="William F." last="Laurance">William F. Laurance</name><affiliation><nlm:aff id="aff16">Centre for Tropical Environmental and Sustainability Science and College of Marine and Environmental Sciences, James Cook University, Cairns, Queensland 4878, Australia.</nlm:aff></affiliation></author><author><name sortKey="Levey, Douglas J" sort="Levey, Douglas J" uniqKey="Levey D" first="Douglas J." last="Levey">Douglas J. Levey</name><affiliation><nlm:aff id="aff17">National Science Foundation, Arlington, VA 22230, USA.</nlm:aff></affiliation></author><author><name sortKey="Margules, Chris R" sort="Margules, Chris R" uniqKey="Margules C" first="Chris R." last="Margules">Chris R. Margules</name><affiliation><nlm:aff id="aff18">Centre for Tropical Environmental and Sustainability Science, School of Earth and Environmental Sciences, James Cook University, Cairns 4878, Australia.</nlm:aff></affiliation><affiliation><nlm:aff id="aff19">Research Center for Climate Change, University of Indonesia, Kota Depok, Java Barat 16424, Indonesia.</nlm:aff></affiliation></author><author><name sortKey="Melbourne, Brett A" sort="Melbourne, Brett A" uniqKey="Melbourne B" first="Brett A." last="Melbourne">Brett A. Melbourne</name><affiliation><nlm:aff id="aff4">Department of Ecology and Evolutionary Biology, UCB 334, University of Colorado, Boulder, CO 80309, USA.</nlm:aff></affiliation></author><author><name sortKey="Nicholls, A O" sort="Nicholls, A O" uniqKey="Nicholls A" first="A. O." last="Nicholls">A. O. Nicholls</name><affiliation><nlm:aff id="aff9">CSIRO Land and Water Flagship, GPO Box 1700, Canberra, Australian Capital Territory 2601, Australia.</nlm:aff></affiliation><affiliation><nlm:aff id="aff20">The Institute for Land, Water and Society, Charles Sturt University, Thurgoona Campus, Albury, New South Wales 2640, Australia.</nlm:aff></affiliation></author><author><name sortKey="Orrock, John L" sort="Orrock, John L" uniqKey="Orrock J" first="John L." last="Orrock">John L. Orrock</name><affiliation><nlm:aff id="aff12">Department of Zoology, University of Wisconsin, Madison, WI 53706, USA.</nlm:aff></affiliation></author><author><name sortKey="Song, Dan Xia" sort="Song, Dan Xia" uniqKey="Song D" first="Dan-Xia" last="Song">Dan-Xia Song</name><affiliation><nlm:aff id="aff8">Global Land Cover Facility, Department of Geographical Sciences, University of Maryland, College Park, MD 20702, USA.</nlm:aff></affiliation></author><author><name sortKey="Townshend, John R" sort="Townshend, John R" uniqKey="Townshend J" first="John R." last="Townshend">John R. Townshend</name><affiliation><nlm:aff id="aff8">Global Land Cover Facility, Department of Geographical Sciences, University of Maryland, College Park, MD 20702, USA.</nlm:aff></affiliation></author></analytic><series><title level="j">Science Advances</title><idno type="eISSN">2375-2548</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Urgent need for conservation and restoration measures to improve landscape connectivity.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Pereira, H M" uniqKey="Pereira H">H. M. Pereira</name></author><author><name sortKey="Leadley, P W" uniqKey="Leadley P">P. W. Leadley</name></author><author><name sortKey="Proenca, V" uniqKey="Proenca V">V. Proenca</name></author><author><name sortKey="Alkemade, R" uniqKey="Alkemade R">R. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Sci Adv</journal-id><journal-id journal-id-type="iso-abbrev">Sci Adv</journal-id><journal-id journal-id-type="publisher-id">SciAdv</journal-id><journal-id journal-id-type="hwp">advances</journal-id><journal-title-group><journal-title>Science Advances</journal-title></journal-title-group><issn pub-type="epub">2375-2548</issn><publisher><publisher-name>American Association for the Advancement of Science</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26601154</article-id><article-id pub-id-type="pmc">4643828</article-id><article-id pub-id-type="publisher-id">1500052</article-id><article-id pub-id-type="doi">10.1126/sciadv.1500052</article-id><article-categories><subj-group subj-group-type="article-type"><subject>Research Article</subject></subj-group><subj-group subj-group-type="heading"><subject>Research Articles</subject></subj-group><subj-group subj-group-type="legacy-article-type"><subject>SciAdv r-articles</subject></subj-group><subj-group subj-group-type="field"><subject>Ecology</subject></subj-group><subj-group subj-group-type="overline"><subject>Applied Ecology</subject></subj-group></article-categories><title-group><article-title>Habitat fragmentation and its lasting impact on Earth’s ecosystems</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Haddad</surname><given-names>Nick M.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1">*</xref></contrib><contrib contrib-type="author"><name><surname>Brudvig</surname><given-names>Lars A.</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Clobert</surname><given-names>Jean</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Davies</surname><given-names>Kendi F.</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Gonzalez</surname><given-names>Andrew</given-names></name><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Holt</surname><given-names>Robert D.</given-names></name><xref ref-type="aff" rid="aff6"><sup>6</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lovejoy</surname><given-names>Thomas E.</given-names></name><xref ref-type="aff" rid="aff7"><sup>7</sup></xref></contrib><contrib contrib-type="author"><name><surname>Sexton</surname><given-names>Joseph O.</given-names></name><xref ref-type="aff" rid="aff8"><sup>8</sup></xref></contrib><contrib contrib-type="author"><name><surname>Austin</surname><given-names>Mike P.</given-names></name><xref ref-type="aff" rid="aff9"><sup>9</sup></xref></contrib><contrib contrib-type="author"><name><surname>Collins</surname><given-names>Cathy D.</given-names></name><xref ref-type="aff" rid="aff10"><sup>10</sup></xref></contrib><contrib contrib-type="author"><name><surname>Cook</surname><given-names>William M.</given-names></name><xref ref-type="aff" rid="aff11"><sup>11</sup></xref></contrib><contrib contrib-type="author"><name><surname>Damschen</surname><given-names>Ellen I.</given-names></name><xref ref-type="aff" rid="aff12"><sup>12</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ewers</surname><given-names>Robert M.</given-names></name><xref ref-type="aff" rid="aff13"><sup>13</sup></xref></contrib><contrib contrib-type="author"><name><surname>Foster</surname><given-names>Bryan L.</given-names></name><xref ref-type="aff" rid="aff14"><sup>14</sup></xref></contrib><contrib contrib-type="author"><name><surname>Jenkins</surname><given-names>Clinton N.</given-names></name><xref ref-type="aff" rid="aff15"><sup>15</sup></xref></contrib><contrib contrib-type="author"><name><surname>King</surname><given-names>Andrew J.</given-names></name><xref ref-type="aff" rid="aff9"><sup>9</sup></xref></contrib><contrib contrib-type="author"><name><surname>Laurance</surname><given-names>William F.</given-names></name><xref ref-type="aff" rid="aff16"><sup>16</sup></xref></contrib><contrib contrib-type="author"><name><surname>Levey</surname><given-names>Douglas J.</given-names></name><xref ref-type="aff" rid="aff17"><sup>17</sup></xref></contrib><contrib contrib-type="author"><name><surname>Margules</surname><given-names>Chris R.</given-names></name><xref ref-type="aff" rid="aff18"><sup>18</sup></xref><xref ref-type="aff" rid="aff19"><sup>19</sup></xref></contrib><contrib contrib-type="author"><name><surname>Melbourne</surname><given-names>Brett A.</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Nicholls</surname><given-names>A. O.</given-names></name><xref ref-type="aff" rid="aff9"><sup>9</sup></xref><xref ref-type="aff" rid="aff20"><sup>20</sup></xref></contrib><contrib contrib-type="author"><name><surname>Orrock</surname><given-names>John L.</given-names></name><xref ref-type="aff" rid="aff12"><sup>12</sup></xref></contrib><contrib contrib-type="author"><name><surname>Song</surname><given-names>Dan-Xia</given-names></name><xref ref-type="aff" rid="aff8"><sup>8</sup></xref></contrib><contrib contrib-type="author"><name><surname>Townshend</surname><given-names>John R.</given-names></name><xref ref-type="aff" rid="aff8"><sup>8</sup></xref></contrib><aff id="aff1"><label>1</label>Department of Biological Sciences, North Carolina State University, Raleigh, NC 27695, USA.</aff><aff id="aff2"><label>2</label>Department of Plant Biology, Michigan State University, East Lansing, MI 48824–1312, USA.</aff><aff id="aff3"><label>3</label>Station d’Ecologie Expérimentale du CNRS a Moulis USR 2936, Moulis, 09200 Saint-Girons, France.</aff><aff id="aff4"><label>4</label>Department of Ecology and Evolutionary Biology, UCB 334, University of Colorado, Boulder, CO 80309, USA.</aff><aff id="aff5"><label>5</label>Department of Biology, McGill University, Montreal, Quebec H3A 1B1, Canada.</aff><aff id="aff6"><label>6</label>Department of Biology, University of Florida, Gainesville, FL 32611, USA.</aff><aff id="aff7"><label>7</label>Department of Environmental Science and Policy, George Mason University, Fairfax, VA 22030, USA.</aff><aff id="aff8"><label>8</label>Global Land Cover Facility, Department of Geographical Sciences, University of Maryland, College Park, MD 20702, USA.</aff><aff id="aff9"><label>9</label>CSIRO Land and Water Flagship, GPO Box 1700, Canberra, Australian Capital Territory 2601, Australia.</aff><aff id="aff10"><label>10</label>Department of Biology, Colby College, 5746 Mayflower Hill, Waterville, ME 04901, USA.</aff><aff id="aff11"><label>11</label>Department of Biological Sciences, St. Cloud State University, St. Cloud, MN 56301, USA.</aff><aff id="aff12"><label>12</label>Department of Zoology, University of Wisconsin, Madison, WI 53706, USA.</aff><aff id="aff13"><label>13</label>Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire SL5 7PY, UK.</aff><aff id="aff14"><label>14</label>Department of Ecology and Evolutionary Biology and Kansas Biological Survey, University of Kansas, 2101 Constant Avenue, Lawrence, KS 66047–3759, USA.</aff><aff id="aff15"><label>15</label>Instituto de Pesquisas Ecológicas, Rod. Dom Pedro I, km 47, Caixa Postal 47, Nazaré Paulista, São Paulo 12960-000, Brazil.</aff><aff id="aff16"><label>16</label>Centre for Tropical Environmental and Sustainability Science and College of Marine and Environmental Sciences, James Cook University, Cairns, Queensland 4878, Australia.</aff><aff id="aff17"><label>17</label>National Science Foundation, Arlington, VA 22230, USA.</aff><aff id="aff18"><label>18</label>Centre for Tropical Environmental and Sustainability Science, School of Earth and Environmental Sciences, James Cook University, Cairns 4878, Australia.</aff><aff id="aff19"><label>19</label>Research Center for Climate Change, University of Indonesia, Kota Depok, Java Barat 16424, Indonesia.</aff><aff id="aff20"><label>20</label>The Institute for Land, Water and Society, Charles Sturt University, Thurgoona Campus, Albury, New South Wales 2640, Australia.</aff></contrib-group><author-notes><corresp id="cor1"><label>*</label>Corresponding author. E-mail: <email xlink:href="nick_haddad@ncsu.edu">nick_haddad@ncsu.edu</email></corresp></author-notes><pub-date pub-type="collection"><month>3</month><year>2015</year></pub-date><pub-date pub-type="epub"><day>20</day><month>3</month><year>2015</year></pub-date><volume>1</volume><issue>2</issue><elocation-id>e1500052</elocation-id><history><date date-type="received"><day>15</day><month>1</month><year>2015</year></date><date date-type="accepted"><day>17</day><month>2</month><year>2015</year></date></history><permissions><copyright-statement>Copyright © 2015, The Authors</copyright-statement><copyright-year>2015</copyright-year><copyright-holder>The Authors</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/" id="p-1"><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution license</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p></license></permissions><abstract abstract-type="teaser"><p>Urgent need for conservation and restoration measures to improve landscape connectivity.</p></abstract><abstract><p>We conducted an analysis of global forest cover to reveal that 70% of remaining forest is within 1 km of the forest’s edge, subject to the degrading effects of fragmentation. A synthesis of fragmentation experiments spanning multiple biomes and scales, five continents, and 35 years demonstrates that habitat fragmentation reduces biodiversity by 13 to 75% and impairs key ecosystem functions by decreasing biomass and altering nutrient cycles. Effects are greatest in the smallest and most isolated fragments, and they magnify with the passage of time. These findings indicate an urgent need for conservation and restoration measures to improve landscape connectivity, which will reduce extinction rates and help maintain ecosystem services.</p></abstract><custom-meta-group><custom-meta><meta-name>Editor</meta-name><meta-value>None</meta-value></custom-meta><custom-meta><meta-name>Copyeditor</meta-name><meta-value>SPI</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec sec-type="introduction" disp-level="1"><title>INTRODUCTION</title><p>Destruction and degradation of natural ecosystems are the primary causes of declines in global biodiversity (<xref rid="R1" ref-type="bibr"><italic>1</italic></xref>, <xref rid="R2" ref-type="bibr"><italic>2</italic></xref>). Habitat destruction typically leads to fragmentation, the division of habitat into smaller and more isolated fragments separated by a matrix of human-transformed land cover. The loss of area, increase in isolation, and greater exposure to human land uses along fragment edges initiate long-term changes to the structure and function of the remaining fragments (<xref rid="R3" ref-type="bibr"><italic>3</italic></xref>).</p><p>Ecologists agree that habitat destruction is detrimental to the maintenance of biodiversity, but they disagree—often strongly—on the extent to which fragmentation itself is to blame (<xref rid="R4" ref-type="bibr"><italic>4</italic></xref>, <xref rid="R5" ref-type="bibr"><italic>5</italic></xref>). Early hypotheses based on the biogeography of oceanic islands (<xref rid="R6" ref-type="bibr"><italic>6</italic></xref>) provided a theoretical framework to understand fragmentation’s effect on extinction in terrestrial landscapes composed of “islands” of natural habitat scattered across a “sea” of human-transformed habitat. Central to the controversy has been a lingering uncertainty about the role of decreased fragment size and increased isolation relative to the widespread and pervasive effects of habitat loss in explaining declines in biodiversity and the degradation of ecosystems (<xref rid="R7" ref-type="bibr"><italic>7</italic></xref>). Observational studies of the effects of fragmentation have often magnified the controversy because inference from nonmanipulative studies is limited to correlation and because they have individually often considered only single aspects of fragmentation (for example, edge, isolation, and area) (<xref rid="R8" ref-type="bibr"><italic>8</italic></xref>). However, together with these correlative observations, experimental studies reveal that fragmentation has multiple simultaneous effects that are interwoven in complex ways and that operate over potentially long time scales (<xref rid="R9" ref-type="bibr"><italic>9</italic></xref>).</p><p>Here, we draw on findings of the world’s largest and longest-running fragmentation experiments that span 35 years and disparate biomes on five continents. Their rigorous designs and long-term implementation overcome many limitations of observational studies. In particular, by manipulating and isolating individual aspects of fragmentation while controlling for others, and by doing so on entire ecosystems, they provide a powerful way to disentangle cause and effect in fragmented landscapes. Here, we present experimental evidence of unexpected long-term ecological changes caused by habitat fragmentation.</p><p>Highlighting one ecosystem type as an example, we first present a global analysis of the fragmentation of forest ecosystems, quantifying for the first time the global hotspots of intensive historical fragmentation. We then synthesize results from the set of long-term experiments conducted in a wide variety of ecosystems to demonstrate consistent impacts of fragmentation, how those impacts change over time, and how they align with predictions from theory and observation. Finally, we identify key knowledge gaps for the next generation of fragmentation experiments.</p></sec><sec disp-level="1"><title>GLOBAL ANALYSIS OF THE EXTREME MAGNITUDE AND EXTENT OF FRAGMENTATION</title><p>New satellite data sets reveal at high resolution how human activities are transforming global ecosystems. Foremost among these observations are those of forest cover because of the high contrast between forest and anthropogenic land cover types. Deforestation, which was already widespread in temperate regions in the mid-18th to 20th centuries and increased in the tropics over the past half century, has resulted in the loss of more than a third of all forest cover worldwide (<xref rid="R10" ref-type="bibr"><italic>10</italic></xref>, <xref rid="R11" ref-type="bibr"><italic>11</italic></xref>). Beyond the direct impacts of forest loss and expanding anthropogenic land cover (for example, agricultural fields and urban areas), remnant forests are likely to suffer from being smaller, more isolated, and with a greater area located near the edge of the forest (<xref rid="R12" ref-type="bibr"><italic>12</italic></xref>).</p><p>We analyzed the world’s first high-resolution map of global tree cover (<xref rid="R13" ref-type="bibr"><italic>13</italic></xref>) to measure the magnitude of forest fragmentation. This analysis revealed that nearly 20% of the world’s remaining forest is within 100 m of an edge (<xref ref-type="fig" rid="F1">Fig. 1</xref>, A and B)—in close proximity to agricultural, urban, or other modified environments where impacts on forest ecosystems are most severe (<xref rid="R14" ref-type="bibr"><italic>14</italic></xref>). More than 70% of the world’s forests are within 1 km of a forest edge. Thus, most forests are well within the range where human activities, altered microclimate, and nonforest species may influence and degrade forest ecosystems (<xref rid="R15" ref-type="bibr"><italic>15</italic></xref>). The largest contiguous expanses of remaining forests are in the humid tropical regions of the Amazon and Congo River Basins (<xref ref-type="fig" rid="F1">Fig. 1A</xref>). Large areas of more disjunct forest also remain in southeastern Asia, New Guinea, and the boreal biomes.</p><fig id="F1" fig-type="figure" orientation="portrait" position="float"><label>Fig. 1</label><caption><title>The global magnitude of forest fragmentation.</title><p>(<bold>A</bold>) Mean distance to forest edge for forested pixels within each 1-km cell. Lines point to locations of ongoing fragmentation experiments identified and described in <xref ref-type="fig" rid="F2">Fig. 2</xref>. (<bold>B</bold>) Proportion of the world’s forest at each distance to the forest edge and the cumulative proportion across increasing distance categories (green line). (<bold>C</bold> and <bold>E</bold>) In the Brazilian Amazon (C) and Atlantic Forests (E), the proportion of forest area at each distance to forest edge for both the current and estimated historic extent of forest. (<bold>D</bold> and <bold>F</bold>) In the Brazilian Amazon (D) and Atlantic Forests (F), the number of fragments and the total area of fragments of that size. The total number of fragments in the smallest bin (1 to 10 ha) is an underestimate in both the Atlantic Forest and Amazon data sets because not all of the very smallest fragments are mapped.</p></caption><graphic xlink:href="1500052-F1"></graphic></fig><p>Historical data enable the study of the process of forest fragmentation over time. We reconstructed the historical forest extent and timing of fragmentation in two forested regions of Brazil that provide a stark contrast in land-use dynamics. The Brazilian Amazon is a rapidly changing frontier (<xref rid="R10" ref-type="bibr"><italic>10</italic></xref>), yet most of its forests remain contiguous and far from an edge despite recent increases in fragmentation (<xref ref-type="fig" rid="F1">Fig. 1</xref>, C and D). In contrast, the Brazilian Atlantic Forest is a largely deforested landscape, cleared for agriculture and logged for timber over the last three centuries (<xref rid="R11" ref-type="bibr"><italic>11</italic></xref>). This remaining forest is dominated by small fragments, with most fragments smaller than 1000 ha and within 1000 m of a forest edge (<xref ref-type="fig" rid="F1">Fig. 1</xref>, E and F) (<xref rid="R16" ref-type="bibr"><italic>16</italic></xref>). In the Brazilian Amazon, the proportion of forest farther than 1 km from the forest edge has decreased from 90% (historical) to 75% (today), and in the Brazilian Atlantic, from 90% to less than 9%.</p><p>These two forested regions of Brazil define extremes of the fragmentation process and are representative of the extent of fragmentation in forested landscapes worldwide (<xref ref-type="fig" rid="F1">Fig. 1</xref>), as well as many other biomes including temperate grasslands, savannas, and even aquatic systems (<xref rid="R17" ref-type="bibr"><italic>17</italic></xref>). For example, although a spatial analysis similar to that of forest is not currently possible in grasslands, 37% of the world’s grassland eco-regions are classified as “highly fragmented” (<xref rid="R18" ref-type="bibr"><italic>18</italic></xref>, <xref rid="R19" ref-type="bibr"><italic>19</italic></xref>). Robust knowledge of how habitat fragmentation affects biodiversity and ecosystem processes is needed if we are to comprehend adequately the implications of this global environmental change.</p></sec><sec disp-level="1"><title>THE VALUE OF LONG-TERM FRAGMENTATION EXPERIMENTS</title><p>Long-term experiments are a powerful tool for understanding the ecological consequences of fragmentation (<xref rid="R20" ref-type="bibr"><italic>20</italic></xref>). Whereas observational studies of fragmented landscapes have yielded important insights (<xref rid="R9" ref-type="bibr"><italic>9</italic></xref>, <xref rid="R21" ref-type="bibr"><italic>21</italic></xref>), they typically lack rigorous controls, replication, randomization, or baseline data. Observational studies have limited ability to isolate the effects of fragmentation from concomitant habitat loss and degradation per se (<xref rid="R4" ref-type="bibr"><italic>4</italic></xref>, <xref rid="R7" ref-type="bibr"><italic>7</italic></xref>, <xref rid="R22" ref-type="bibr"><italic>22</italic></xref>). Remnant fragments are embedded in different types and qualities of surrounding habitat, complicating interpretation because the surrounding habitat also influences biodiversity and ecosystem productivity (<xref rid="R23" ref-type="bibr"><italic>23</italic></xref>).</p><p>The long-term fragmentation experiments we analyze here comprise the entire set of ongoing terrestrial long-term experiments. They occur in several biomes (<xref ref-type="fig" rid="F2">Fig. 2</xref> and Supplementary Materials) and were designed to manipulate specific components of fragmentation—habitat size, isolation, and connectivity—while controlling for confounding factors such as the amount of habitat lost across a landscape (<xref ref-type="fig" rid="F2">Fig. 2</xref>). The largest fragments across these experiments match the size of fragments commonly created by anthropogenic activities (<xref ref-type="fig" rid="F1">Figs. 1</xref> and <xref ref-type="fig" rid="F2">2</xref>). Distances to the edge of experimental fragments range to 500 m, encompassing edge distances found in more than half of forests worldwide (<xref ref-type="fig" rid="F1">Fig. 1B</xref>). In each experiment, different fragmentation treatments with replication were established, starting from continuous, nonfragmented landscapes and controlling for background environmental variation either by experimental design (blocking) or by measurement of covariates for use in subsequent analyses. Tests were conducted within fragments that varied experimentally in area or edge, within fragments that were experimentally isolated or connected, or within experimental fragments compared to the same area within continuous habitat. All treatments were replicated. Experiments were created by destroying or creating precise amounts of habitat across replicate landscapes, allowing tests of fragmentation effects independent of habitat loss. The robust and comparable experimental designs allow for powerful tests of the mechanisms underpinning the ecological impacts of fragmentation, and the long-term nature of ensuing studies has revealed consistent emergent effects.</p><fig id="F2" fig-type="figure" orientation="portrait" position="float"><label>Fig. 2</label><caption><title>The world’s ongoing fragmentation experiments.</title><p>All experiments have been running continuously since the time indicated by the start of the associated arrow (with the exception of the moss fragmentation experiment, which represents a series of studies over nearly two decades). The variables under study in each experiment are checked. The area is that of the experiment’s largest fragments. Icons under “Fragment” and “Matrix” indicate the dominant community and its relative height, with multiple trees representing succession.</p></caption><graphic xlink:href="1500052-F2"></graphic></fig><p>These experiments mimic anthropogenic fragmentation; they are whole-ecosystem manipulations in which all species and processes experienced the same treatment (<xref rid="R24" ref-type="bibr"><italic>24</italic></xref>). Emergent responses thus reflect the multiple direct and indirect effects of interacting species and processes. Further, because experimentally fragmented ecosystems are open to fluxes of individuals and resources, fragmentation effects can manifest across multiple levels of ecological organization (<xref ref-type="fig" rid="F3">Fig. 3</xref>). Long-term experiments have the power to detect lagged and/or chronic impacts.</p><fig id="F3" fig-type="figure" orientation="portrait" position="float"><label>Fig. 3</label><caption><title>Fragmentation effects propagate through the whole ecosystem.</title><p>(<bold>A</bold> to <bold>C</bold>) For each fragmentation treatment [reduced area in BDFFP, Wog Wog, Kansas (A); increased isolation in SRS and Moss (B); and increased edge in all experiments (C)], we summarize major findings for ecological processes at all levels of ecological organization. Each dot represents the mean effect size [computed as log response ratio: ln(mean in more fragmented treatment/mean in non- or less-fragmented treatment)] for an ecological process. Effect sizes are statistical, such that negative or positive values could represent degrading function. Horizontal bars are the range when a dot is represented by more than one study. Details, including individual effect sizes for each study, are reported in table S1.</p></caption><graphic xlink:href="1500052-F3"></graphic></fig><p>The first fragmentation experiments, now more than three decades old, were created to test effects of fragment area on both species persistence and patterns of immigration, reflecting concern in conservation biology about the role of fragmentation in reducing population sizes below viable levels (<xref rid="R25" ref-type="bibr"><italic>25</italic></xref>) (<xref ref-type="fig" rid="F2">Fig. 2</xref>). Subsequent experiments, created two decades ago, shifted focus to modifying habitat isolation, reflecting recognition of the potential to mitigate negative effects of fragmentation by recreating habitat—specifically with corridors—to increase connectivity among fragments (<xref rid="R26" ref-type="bibr"><italic>26</italic></xref>) (<xref ref-type="fig" rid="F2">Fig. 2</xref>). The newest experiments test emerging questions about potentially deleterious synergies between fragmentation and global changes in climate and land use (<xref ref-type="fig" rid="F2">Fig. 2</xref>).</p><p>We synthesized results available 31 January 2014 for all studies within these experiments that were conducted in all treatments and replicates, and tested fragmentation effects on dispersal, abundance, extinction, species richness, community composition, and ecosystem functioning. We first calculated effect sizes of fragmentation as log response ratios (<xref ref-type="fig" rid="F3">Fig. 3</xref>). Data from 76 different studies across the five longest-running experiments were drawn from published and unpublished sources (table S1). We synthesized results according to three fragmentation treatments: reduced fragment area [the focus of Biological Dynamics of Forest Fragments Project (BDFFP), Wog Wog, and Kansas; see <xref ref-type="fig" rid="F2">Fig. 2</xref> for identifiers of experiments], increased fragment isolation [Savannah River Site (SRS) and Moss], and increased proportion of edge (all experiments). Fragmented treatments were compared directly to non- or less-fragmented habitats that were either larger or connected via structural corridors (table S1).</p><sec disp-level="2"><title>Strong, consistent, and accumulating effects of habitat fragmentation</title><p>Our synthesis revealed strong and consistent responses of organisms and ecosystem processes to fragmentation arising from decreased fragment area, increased isolation, and the creation of habitat edges (<xref ref-type="fig" rid="F3">Fig. 3</xref>).</p><p>Community and ecosystem responses emerge from observed responses at the level of populations. Reduced area decreased animal residency within fragments, and increased isolation reduced movement among fragments, thus reducing fragment recolonization after local extinction (<xref ref-type="fig" rid="F3">Fig. 3</xref>, A and B). Reduced fragment area and increased fragment isolation generally reduced abundance of birds, mammals, insects, and plants (<xref ref-type="fig" rid="F3">Fig. 3</xref>, A and B). This overall pattern emerged despite complex patterns of increases or declines in abundance of individual species (<xref ref-type="fig" rid="F3">Fig. 3A</xref>) with various proximate causes such as release from competition or predation, shifts in disturbance regimes, or alteration of abiotic factors (<xref rid="R14" ref-type="bibr"><italic>14</italic></xref>, <xref rid="R27" ref-type="bibr"><italic>27</italic></xref>–<xref rid="R29" ref-type="bibr"><italic>29</italic></xref>). Reduced area, increased isolation, and increased proportion of edge habitat reduced seed predation and herbivory, whereas increased proportion of edge caused higher fledgling predation that had the effect of reducing bird fecundity (represented together as trophic dynamics in <xref ref-type="fig" rid="F3">Fig. 3</xref>, A to C). Perhaps because of reduced movement and abundance, the ability of species to persist was lower in smaller and more isolated fragments (<xref ref-type="fig" rid="F3">Fig. 3</xref>, A and B).</p><p>As predicted by theory (<xref rid="R6" ref-type="bibr"><italic>6</italic></xref>, <xref rid="R30" ref-type="bibr"><italic>30</italic></xref>, <xref rid="R31" ref-type="bibr"><italic>31</italic></xref>), fragmentation strongly reduced species richness of plants and animals across experiments (<xref ref-type="fig" rid="F3">Fig. 3</xref>, A and B), often changing the composition of entire communities (<xref ref-type="fig" rid="F3">Fig. 3</xref>, A to C). In tropical forests, reduced fragment size and increased proportion of edge habitat caused shifts in the physical environment that led to the loss of large and old trees in favor of pioneer trees (<xref ref-type="fig" rid="F3">Fig. 3</xref>, A and C), with subsequent impacts on the community composition of insects (<xref rid="R32" ref-type="bibr"><italic>32</italic></xref>). In grasslands, fragment size also affected succession rate, such that increased light penetration and altered seed pools in smaller fragments impeded the rate of ecological succession relative to that of larger fragments (<xref rid="R33" ref-type="bibr"><italic>33</italic></xref>) (<xref ref-type="fig" rid="F3">Fig. 3A</xref>).</p><p>Consistently, all aspects of fragmentation—reduced fragment area, increased isolation, and increased edge—had degrading effects on a disparate set of core ecosystem functions. Degraded functions included reduced carbon and nitrogen retention (<xref ref-type="fig" rid="F3">Fig. 3</xref>, A to C), productivity (<xref ref-type="fig" rid="F3">Fig. 3C</xref>), and pollination (<xref ref-type="fig" rid="F3">Fig. 3B</xref>).</p><p>In summary, across experiments spanning numerous studies and ecosystems, fragmentation consistently degraded ecosystems, reducing species persistence, species richness, nutrient retention, trophic dynamics, and, in more isolated fragments, movement.</p></sec><sec disp-level="2"><title>Long-term consequences of fragmentation</title><p>To synthesize all time series of species richness and ecosystem functioning gathered across experiments, we measured effects of fragmentation over the course of each study. The effect of fragmentation was calculated over time as the proportional change in fragmented relative to non- or less-fragmented treatments (<xref ref-type="fig" rid="F4">Fig. 4</xref>).</p><fig id="F4" fig-type="figure" orientation="portrait" position="float"><label>Fig. 4</label><caption><title>Delayed effects of fragmentation on ecosystem degradation.</title><p>(<bold>A</bold>) The extinction debt represents a delayed loss of species due to fragmentation. (<bold>B</bold>) The immigration lag represents differences in species richness caused by smaller fragment area or increased isolation during fragment succession. (<bold>C</bold>) The ecosystem function debt represents delayed changes in ecosystem function due to reduced fragment size or increased isolation. Percent loss is calculated as proportional change in fragmented treatments [for example, (no. of species in fragment − no. of species in control)/(no. of species in control) × 100]. Fragments and controls were either the same area before and after fragmentation, fragments compared to unfragmented controls, or small compared to large fragments. Filled symbols indicate times when fragmentation effects became significant, as determined by the original studies (see table S2). Mean slopes (dashed lines) were estimated using linear mixed (random slopes) models. Mean slope estimates (mean and SE) were as follows: (A) −0.22935 (0.07529); (B) −0.06519 (0.03495); (C) −0.38568 (0.16010).</p></caption><graphic xlink:href="1500052-F4"></graphic></fig><p>In most cases, the large and consistent effects of fragmentation revealed by the experiments were predicted from theory. However, we were struck by the persistence of degradation to biodiversity and ecosystem processes and by the increase in many of the effects over time (<xref ref-type="fig" rid="F4">Fig. 4</xref>). For example, extreme rainfall events at Wog Wog appeared to delay the decline in plant species richness for 5 years after fragmentation. In the Kansas Experiment, a lag of 12 years occurred before fragmentation effects on plant succession were detected. Our results thus reveal long-term and progressive effects of fragmentation and provide support for three processes proposed by recent studies in spatial ecology: extinction debt, immigration lag, and ecosystem function debt (<xref ref-type="fig" rid="F4">Fig. 4</xref>).</p><p>First, we found strong evidence for temporal lags in extinction [that is, “extinction debt” (<xref rid="R30" ref-type="bibr"><italic>30</italic></xref>)] in fragments. Species richness of plants, arthropods, and birds sampled in the experiments conducted in mature forest fragments and replicated moss landscapes showed decreases of 20 to 75% after fragmentation (<xref ref-type="fig" rid="F4">Fig. 4A</xref>). Some declines were evident almost immediately after fragmentation, whereas others increased in magnitude over the experiment’s duration. Across experiments, average loss was >20% after 1 year, >50% after 10 years, and is still increasing in the longest time series measured (more than two decades). The rate of change appears to be slower in larger fragments [in BDFFP, 50% decline in bird species after 5 years in 1-ha fragments, but after 12 years in 100-ha fragments; in Moss, 40% decline in arthropod species richness of small fragments and 26% reduction in large fragments after 1 year (<xref rid="R34" ref-type="bibr"><italic>34</italic></xref>, <xref rid="R35" ref-type="bibr"><italic>35</italic></xref>)]. As predicted by theory (<xref rid="R36" ref-type="bibr"><italic>36</italic></xref>), the extinction debt appears to take longer to pay in larger fragments.</p><p>Second, we observed that reduced richness was coincident with an “immigration lag” (<xref rid="R37" ref-type="bibr"><italic>37</italic></xref>), whereby small or isolated fragments are slower to accumulate species during community assembly (<xref rid="R33" ref-type="bibr"><italic>33</italic></xref>, <xref rid="R38" ref-type="bibr"><italic>38</italic></xref>) (<xref ref-type="fig" rid="F4">Fig. 4B</xref>). Immigration lags were observed in experiments conducted in successional systems that were initiated by creating new habitat fragments, rather than by fragmenting existing habitats. After more than a decade, immigration lags resulted in 5% fewer species after 1 year, and 15% fewer species after 10 years in small or isolated fragments compared to large or connected fragments (<xref ref-type="fig" rid="F4">Fig. 4B</xref>).</p><p>Third, we observed an ecosystem function debt caused by fragmentation (<xref rid="R39" ref-type="bibr"><italic>39</italic></xref>) in forest and moss fragments (<xref ref-type="fig" rid="F4">Fig. 4C</xref>). An ecosystem function debt is manifest both as delayed changes in nutrient cycling and as changes to plant and consumer biomass. Loss of function amounted to 30% after 1 year, rising to 80% after a decade in small and isolated fragments when compared to larger and more connected fragments (<xref ref-type="fig" rid="F4">Fig. 4C</xref>). Functional debts can result from biodiversity loss, as when loss of nutrients and reduction in decomposition are caused by simplification of food webs. Alternatively, the impact is exhibited through pathways whereby fragmentation changes biotic (for example, tree density in successional systems) or abiotic conditions (for example, light regimes or humidity) in ways that alter and potentially impair ecosystem function [for example, biomass collapse in fragments; <xref ref-type="fig" rid="F3">Figs. 3</xref> and <xref ref-type="fig" rid="F4">4</xref>; altered nitrogen and carbon soil dynamics (<xref rid="R40" ref-type="bibr"><italic>40</italic></xref>)].</p></sec><sec disp-level="2"><title>A new understanding of the effects of fragmentation</title><p>By testing existing theory, experiments play a pivotal role in advancing ideas and developing new theory. We draw on experimental evidence to highlight two ways that the understanding of fragmentation has been enriched by the interplay between long-term experiments and development of theory.</p><p>First, island biogeography (<xref rid="R6" ref-type="bibr"><italic>6</italic></xref>) was among the earliest theories to predict extinction and immigration rates and patterns of species richness in isolated biotas, which were later used to predict the effects of fragmentation on these variables. Experiments in continental settings tested the theory and gave rise to fresh perspectives. For example, islands are surrounded by sea, a thoroughly inimical matrix for island-dwelling species. Habitat islands, or fragments, are surrounded by a matrix that may not be so unsuitable for some species. In terms of all of the ecological variables studied in our long-term experiments, our results support the conclusion that ecological dynamics in human-modified fragments are a stark contrast to the dynamics in intact habitats that remain. Observational studies that have devoted more detailed consideration to the countryside within which fragments are embedded explain the diversity of ecological responses in remaining fragments (<xref rid="R41" ref-type="bibr"><italic>41</italic></xref>). At the same time as experiments supported the core predictions of classical theories about effects of fragment size and isolation (<xref ref-type="fig" rid="F3">Figs. 3</xref> and <xref ref-type="fig" rid="F4">4</xref>), they spurred and tested new theories such as metacommunity theory (<xref rid="R42" ref-type="bibr"><italic>42</italic></xref>) to account for variation in connectivity and habitat quality within and between fragments (<xref rid="R33" ref-type="bibr"><italic>33</italic></xref>, <xref rid="R43" ref-type="bibr"><italic>43</italic></xref>–<xref rid="R45" ref-type="bibr"><italic>45</italic></xref>), spatial dynamics (<xref rid="R14" ref-type="bibr"><italic>14</italic></xref>, <xref rid="R46" ref-type="bibr"><italic>46</italic></xref>), and spatially varying interspecific interactions (<xref rid="R47" ref-type="bibr"><italic>47</italic></xref>).</p><p>Second, experiments have demonstrated that the effects of fragmentation are mediated by variation in traits across species. More realistic predictions of community responses to fragmentation emerged after explicit consideration of species traits such as rarity and trophic levels (<xref rid="R48" ref-type="bibr"><italic>48</italic></xref>, <xref rid="R49" ref-type="bibr"><italic>49</italic></xref>), dispersal mode (<xref rid="R50" ref-type="bibr"><italic>50</italic></xref>–<xref rid="R52" ref-type="bibr"><italic>52</italic></xref>), reproductive mode and life span (<xref rid="R29" ref-type="bibr"><italic>29</italic></xref>, <xref rid="R53" ref-type="bibr"><italic>53</italic></xref>), diet (<xref rid="R54" ref-type="bibr"><italic>54</italic></xref>), and movement behavior (<xref rid="R55" ref-type="bibr"><italic>55</italic></xref>, <xref rid="R56" ref-type="bibr"><italic>56</italic></xref>). Increasingly, the simple theoretical prediction that fragmentation reduces species richness is being modified to account for species identity through models that focus on how species vary in their traits (<xref rid="R4" ref-type="bibr"><italic>4</italic></xref>, <xref rid="R21" ref-type="bibr"><italic>21</italic></xref>, <xref rid="R36" ref-type="bibr"><italic>36</italic></xref>, <xref rid="R48" ref-type="bibr"><italic>48</italic></xref>, <xref rid="R57" ref-type="bibr"><italic>57</italic></xref>, <xref rid="R58" ref-type="bibr"><italic>58</italic></xref>). Consideration of traits may help to interpret variation around the overarching pattern that fragmentation consistently reduces species richness across many species and biomes (<xref ref-type="fig" rid="F3">Figs. 3</xref> and <xref ref-type="fig" rid="F4">4</xref>).</p></sec></sec><sec disp-level="1"><title>A NEW GENERATION OF FRAGMENTATION EXPERIMENTS</title><p>New foci are emerging for studying ecosystem fragmentation, including (i) synergies between fragmentation and global changes, (ii) eco-evolutionary responses of species to fragmentation, and (iii) ecological responses to fragmentation in production landscapes—that is, ecosystems whose services are under extreme appropriation by humans (<xref rid="R59" ref-type="bibr"><italic>59</italic></xref>).</p><p>First, conclusions from experiments thus far are likely to have been conservative because impacts from other environmental changes have been mostly excluded. Most forms of global change known to reduce population sizes and biodiversity will be exacerbated by fragmentation (<xref rid="R58" ref-type="bibr"><italic>58</italic></xref>, <xref rid="R60" ref-type="bibr"><italic>60</italic></xref>), including climate change (<xref rid="R61" ref-type="bibr"><italic>61</italic></xref>), invasive species (<xref rid="R62" ref-type="bibr"><italic>62</italic></xref>, <xref rid="R63" ref-type="bibr"><italic>63</italic></xref>), hunting (<xref rid="R64" ref-type="bibr"><italic>64</italic></xref>), pollution [including light, noise, and chemicals (<xref rid="R65" ref-type="bibr"><italic>65</italic></xref>)], and altered disturbance regimes (<xref rid="R66" ref-type="bibr"><italic>66</italic></xref>).</p><p>More complex experiments with unparalleled control and capacity to simultaneously manipulate fragmentation and other global changes are now under way (<xref rid="R53" ref-type="bibr"><italic>53</italic></xref>). The Metatron, created in 2011 in southern France (<xref rid="R67" ref-type="bibr"><italic>67</italic></xref>), enables ecologists to assess effects of variation in temperature and other abiotic factors in addition to habitat isolation. The SAFE Project is being created in the rainforest of Borneo (<xref rid="R68" ref-type="bibr"><italic>68</italic></xref>) and will embed a fragmentation experiment within a production agricultural plantation in which poaching will occur. Other synergies should be investigated experimentally, including the interaction between fragmentation and hunting, fire, infectious disease outbreaks, or nitrogen deposition. Within these experiments, fragmentation and loss of habitat can then be varied independently.</p><p>Second, current experiments have stopped short of examining how fragmentation drives evolution through genetic bottlenecks, ecological traps, changing patterns of selection, inbreeding, drift, and gene flow (<xref rid="R69" ref-type="bibr"><italic>69</italic></xref>–<xref rid="R72" ref-type="bibr"><italic>72</italic></xref>). Extensive fragmentation has occurred over many years, and in some regions over millennia (<xref rid="R11" ref-type="bibr"><italic>11</italic></xref>). Changes caused by fragmentation undoubtedly lead to altered patterns of selection and trait evolution. Evolutionary responses to fragmentation have already been suggested (<xref rid="R73" ref-type="bibr"><italic>73</italic></xref>, <xref rid="R74" ref-type="bibr"><italic>74</italic></xref>), and it is likely that such changes will, in turn, feed back to influence population persistence and ecosystem resilience in fragmented landscapes. Linking long-term experiments with the tools of landscape genetics (<xref rid="R75" ref-type="bibr"><italic>75</italic></xref>) may provide powerful insights into the evolutionary dynamics of species inhabiting fragmented landscapes.</p><p>Third, new experiments should address the management of natural habitats in production landscapes by monitoring vegetation, networks of interacting species, and ecosystem services at ecologically relevant spatial and temporal scales (<xref rid="R76" ref-type="bibr"><italic>76</italic></xref>–<xref rid="R78" ref-type="bibr"><italic>78</italic></xref>). Some ecosystem services have global consequences, for example, local carbon sequestration affects global atmospheric CO<sub>2</sub>. However, in many cases the benefits obtained by people depend on their proximity to habitat fragments (<xref rid="R79" ref-type="bibr"><italic>79</italic></xref>). For example, crop pollination and biological pest control from natural areas adjacent to farms are made available by the very process of habitat fragmentation, bringing people and agriculture closer to those services. Yet, further fragmentation reduces access to many services and ultimately may push landscapes past tipping points, beyond which essential ecosystem services are not merely diminished but lost completely (<xref rid="R80" ref-type="bibr"><italic>80</italic></xref>). This complex relationship creates a double-edged sword, for which locally optimal levels and arrangements of habitat must be sought. New fragmentation experiments should consider how multiple fragments in a landscape interact, creating an ecological network in which the collective benefit of ecosystem services may be greater than the sum of services provided by individual fragments (<xref rid="R81" ref-type="bibr"><italic>81</italic></xref>, <xref rid="R82" ref-type="bibr"><italic>82</italic></xref>). Experimental inferences may then be tested beyond their spatiotemporal domains and, if successful, extrapolated across scales. Such research will be aided by satellite monitoring of ecosystems and human land use across the globe. The most powerful research programs will integrate experiments, observational studies, air- and space-borne imaging, and modeling.</p></sec><sec sec-type="conclusions" disp-level="1"><title>CONCLUSIONS</title><p>Fragmentation experiments—some of the largest and longest-running experiments in ecology—provide clear evidence of strong and typically degrading impacts of habitat fragmentation on biodiversity and ecological processes. The findings of these experiments extend to a large fraction of the terrestrial surface of the Earth. Much of the Earth’s remaining forest fragments are less than 10 ha in area, and half of the world’s forest is within 500 m of the forest edge—areas and distances matched to existing long-term experiments (<xref ref-type="fig" rid="F1">Figs. 1</xref> and <xref ref-type="fig" rid="F2">2</xref>) from which consistent effects of fragmentation have emerged (<xref ref-type="fig" rid="F3">Figs. 3</xref> and <xref ref-type="fig" rid="F4">4</xref>).</p><p>Reduced fragment area, increased isolation, and increased edge initiate changes that percolate through ecosystems (<xref ref-type="fig" rid="F3">Fig. 3</xref>). Fragmentation has the capacity to generate persistent, deleterious, and often unpredicted outcomes, including surprising surges in abundance of some species and the pattern that long temporal scales are required to discern many strong system responses. In light of these conclusions and ongoing debates, we suggest that fragmentation’s consistency, pervasiveness, and long-term degrading effect on biodiversity and ecosystem function have not been fully appreciated (<xref rid="R9" ref-type="bibr"><italic>9</italic></xref>).</p><p>Without gains in yield and efficiency of agricultural systems (<xref rid="R83" ref-type="bibr"><italic>83</italic></xref>), the expansion of human populations will inevitably continue to reduce and fragment natural areas. The area of Earth’s land surface devoted to cropland already occupies 1.53 billion hectares (<xref rid="R83" ref-type="bibr"><italic>83</italic></xref>) and may expand 18% by the middle of this century (<xref rid="R84" ref-type="bibr"><italic>84</italic></xref>), and the area committed to urban centers is predicted to triple to 0.18 billion hectares by 2030 (<xref rid="R85" ref-type="bibr"><italic>85</italic></xref>). The capacity of the surviving forests and other natural habitats to sustain biodiversity and ecosystem services will hinge upon the total amount and quality of habitat left in fragments, their degree of connectivity, and how they are affected by other human-induced perturbations such as climate change and invasive species. Long-term experiments will be even more needed to appreciate, explain, and predict long-term effects. New efforts should work in concert, coordinating a network of experiments across ecosystems and spatial extents.</p><p>The effects of current fragmentation will continue to emerge for decades. Extinction debts are likely to come due, although the counteracting immigration debts may never fully be paid. Indeed, the experiments here reveal ongoing losses of biodiversity and ecosystem functioning two decades or longer after fragmentation occurred. Understanding the relationship between transient and long-term dynamics is a substantial challenge that ecologists must tackle, and fragmentation experiments will be central for relating observation to theory.</p><p>Experimental results to date show that the effects of fragmentation are strong and markedly consistent across a diverse array of terrestrial systems on five continents. Increasingly, these effects will march in concert with other global changes. New experiments should be coupled with emerging technologies, landscape genetics, and detailed imagery of our planet, and should be coordinated with current ecological theory to understand more deeply the coupled dynamics of ecological and social systems. These insights will be increasingly critical for those responsible for managing and prioritizing areas for preservation and ecological restoration in fragmented landscapes.</p></sec></body><back><ack><title>Acknowledgments</title><p>For comments, we thank R. Dunn, P. Ehrlich, L. Frishkoff, F. Gould, A. Leidner, C. Mendenhall, A. Tal, J. Watling, and the Fukami and Peay labs at Stanford. For symbols in figures, we thank the Integration and Application Network, University of Maryland Center for Environmental Science. <bold>Funding:</bold> R.M.E. is supported by ERC (European Research Council) Project number 281986. A.G. is supported by the Natural Sciences and Engineering Research Council, the Canada Research Chair program, and the Quebec Centre for Biodiversity Science. C.N.J. was supported by the Brazilian agency CAPES through the Ciência Sem Fronteiras program. R.D.H. thanks the University of Florida Foundation. J.C. is supported by the labex TULIP and the ANR Infrastructure grant AnaEE-France. Global forest cover data and analysis were provided under support from the NASA Making Earth System Data Records for Use in Research Environments (MEaSUREs; NNH06ZDA001N) and Land Cover and Land Use Change (NNH07ZDA001N-LCLUC) programs. For long-term support of experiments, we thank the Andrew W. Mellon Foundation (BDFFP); the Kansas Biological Survey and National Science Foundation (NSF) (DEB 01-08302 and DEB-0950100; Kansas Experiment); NSF and U.S. Department of Agriculture Forest Service–Savannah River (SRS Corridor Experiment); NSF DEB 0841892 and Environment and Heritage NSW, Forestry Corporation NSW, and CSIRO Ecosystem Sciences (Wog Wog); and the Sime Darby Foundation (SAFE).</p></ack><app-group><app><title>SUPPLEMENTARY MATERIALS</title><supplementary-material content-type="local-data"><p>Supplementary material for this article is available at <ext-link ext-link-type="uri" xlink:href="http://advances.sciencemag.org/cgi/content/full/1/2/e1500052/DC1">http://advances.sciencemag.org/cgi/content/full/1/2/e1500052/DC1</ext-link></p><p>Materials and Methods</p><p>Fig. S1. Map of the BDFFP experiment and location within Brazil.</p><p>Fig. S2. Map of the Kansas fragmentation experiment.</p><p>Fig. S3. Map of the Wog Wog experiment and location within Australia.</p><p>Fig. S4. Map of the SRS experiment showing locations of the eight blocks in the second SRS Corridor Experiment within the SRS, South Carolina, USA.</p><p>Fig. S5. Design of the Moss experiment.</p><p>Fig. S6. Design of the Metatron experiment with 48 enclosed fragments and adjoining enclosed corridors.</p><p>Fig. S7. Map of the SAFE experiment and location within Borneo [after Ewers <italic>et al</italic>. (<xref rid="R68" ref-type="bibr"><italic>68</italic></xref>)].</p><p>Table S1. Metadata for <xref ref-type="fig" rid="F3">Fig. 3</xref> in the main text.</p><p>Table S2. Metadata for <xref ref-type="fig" rid="F4">Fig. 4</xref> in the main text.</p></supplementary-material></app></app-group><ref-list><title>REFERENCES AND NOTES</title><ref id="R1"><label>1</label><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Pereira</surname><given-names>H. 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