Fragmented tropical forests lose mutualistic plant–animal interactions

Aim Forest fragmentation is among the principal causes of global biodiversity loss, yet how it affects mutualistic interactions between plants and animals at large spatial scale is poorly understood. In particular, tropical forest regeneration depends on animal‐mediated seed dispersal, but the seed‐...

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Veröffentlicht in:Diversity & distributions 2020-02, Vol.26 (2), p.154-168
Hauptverfasser: Marjakangas, Emma-Liina, Abrego, Nerea, Grøtan, Vidar, de Lima, Renato A. F., Bello, Carolina, Bovendorp, Ricardo S., Culot, Laurence, Hasui, Érica, Lima, Fernando, Muylaert, Renata Lara, Niebuhr, Bernardo Brandão, Oliveira, Alexandre A., Pereira, Lucas Augusto, Prado, Paulo I., Stevens, Richard D., Vancine, Maurício Humberto, Ribeiro, Milton Cezar, Galetti, Mauro, Ovaskainen, Otso
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container_issue 2
container_start_page 154
container_title Diversity & distributions
container_volume 26
creator Marjakangas, Emma-Liina
Abrego, Nerea
Grøtan, Vidar
de Lima, Renato A. F.
Bello, Carolina
Bovendorp, Ricardo S.
Culot, Laurence
Hasui, Érica
Lima, Fernando
Muylaert, Renata Lara
Niebuhr, Bernardo Brandão
Oliveira, Alexandre A.
Pereira, Lucas Augusto
Prado, Paulo I.
Stevens, Richard D.
Vancine, Maurício Humberto
Ribeiro, Milton Cezar
Galetti, Mauro
Ovaskainen, Otso
description Aim Forest fragmentation is among the principal causes of global biodiversity loss, yet how it affects mutualistic interactions between plants and animals at large spatial scale is poorly understood. In particular, tropical forest regeneration depends on animal‐mediated seed dispersal, but the seed‐dispersing animals face rapid decline due to forest fragmentation and defaunation. Here, we assess how fragmentation influences the pairwise interactions between 407 seed disperser and 1,424 tree species in a highly fragmented biodiversity hotspot. Location Atlantic Forest, South America. Methods We predicted interaction networks in 912 sites covering the entire biome by combining verified interaction data with co‐occurrence probabilities obtained from a spatially explicit joint species distribution model. We identified keystone seed dispersers by computing a species‐specific keystone index and by selecting those species belonging to the top 5% quantile. Results We show that forest fragmentation affects seed dispersal interactions negatively, and the decreased area of functionally connected forest, rather than increased edge effects, is the main driver behind the loss of interactions. Both the seed disperser availability for the local tree communities and in particular the proportion of interactions provided by keystone seed dispersers decline with increasing degree of fragmentation. Importantly, just 21 keystone species provided >40% of all interactions. The numbers of interactions provided by keystone and non‐keystone species, however, were equally negatively affected by fragmentation, suggesting that seed dispersal interactions may not be rewired under strong fragmentation effects. Conclusions We highlight the importance of understanding the fragmentation‐induced compositional shifts in seed disperser communities as they may lead to lagged and multiplicative effects on tree communities. Our results illustrate the utility of model‐based prediction of interaction networks as well as model‐based identification of keystone species as a tool for prioritizing conservation efforts. Similar modelling approaches could be applied to other threatened ecosystems and interaction types globally.
doi_str_mv 10.1111/ddi.13010
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F. ; Bello, Carolina ; Bovendorp, Ricardo S. ; Culot, Laurence ; Hasui, Érica ; Lima, Fernando ; Muylaert, Renata Lara ; Niebuhr, Bernardo Brandão ; Oliveira, Alexandre A. ; Pereira, Lucas Augusto ; Prado, Paulo I. ; Stevens, Richard D. ; Vancine, Maurício Humberto ; Ribeiro, Milton Cezar ; Galetti, Mauro ; Ovaskainen, Otso</creator><contributor>Knop, Eva</contributor><creatorcontrib>Marjakangas, Emma-Liina ; Abrego, Nerea ; Grøtan, Vidar ; de Lima, Renato A. F. ; Bello, Carolina ; Bovendorp, Ricardo S. ; Culot, Laurence ; Hasui, Érica ; Lima, Fernando ; Muylaert, Renata Lara ; Niebuhr, Bernardo Brandão ; Oliveira, Alexandre A. ; Pereira, Lucas Augusto ; Prado, Paulo I. ; Stevens, Richard D. ; Vancine, Maurício Humberto ; Ribeiro, Milton Cezar ; Galetti, Mauro ; Ovaskainen, Otso ; Knop, Eva</creatorcontrib><description>Aim Forest fragmentation is among the principal causes of global biodiversity loss, yet how it affects mutualistic interactions between plants and animals at large spatial scale is poorly understood. In particular, tropical forest regeneration depends on animal‐mediated seed dispersal, but the seed‐dispersing animals face rapid decline due to forest fragmentation and defaunation. Here, we assess how fragmentation influences the pairwise interactions between 407 seed disperser and 1,424 tree species in a highly fragmented biodiversity hotspot. Location Atlantic Forest, South America. Methods We predicted interaction networks in 912 sites covering the entire biome by combining verified interaction data with co‐occurrence probabilities obtained from a spatially explicit joint species distribution model. We identified keystone seed dispersers by computing a species‐specific keystone index and by selecting those species belonging to the top 5% quantile. Results We show that forest fragmentation affects seed dispersal interactions negatively, and the decreased area of functionally connected forest, rather than increased edge effects, is the main driver behind the loss of interactions. Both the seed disperser availability for the local tree communities and in particular the proportion of interactions provided by keystone seed dispersers decline with increasing degree of fragmentation. Importantly, just 21 keystone species provided &gt;40% of all interactions. The numbers of interactions provided by keystone and non‐keystone species, however, were equally negatively affected by fragmentation, suggesting that seed dispersal interactions may not be rewired under strong fragmentation effects. Conclusions We highlight the importance of understanding the fragmentation‐induced compositional shifts in seed disperser communities as they may lead to lagged and multiplicative effects on tree communities. Our results illustrate the utility of model‐based prediction of interaction networks as well as model‐based identification of keystone species as a tool for prioritizing conservation efforts. Similar modelling approaches could be applied to other threatened ecosystems and interaction types globally.</description><identifier>ISSN: 1366-9516</identifier><identifier>EISSN: 1472-4642</identifier><identifier>DOI: 10.1111/ddi.13010</identifier><language>eng</language><publisher>Wiley</publisher><subject>Atlantic Forest ; BIODIVERSITY RESEARCH ; co‐occurrence ; ecological network ; fragmentation ; frugivory ; Hierarchical Modelling of Species Communities ; joint species distribution model ; keystone species ; seed dispersal ; zoochory</subject><ispartof>Diversity &amp; distributions, 2020-02, Vol.26 (2), p.154-168</ispartof><rights>2019 The Authors</rights><rights>2019 The Authors. published by John Wiley &amp; Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3260-822987c15a02954a47f8a6621c1248082392abd9f6f77d936999ef4ab171741a3</citedby><cites>FETCH-LOGICAL-c3260-822987c15a02954a47f8a6621c1248082392abd9f6f77d936999ef4ab171741a3</cites><orcidid>0000-0001-9650-7575 ; 0000-0002-5245-3779</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26868300$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26868300$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,780,784,864,1417,11562,25354,27924,27925,45574,45575,46052,46476,54524,54530</link.rule.ids><linktorsrc>$$Uhttps://www.jstor.org/stable/26868300$$EView_record_in_JSTOR$$FView_record_in_$$GJSTOR</linktorsrc></links><search><contributor>Knop, Eva</contributor><creatorcontrib>Marjakangas, Emma-Liina</creatorcontrib><creatorcontrib>Abrego, Nerea</creatorcontrib><creatorcontrib>Grøtan, Vidar</creatorcontrib><creatorcontrib>de Lima, Renato A. F.</creatorcontrib><creatorcontrib>Bello, Carolina</creatorcontrib><creatorcontrib>Bovendorp, Ricardo S.</creatorcontrib><creatorcontrib>Culot, Laurence</creatorcontrib><creatorcontrib>Hasui, Érica</creatorcontrib><creatorcontrib>Lima, Fernando</creatorcontrib><creatorcontrib>Muylaert, Renata Lara</creatorcontrib><creatorcontrib>Niebuhr, Bernardo Brandão</creatorcontrib><creatorcontrib>Oliveira, Alexandre A.</creatorcontrib><creatorcontrib>Pereira, Lucas Augusto</creatorcontrib><creatorcontrib>Prado, Paulo I.</creatorcontrib><creatorcontrib>Stevens, Richard D.</creatorcontrib><creatorcontrib>Vancine, Maurício Humberto</creatorcontrib><creatorcontrib>Ribeiro, Milton Cezar</creatorcontrib><creatorcontrib>Galetti, Mauro</creatorcontrib><creatorcontrib>Ovaskainen, Otso</creatorcontrib><title>Fragmented tropical forests lose mutualistic plant–animal interactions</title><title>Diversity &amp; distributions</title><description>Aim Forest fragmentation is among the principal causes of global biodiversity loss, yet how it affects mutualistic interactions between plants and animals at large spatial scale is poorly understood. In particular, tropical forest regeneration depends on animal‐mediated seed dispersal, but the seed‐dispersing animals face rapid decline due to forest fragmentation and defaunation. Here, we assess how fragmentation influences the pairwise interactions between 407 seed disperser and 1,424 tree species in a highly fragmented biodiversity hotspot. Location Atlantic Forest, South America. Methods We predicted interaction networks in 912 sites covering the entire biome by combining verified interaction data with co‐occurrence probabilities obtained from a spatially explicit joint species distribution model. We identified keystone seed dispersers by computing a species‐specific keystone index and by selecting those species belonging to the top 5% quantile. Results We show that forest fragmentation affects seed dispersal interactions negatively, and the decreased area of functionally connected forest, rather than increased edge effects, is the main driver behind the loss of interactions. Both the seed disperser availability for the local tree communities and in particular the proportion of interactions provided by keystone seed dispersers decline with increasing degree of fragmentation. Importantly, just 21 keystone species provided &gt;40% of all interactions. The numbers of interactions provided by keystone and non‐keystone species, however, were equally negatively affected by fragmentation, suggesting that seed dispersal interactions may not be rewired under strong fragmentation effects. Conclusions We highlight the importance of understanding the fragmentation‐induced compositional shifts in seed disperser communities as they may lead to lagged and multiplicative effects on tree communities. Our results illustrate the utility of model‐based prediction of interaction networks as well as model‐based identification of keystone species as a tool for prioritizing conservation efforts. 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F.</creatorcontrib><creatorcontrib>Bello, Carolina</creatorcontrib><creatorcontrib>Bovendorp, Ricardo S.</creatorcontrib><creatorcontrib>Culot, Laurence</creatorcontrib><creatorcontrib>Hasui, Érica</creatorcontrib><creatorcontrib>Lima, Fernando</creatorcontrib><creatorcontrib>Muylaert, Renata Lara</creatorcontrib><creatorcontrib>Niebuhr, Bernardo Brandão</creatorcontrib><creatorcontrib>Oliveira, Alexandre A.</creatorcontrib><creatorcontrib>Pereira, Lucas Augusto</creatorcontrib><creatorcontrib>Prado, Paulo I.</creatorcontrib><creatorcontrib>Stevens, Richard D.</creatorcontrib><creatorcontrib>Vancine, Maurício Humberto</creatorcontrib><creatorcontrib>Ribeiro, Milton Cezar</creatorcontrib><creatorcontrib>Galetti, Mauro</creatorcontrib><creatorcontrib>Ovaskainen, Otso</creatorcontrib><collection>Wiley Online Library (Open Access Collection)</collection><collection>Wiley Online Library (Open Access Collection)</collection><collection>CrossRef</collection><jtitle>Diversity &amp; distributions</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext_linktorsrc</fulltext></delivery><addata><au>Marjakangas, Emma-Liina</au><au>Abrego, Nerea</au><au>Grøtan, Vidar</au><au>de Lima, Renato A. F.</au><au>Bello, Carolina</au><au>Bovendorp, Ricardo S.</au><au>Culot, Laurence</au><au>Hasui, Érica</au><au>Lima, Fernando</au><au>Muylaert, Renata Lara</au><au>Niebuhr, Bernardo Brandão</au><au>Oliveira, Alexandre A.</au><au>Pereira, Lucas Augusto</au><au>Prado, Paulo I.</au><au>Stevens, Richard D.</au><au>Vancine, Maurício Humberto</au><au>Ribeiro, Milton Cezar</au><au>Galetti, Mauro</au><au>Ovaskainen, Otso</au><au>Knop, Eva</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Fragmented tropical forests lose mutualistic plant–animal interactions</atitle><jtitle>Diversity &amp; distributions</jtitle><date>2020-02-01</date><risdate>2020</risdate><volume>26</volume><issue>2</issue><spage>154</spage><epage>168</epage><pages>154-168</pages><issn>1366-9516</issn><eissn>1472-4642</eissn><abstract>Aim Forest fragmentation is among the principal causes of global biodiversity loss, yet how it affects mutualistic interactions between plants and animals at large spatial scale is poorly understood. In particular, tropical forest regeneration depends on animal‐mediated seed dispersal, but the seed‐dispersing animals face rapid decline due to forest fragmentation and defaunation. Here, we assess how fragmentation influences the pairwise interactions between 407 seed disperser and 1,424 tree species in a highly fragmented biodiversity hotspot. Location Atlantic Forest, South America. Methods We predicted interaction networks in 912 sites covering the entire biome by combining verified interaction data with co‐occurrence probabilities obtained from a spatially explicit joint species distribution model. We identified keystone seed dispersers by computing a species‐specific keystone index and by selecting those species belonging to the top 5% quantile. Results We show that forest fragmentation affects seed dispersal interactions negatively, and the decreased area of functionally connected forest, rather than increased edge effects, is the main driver behind the loss of interactions. Both the seed disperser availability for the local tree communities and in particular the proportion of interactions provided by keystone seed dispersers decline with increasing degree of fragmentation. Importantly, just 21 keystone species provided &gt;40% of all interactions. The numbers of interactions provided by keystone and non‐keystone species, however, were equally negatively affected by fragmentation, suggesting that seed dispersal interactions may not be rewired under strong fragmentation effects. Conclusions We highlight the importance of understanding the fragmentation‐induced compositional shifts in seed disperser communities as they may lead to lagged and multiplicative effects on tree communities. Our results illustrate the utility of model‐based prediction of interaction networks as well as model‐based identification of keystone species as a tool for prioritizing conservation efforts. Similar modelling approaches could be applied to other threatened ecosystems and interaction types globally.</abstract><pub>Wiley</pub><doi>10.1111/ddi.13010</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0001-9650-7575</orcidid><orcidid>https://orcid.org/0000-0002-5245-3779</orcidid><oa>free_for_read</oa></addata></record>
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subjects Atlantic Forest
BIODIVERSITY RESEARCH
co‐occurrence
ecological network
fragmentation
frugivory
Hierarchical Modelling of Species Communities
joint species distribution model
keystone species
seed dispersal
zoochory
title Fragmented tropical forests lose mutualistic plant–animal interactions
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