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Local climate modulates the development of soil nematode communities after glacier retreat

The worldwide retreat of glaciers is causing a faster than ever increase in ice‐free areas that are leading to the emergence of new ecosystems. Understanding the dynamics of these environments is critical to predicting the consequences of climate change on mountains and at high latitudes. Climatic d...

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Published in:Global change biology 2024-01, Vol.30 (1), p.e17057-n/a
Main Authors: Guerrieri, Alessia, Cantera, Isabel, Marta, Silvio, Bonin, Aurélie, Carteron, Alexis, Ambrosini, Roberto, Caccianiga, Marco, Anthelme, Fabien, Azzoni, Roberto Sergio, Almond, Peter, Alviz Gazitúa, Pablo, Cauvy‐Fraunié, Sophie, Ceballos Lievano, Jorge Luis, Chand, Pritam, Chand Sharma, Milap, Clague, John, Cochachín Rapre, Justiniano Alejo, Compostella, Chiara, Cruz Encarnación, Rolando, Dangles, Olivier, Deline, Philip, Eger, Andre, Erokhin, Sergey, Franzetti, Andrea, Gielly, Ludovic, Gili, Fabrizio, Gobbi, Mauro, Hågvar, Sigmund, Khedim, Norine, Meneses, Rosa Isela, Peyre, Gwendolyn, Pittino, Francesca, Proietto, Angela, Rabatel, Antoine, Urseitova, Nurai, Yang, Yan, Zaginaev, Vitalii, Zerboni, Andrea, Zimmer, Anaïs, Taberlet, Pierre, Diolaiuti, Guglielmina Adele, Poulenard, Jerome, Fontaneto, Diego, Thuiller, Wilfried, Ficetola, Gentile Francesco
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container_title Global change biology
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creator Guerrieri, Alessia
Cantera, Isabel
Marta, Silvio
Bonin, Aurélie
Carteron, Alexis
Ambrosini, Roberto
Caccianiga, Marco
Anthelme, Fabien
Azzoni, Roberto Sergio
Almond, Peter
Alviz Gazitúa, Pablo
Cauvy‐Fraunié, Sophie
Ceballos Lievano, Jorge Luis
Chand, Pritam
Chand Sharma, Milap
Clague, John
Cochachín Rapre, Justiniano Alejo
Compostella, Chiara
Cruz Encarnación, Rolando
Dangles, Olivier
Deline, Philip
Eger, Andre
Erokhin, Sergey
Franzetti, Andrea
Gielly, Ludovic
Gili, Fabrizio
Gobbi, Mauro
Hågvar, Sigmund
Khedim, Norine
Meneses, Rosa Isela
Peyre, Gwendolyn
Pittino, Francesca
Proietto, Angela
Rabatel, Antoine
Urseitova, Nurai
Yang, Yan
Zaginaev, Vitalii
Zerboni, Andrea
Zimmer, Anaïs
Taberlet, Pierre
Diolaiuti, Guglielmina Adele
Poulenard, Jerome
Fontaneto, Diego
Thuiller, Wilfried
Ficetola, Gentile Francesco
description The worldwide retreat of glaciers is causing a faster than ever increase in ice‐free areas that are leading to the emergence of new ecosystems. Understanding the dynamics of these environments is critical to predicting the consequences of climate change on mountains and at high latitudes. Climatic differences between regions of the world could modulate the emergence of biodiversity and functionality after glacier retreat, yet global tests of this hypothesis are lacking. Nematodes are the most abundant soil animals, with keystone roles in ecosystem functioning, but the lack of global‐scale studies limits our understanding of how the taxonomic and functional diversity of nematodes changes during the colonization of proglacial landscapes. We used environmental DNA metabarcoding to characterize nematode communities of 48 glacier forelands from five continents. We assessed how different facets of biodiversity change with the age of deglaciated terrains and tested the hypothesis that colonization patterns are different across forelands with different climatic conditions. Nematodes colonized ice‐free areas almost immediately. Both taxonomic and functional richness quickly increased over time, but the increase in nematode diversity was modulated by climate, so that colonization started earlier in forelands with mild summer temperatures. Colder forelands initially hosted poor communities, but the colonization rate then accelerated, eventually leveling biodiversity differences between climatic regimes in the long term. Immediately after glacier retreat, communities were dominated by colonizer taxa with short generation time and r‐ecological strategy but community composition shifted through time, with increased frequency of more persister taxa with K‐ecological strategy. These changes mostly occurred through the addition of new traits instead of their replacement during succession. The effects of local climate on nematode colonization led to heterogeneous but predictable patterns around the world that likely affect soil communities and overall ecosystem development. The worldwide retreat of glaciers is expanding ice‐free areas, creating new ecosystems. Our global‐scale study reveals that deglaciation is followed by heterogeneous but predictable soil colonization dynamics by nematodes, depending on local climates. Cold forelands initially hosted limited biodiversity, but here the colonization rate was higher, so that in the long term (after ~150 years) biodiversity e
doi_str_mv 10.1111/gcb.17057
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Understanding the dynamics of these environments is critical to predicting the consequences of climate change on mountains and at high latitudes. Climatic differences between regions of the world could modulate the emergence of biodiversity and functionality after glacier retreat, yet global tests of this hypothesis are lacking. Nematodes are the most abundant soil animals, with keystone roles in ecosystem functioning, but the lack of global‐scale studies limits our understanding of how the taxonomic and functional diversity of nematodes changes during the colonization of proglacial landscapes. We used environmental DNA metabarcoding to characterize nematode communities of 48 glacier forelands from five continents. We assessed how different facets of biodiversity change with the age of deglaciated terrains and tested the hypothesis that colonization patterns are different across forelands with different climatic conditions. Nematodes colonized ice‐free areas almost immediately. Both taxonomic and functional richness quickly increased over time, but the increase in nematode diversity was modulated by climate, so that colonization started earlier in forelands with mild summer temperatures. Colder forelands initially hosted poor communities, but the colonization rate then accelerated, eventually leveling biodiversity differences between climatic regimes in the long term. Immediately after glacier retreat, communities were dominated by colonizer taxa with short generation time and r‐ecological strategy but community composition shifted through time, with increased frequency of more persister taxa with K‐ecological strategy. These changes mostly occurred through the addition of new traits instead of their replacement during succession. The effects of local climate on nematode colonization led to heterogeneous but predictable patterns around the world that likely affect soil communities and overall ecosystem development. The worldwide retreat of glaciers is expanding ice‐free areas, creating new ecosystems. Our global‐scale study reveals that deglaciation is followed by heterogeneous but predictable soil colonization dynamics by nematodes, depending on local climates. Cold forelands initially hosted limited biodiversity, but here the colonization rate was higher, so that in the long term (after ~150 years) biodiversity equalized that of mild climates, where the colonization started earlier. 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Understanding the dynamics of these environments is critical to predicting the consequences of climate change on mountains and at high latitudes. Climatic differences between regions of the world could modulate the emergence of biodiversity and functionality after glacier retreat, yet global tests of this hypothesis are lacking. Nematodes are the most abundant soil animals, with keystone roles in ecosystem functioning, but the lack of global‐scale studies limits our understanding of how the taxonomic and functional diversity of nematodes changes during the colonization of proglacial landscapes. We used environmental DNA metabarcoding to characterize nematode communities of 48 glacier forelands from five continents. We assessed how different facets of biodiversity change with the age of deglaciated terrains and tested the hypothesis that colonization patterns are different across forelands with different climatic conditions. Nematodes colonized ice‐free areas almost immediately. Both taxonomic and functional richness quickly increased over time, but the increase in nematode diversity was modulated by climate, so that colonization started earlier in forelands with mild summer temperatures. Colder forelands initially hosted poor communities, but the colonization rate then accelerated, eventually leveling biodiversity differences between climatic regimes in the long term. Immediately after glacier retreat, communities were dominated by colonizer taxa with short generation time and r‐ecological strategy but community composition shifted through time, with increased frequency of more persister taxa with K‐ecological strategy. These changes mostly occurred through the addition of new traits instead of their replacement during succession. The effects of local climate on nematode colonization led to heterogeneous but predictable patterns around the world that likely affect soil communities and overall ecosystem development. 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Francesco</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4227-2ba4523d622696605467c6be195e997d24ac24b1f75eccc307d6bb2f3f2b312a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Biodiversity</topic><topic>Climate change</topic><topic>Climatic conditions</topic><topic>Colonization</topic><topic>colonization rates</topic><topic>Community composition</topic><topic>DNA barcoding</topic><topic>Ecological succession</topic><topic>Ecosystem</topic><topic>Ecosystems</topic><topic>eDNA metabarcoding</topic><topic>Emergence</topic><topic>Environmental DNA</topic><topic>Environmental Sciences</topic><topic>functional diversity</topic><topic>Glacier retreat</topic><topic>Glaciers</topic><topic>global scale</topic><topic>Hypotheses</topic><topic>Ice Cover</topic><topic>Life Sciences</topic><topic>Local climates</topic><topic>Low income areas</topic><topic>Mountains</topic><topic>Nematoda</topic><topic>Nematodes</topic><topic>Soil</topic><topic>Soils</topic><topic>succession</topic><topic>Summer temperatures</topic><topic>Taxa</topic><topic>Taxonomy</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Guerrieri, Alessia</creatorcontrib><creatorcontrib>Cantera, Isabel</creatorcontrib><creatorcontrib>Marta, Silvio</creatorcontrib><creatorcontrib>Bonin, Aurélie</creatorcontrib><creatorcontrib>Carteron, Alexis</creatorcontrib><creatorcontrib>Ambrosini, Roberto</creatorcontrib><creatorcontrib>Caccianiga, Marco</creatorcontrib><creatorcontrib>Anthelme, Fabien</creatorcontrib><creatorcontrib>Azzoni, Roberto Sergio</creatorcontrib><creatorcontrib>Almond, Peter</creatorcontrib><creatorcontrib>Alviz Gazitúa, Pablo</creatorcontrib><creatorcontrib>Cauvy‐Fraunié, Sophie</creatorcontrib><creatorcontrib>Ceballos Lievano, Jorge Luis</creatorcontrib><creatorcontrib>Chand, Pritam</creatorcontrib><creatorcontrib>Chand Sharma, Milap</creatorcontrib><creatorcontrib>Clague, John</creatorcontrib><creatorcontrib>Cochachín Rapre, Justiniano Alejo</creatorcontrib><creatorcontrib>Compostella, Chiara</creatorcontrib><creatorcontrib>Cruz Encarnación, Rolando</creatorcontrib><creatorcontrib>Dangles, Olivier</creatorcontrib><creatorcontrib>Deline, Philip</creatorcontrib><creatorcontrib>Eger, Andre</creatorcontrib><creatorcontrib>Erokhin, Sergey</creatorcontrib><creatorcontrib>Franzetti, Andrea</creatorcontrib><creatorcontrib>Gielly, Ludovic</creatorcontrib><creatorcontrib>Gili, Fabrizio</creatorcontrib><creatorcontrib>Gobbi, Mauro</creatorcontrib><creatorcontrib>Hågvar, Sigmund</creatorcontrib><creatorcontrib>Khedim, Norine</creatorcontrib><creatorcontrib>Meneses, Rosa Isela</creatorcontrib><creatorcontrib>Peyre, Gwendolyn</creatorcontrib><creatorcontrib>Pittino, Francesca</creatorcontrib><creatorcontrib>Proietto, Angela</creatorcontrib><creatorcontrib>Rabatel, Antoine</creatorcontrib><creatorcontrib>Urseitova, Nurai</creatorcontrib><creatorcontrib>Yang, Yan</creatorcontrib><creatorcontrib>Zaginaev, Vitalii</creatorcontrib><creatorcontrib>Zerboni, Andrea</creatorcontrib><creatorcontrib>Zimmer, Anaïs</creatorcontrib><creatorcontrib>Taberlet, Pierre</creatorcontrib><creatorcontrib>Diolaiuti, Guglielmina Adele</creatorcontrib><creatorcontrib>Poulenard, Jerome</creatorcontrib><creatorcontrib>Fontaneto, Diego</creatorcontrib><creatorcontrib>Thuiller, Wilfried</creatorcontrib><creatorcontrib>Ficetola, Gentile Francesco</creatorcontrib><collection>Open Access: Wiley-Blackwell Open Access Journals</collection><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Water Resources Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science &amp; Fisheries Abstracts (ASFA) 3: Aquatic Pollution &amp; Environmental Quality</collection><collection>Aquatic Science &amp; Fisheries Abstracts (ASFA) Professional</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Global change biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Guerrieri, Alessia</au><au>Cantera, Isabel</au><au>Marta, Silvio</au><au>Bonin, Aurélie</au><au>Carteron, Alexis</au><au>Ambrosini, Roberto</au><au>Caccianiga, Marco</au><au>Anthelme, Fabien</au><au>Azzoni, Roberto Sergio</au><au>Almond, Peter</au><au>Alviz Gazitúa, Pablo</au><au>Cauvy‐Fraunié, Sophie</au><au>Ceballos Lievano, Jorge Luis</au><au>Chand, Pritam</au><au>Chand Sharma, Milap</au><au>Clague, John</au><au>Cochachín Rapre, Justiniano Alejo</au><au>Compostella, Chiara</au><au>Cruz Encarnación, Rolando</au><au>Dangles, Olivier</au><au>Deline, Philip</au><au>Eger, Andre</au><au>Erokhin, Sergey</au><au>Franzetti, Andrea</au><au>Gielly, Ludovic</au><au>Gili, Fabrizio</au><au>Gobbi, Mauro</au><au>Hågvar, Sigmund</au><au>Khedim, Norine</au><au>Meneses, Rosa Isela</au><au>Peyre, Gwendolyn</au><au>Pittino, Francesca</au><au>Proietto, Angela</au><au>Rabatel, Antoine</au><au>Urseitova, Nurai</au><au>Yang, Yan</au><au>Zaginaev, Vitalii</au><au>Zerboni, Andrea</au><au>Zimmer, Anaïs</au><au>Taberlet, Pierre</au><au>Diolaiuti, Guglielmina Adele</au><au>Poulenard, Jerome</au><au>Fontaneto, Diego</au><au>Thuiller, Wilfried</au><au>Ficetola, Gentile Francesco</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Local climate modulates the development of soil nematode communities after glacier retreat</atitle><jtitle>Global change biology</jtitle><addtitle>Glob Chang Biol</addtitle><date>2024-01</date><risdate>2024</risdate><volume>30</volume><issue>1</issue><spage>e17057</spage><epage>n/a</epage><pages>e17057-n/a</pages><issn>1354-1013</issn><eissn>1365-2486</eissn><notes>Died January 5, 2023.</notes><notes>Alessia Guerrieri, Isabel Cantera, Silvio Marta, Aurélie Bonin, Diego Fontaneto, Wilfried Thuiller, and Gentile Francesco Ficetola contributed equally to this work.</notes><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>The worldwide retreat of glaciers is causing a faster than ever increase in ice‐free areas that are leading to the emergence of new ecosystems. Understanding the dynamics of these environments is critical to predicting the consequences of climate change on mountains and at high latitudes. Climatic differences between regions of the world could modulate the emergence of biodiversity and functionality after glacier retreat, yet global tests of this hypothesis are lacking. Nematodes are the most abundant soil animals, with keystone roles in ecosystem functioning, but the lack of global‐scale studies limits our understanding of how the taxonomic and functional diversity of nematodes changes during the colonization of proglacial landscapes. We used environmental DNA metabarcoding to characterize nematode communities of 48 glacier forelands from five continents. We assessed how different facets of biodiversity change with the age of deglaciated terrains and tested the hypothesis that colonization patterns are different across forelands with different climatic conditions. Nematodes colonized ice‐free areas almost immediately. Both taxonomic and functional richness quickly increased over time, but the increase in nematode diversity was modulated by climate, so that colonization started earlier in forelands with mild summer temperatures. Colder forelands initially hosted poor communities, but the colonization rate then accelerated, eventually leveling biodiversity differences between climatic regimes in the long term. Immediately after glacier retreat, communities were dominated by colonizer taxa with short generation time and r‐ecological strategy but community composition shifted through time, with increased frequency of more persister taxa with K‐ecological strategy. These changes mostly occurred through the addition of new traits instead of their replacement during succession. The effects of local climate on nematode colonization led to heterogeneous but predictable patterns around the world that likely affect soil communities and overall ecosystem development. The worldwide retreat of glaciers is expanding ice‐free areas, creating new ecosystems. Our global‐scale study reveals that deglaciation is followed by heterogeneous but predictable soil colonization dynamics by nematodes, depending on local climates. Cold forelands initially hosted limited biodiversity, but here the colonization rate was higher, so that in the long term (after ~150 years) biodiversity equalized that of mild climates, where the colonization started earlier. Nematode communities experienced functional changes involving a shift from communities dominated by fast‐reproducing taxa (r‐ecological strategy) to an increased frequency of more persister taxa (K‐strategy) during colonization.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>38273541</pmid><doi>10.1111/gcb.17057</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0002-9020-9005</orcidid><orcidid>https://orcid.org/0000-0001-8850-610X</orcidid><orcidid>https://orcid.org/0000-0003-3161-1878</orcidid><orcidid>https://orcid.org/0000-0003-0858-7603</orcidid><orcidid>https://orcid.org/0000-0001-7800-8609</orcidid><orcidid>https://orcid.org/0000-0002-5304-1055</orcidid><orcidid>https://orcid.org/0000-0001-8703-9634</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1354-1013
ispartof Global change biology, 2024-01, Vol.30 (1), p.e17057-n/a
issn 1354-1013
1365-2486
language eng
recordid cdi_hal_primary_oai_HAL_hal_04381078v1
source Wiley Online Library
subjects Animals
Biodiversity
Climate change
Climatic conditions
Colonization
colonization rates
Community composition
DNA barcoding
Ecological succession
Ecosystem
Ecosystems
eDNA metabarcoding
Emergence
Environmental DNA
Environmental Sciences
functional diversity
Glacier retreat
Glaciers
global scale
Hypotheses
Ice Cover
Life Sciences
Local climates
Low income areas
Mountains
Nematoda
Nematodes
Soil
Soils
succession
Summer temperatures
Taxa
Taxonomy
title Local climate modulates the development of soil nematode communities after glacier retreat
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