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Species-specific effects of earthworms on microbial communities and the fate of litter-derived carbon
Soil respiration is frequently measured as a surrogate for biological activities and is important in soil carbon cycling. The heterotrophic component of soil respiration is primarily driven by microbial decomposition of leaf litter and soil organic matter, and is partially controlled by resource ava...
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Published in: | Soil biology & biochemistry 2016-09, Vol.100, p.129-139 |
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description | Soil respiration is frequently measured as a surrogate for biological activities and is important in soil carbon cycling. The heterotrophic component of soil respiration is primarily driven by microbial decomposition of leaf litter and soil organic matter, and is partially controlled by resource availability. In North American temperate deciduous forests, invasive European and Asian earthworms are known to variously affect soil properties and resource availability through their feeding, burrowing, and casting behaviors, and may affect different components of soil respiration through modulating the microbial communities. By tracing litter-derived C from 13C and 15N double-enriched leaf litter into soil and CO2 efflux in a mesocosm experiment, we tested the hypothesis that earthworms inhibit litter C-derived soil respiration by reducing resource availability and microbial biomass, and further examined how species-specific effects of earthworms on soil respiration are mediated by soil microbial community. We showed that while earthworms generally had no effect on total soil respiration, the interaction between Octolasion lacteum and Lumbricus rubellus had a significant negative non-additive effect, presumably through affecting anaerobic microsites in the soil. Moreover, litter C-derived soil respiration was reduced by the Asian Amynthas hilgendorfi, the European L. rubellus, and the North American native species Eisenoides lonnbergi, but not by the European species O. lacteum. Phospholipid fatty acid (PLFA) analysis and structural equation modeling indicated that while soil bacteria and fungi abundances were affected by earthworm species identities, the observed reduction of litter C-derived soil respiration could not be fully explained by changes in microbial biomass. We attributed these effects to earthworm-induced aggregate formation, reduction of microbial transformation of labile carbon, and antimicrobial peptide activities, and concluded that the mechanisms through which the four earthworm species affect the fate of litter-derived C and its mineralization are species-specific.
•Earthworms reduced litter carbon-derived CO2 efflux from soil.•The reduced efflux was not caused by reduced microbial biomass.•The effects of interspecific interactions were generally additive.•Interaction between Lumbricus rubellus and Octolasion lacteum had non-additive effects on C dynamics.•Species identity determined the mechanisms and pathways involved. |
doi_str_mv | 10.1016/j.soilbio.2016.06.004 |
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•Earthworms reduced litter carbon-derived CO2 efflux from soil.•The reduced efflux was not caused by reduced microbial biomass.•The effects of interspecific interactions were generally additive.•Interaction between Lumbricus rubellus and Octolasion lacteum had non-additive effects on C dynamics.•Species identity determined the mechanisms and pathways involved.</description><identifier>ISSN: 0038-0717</identifier><identifier>EISSN: 1879-3428</identifier><identifier>DOI: 10.1016/j.soilbio.2016.06.004</identifier><language>eng</language><publisher>Elsevier Ltd</publisher><subject>Amynthas ; antimicrobial peptides ; bioactive properties ; biodegradation ; burrowing ; carbon ; carbon cycle ; carbon dioxide ; deciduous forests ; Earthworm ; earthworms ; indigenous species ; Lumbricus rubellus ; microbial biomass ; microbial communities ; mineralization ; Octolasion lacteum ; Phospholipid fatty acid analysis ; phospholipid fatty acids ; plant litter ; soil aggregation ; soil bacteria ; soil fungi ; soil organic matter ; soil properties ; Soil respiration ; Stable isotope ; Structural equation modeling</subject><ispartof>Soil biology & biochemistry, 2016-09, Vol.100, p.129-139</ispartof><rights>2016 Elsevier Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c413t-f2cc17123c1d1a5ef4048bb696c1e8f5feea55e960cc5a8976946f998849c7183</citedby><cites>FETCH-LOGICAL-c413t-f2cc17123c1d1a5ef4048bb696c1e8f5feea55e960cc5a8976946f998849c7183</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids></links><search><creatorcontrib>Chang, Chih-Han</creatorcontrib><creatorcontrib>Szlavecz, Katalin</creatorcontrib><creatorcontrib>Buyer, Jeffrey S.</creatorcontrib><title>Species-specific effects of earthworms on microbial communities and the fate of litter-derived carbon</title><title>Soil biology & biochemistry</title><description>Soil respiration is frequently measured as a surrogate for biological activities and is important in soil carbon cycling. The heterotrophic component of soil respiration is primarily driven by microbial decomposition of leaf litter and soil organic matter, and is partially controlled by resource availability. In North American temperate deciduous forests, invasive European and Asian earthworms are known to variously affect soil properties and resource availability through their feeding, burrowing, and casting behaviors, and may affect different components of soil respiration through modulating the microbial communities. By tracing litter-derived C from 13C and 15N double-enriched leaf litter into soil and CO2 efflux in a mesocosm experiment, we tested the hypothesis that earthworms inhibit litter C-derived soil respiration by reducing resource availability and microbial biomass, and further examined how species-specific effects of earthworms on soil respiration are mediated by soil microbial community. We showed that while earthworms generally had no effect on total soil respiration, the interaction between Octolasion lacteum and Lumbricus rubellus had a significant negative non-additive effect, presumably through affecting anaerobic microsites in the soil. Moreover, litter C-derived soil respiration was reduced by the Asian Amynthas hilgendorfi, the European L. rubellus, and the North American native species Eisenoides lonnbergi, but not by the European species O. lacteum. Phospholipid fatty acid (PLFA) analysis and structural equation modeling indicated that while soil bacteria and fungi abundances were affected by earthworm species identities, the observed reduction of litter C-derived soil respiration could not be fully explained by changes in microbial biomass. We attributed these effects to earthworm-induced aggregate formation, reduction of microbial transformation of labile carbon, and antimicrobial peptide activities, and concluded that the mechanisms through which the four earthworm species affect the fate of litter-derived C and its mineralization are species-specific.
•Earthworms reduced litter carbon-derived CO2 efflux from soil.•The reduced efflux was not caused by reduced microbial biomass.•The effects of interspecific interactions were generally additive.•Interaction between Lumbricus rubellus and Octolasion lacteum had non-additive effects on C dynamics.•Species identity determined the mechanisms and pathways involved.</description><subject>Amynthas</subject><subject>antimicrobial peptides</subject><subject>bioactive properties</subject><subject>biodegradation</subject><subject>burrowing</subject><subject>carbon</subject><subject>carbon cycle</subject><subject>carbon dioxide</subject><subject>deciduous forests</subject><subject>Earthworm</subject><subject>earthworms</subject><subject>indigenous species</subject><subject>Lumbricus rubellus</subject><subject>microbial biomass</subject><subject>microbial communities</subject><subject>mineralization</subject><subject>Octolasion lacteum</subject><subject>Phospholipid fatty acid analysis</subject><subject>phospholipid fatty acids</subject><subject>plant litter</subject><subject>soil aggregation</subject><subject>soil bacteria</subject><subject>soil fungi</subject><subject>soil organic matter</subject><subject>soil properties</subject><subject>Soil respiration</subject><subject>Stable isotope</subject><subject>Structural equation modeling</subject><issn>0038-0717</issn><issn>1879-3428</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><recordid>eNqFkE1rGzEQhkVpoW6anxCqYy7rzOyndCrBNB9g6MH1WWi1o1pmd-VKckr_fbXY98DAMPC-M_M-jN0hrBGwfTiuo3dj7_y6zOMackH9ga1QdLKo6lJ8ZCuAShTQYfeZfYnxCABlg9WK0e5ExlEs4tKtM5ysJZMi95aTDunw14cpTzOfnAm-d3rkxk_TeXYp-7ieB54OxK1OtHhGlxKFYqDg3mjgRofez1_ZJ6vHSLfXfsP2Tz9-bV6K7c_n183jtjA1VqmwpTHYYVkZHFA3ZGuoRd-3sjVIwjaWSDcNyRaMabSQXSvr1kopRC1Nh6K6YfeXvafg_5wpJjW5aGgc9Uz-HBUKRCHbSpRZ2lykOVSMgaw6BTfp8E8hqAWrOqorVrVgVZAL6uz7dvFZ7ZX-HVxU-90iAMgPQLds_n5RUE765iiomAnPhgYXMlk1ePfOjf_WHo4a</recordid><startdate>20160901</startdate><enddate>20160901</enddate><creator>Chang, Chih-Han</creator><creator>Szlavecz, Katalin</creator><creator>Buyer, Jeffrey S.</creator><general>Elsevier Ltd</general><scope>FBQ</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7SN</scope><scope>7T7</scope><scope>7UA</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>P64</scope></search><sort><creationdate>20160901</creationdate><title>Species-specific effects of earthworms on microbial communities and the fate of litter-derived carbon</title><author>Chang, Chih-Han ; Szlavecz, Katalin ; Buyer, Jeffrey S.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c413t-f2cc17123c1d1a5ef4048bb696c1e8f5feea55e960cc5a8976946f998849c7183</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Amynthas</topic><topic>antimicrobial peptides</topic><topic>bioactive properties</topic><topic>biodegradation</topic><topic>burrowing</topic><topic>carbon</topic><topic>carbon cycle</topic><topic>carbon dioxide</topic><topic>deciduous forests</topic><topic>Earthworm</topic><topic>earthworms</topic><topic>indigenous species</topic><topic>Lumbricus rubellus</topic><topic>microbial biomass</topic><topic>microbial communities</topic><topic>mineralization</topic><topic>Octolasion lacteum</topic><topic>Phospholipid fatty acid analysis</topic><topic>phospholipid fatty acids</topic><topic>plant litter</topic><topic>soil aggregation</topic><topic>soil bacteria</topic><topic>soil fungi</topic><topic>soil organic matter</topic><topic>soil properties</topic><topic>Soil respiration</topic><topic>Stable isotope</topic><topic>Structural equation modeling</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chang, Chih-Han</creatorcontrib><creatorcontrib>Szlavecz, Katalin</creatorcontrib><creatorcontrib>Buyer, Jeffrey S.</creatorcontrib><collection>AGRIS</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Water Resources Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Biotechnology and BioEngineering Abstracts</collection><jtitle>Soil biology & biochemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chang, Chih-Han</au><au>Szlavecz, Katalin</au><au>Buyer, Jeffrey S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Species-specific effects of earthworms on microbial communities and the fate of litter-derived carbon</atitle><jtitle>Soil biology & biochemistry</jtitle><date>2016-09-01</date><risdate>2016</risdate><volume>100</volume><spage>129</spage><epage>139</epage><pages>129-139</pages><issn>0038-0717</issn><eissn>1879-3428</eissn><abstract>Soil respiration is frequently measured as a surrogate for biological activities and is important in soil carbon cycling. The heterotrophic component of soil respiration is primarily driven by microbial decomposition of leaf litter and soil organic matter, and is partially controlled by resource availability. In North American temperate deciduous forests, invasive European and Asian earthworms are known to variously affect soil properties and resource availability through their feeding, burrowing, and casting behaviors, and may affect different components of soil respiration through modulating the microbial communities. By tracing litter-derived C from 13C and 15N double-enriched leaf litter into soil and CO2 efflux in a mesocosm experiment, we tested the hypothesis that earthworms inhibit litter C-derived soil respiration by reducing resource availability and microbial biomass, and further examined how species-specific effects of earthworms on soil respiration are mediated by soil microbial community. We showed that while earthworms generally had no effect on total soil respiration, the interaction between Octolasion lacteum and Lumbricus rubellus had a significant negative non-additive effect, presumably through affecting anaerobic microsites in the soil. Moreover, litter C-derived soil respiration was reduced by the Asian Amynthas hilgendorfi, the European L. rubellus, and the North American native species Eisenoides lonnbergi, but not by the European species O. lacteum. Phospholipid fatty acid (PLFA) analysis and structural equation modeling indicated that while soil bacteria and fungi abundances were affected by earthworm species identities, the observed reduction of litter C-derived soil respiration could not be fully explained by changes in microbial biomass. We attributed these effects to earthworm-induced aggregate formation, reduction of microbial transformation of labile carbon, and antimicrobial peptide activities, and concluded that the mechanisms through which the four earthworm species affect the fate of litter-derived C and its mineralization are species-specific.
•Earthworms reduced litter carbon-derived CO2 efflux from soil.•The reduced efflux was not caused by reduced microbial biomass.•The effects of interspecific interactions were generally additive.•Interaction between Lumbricus rubellus and Octolasion lacteum had non-additive effects on C dynamics.•Species identity determined the mechanisms and pathways involved.</abstract><pub>Elsevier Ltd</pub><doi>10.1016/j.soilbio.2016.06.004</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Amynthas antimicrobial peptides bioactive properties biodegradation burrowing carbon carbon cycle carbon dioxide deciduous forests Earthworm earthworms indigenous species Lumbricus rubellus microbial biomass microbial communities mineralization Octolasion lacteum Phospholipid fatty acid analysis phospholipid fatty acids plant litter soil aggregation soil bacteria soil fungi soil organic matter soil properties Soil respiration Stable isotope Structural equation modeling |
title | Species-specific effects of earthworms on microbial communities and the fate of litter-derived carbon |
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