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Selenium Hyperaccumulators Facilitate Selenium-Tolerant Neighbors via Phytoenrichment and Reduced Herbivory

Soil surrounding selenium (Se) hyperaccumulator plants was shown earlier to be enriched in Se, impairing the growth of Se-sensitive plant species. Because Se levels in neighbors of hyperaccumulators were higher and Se has been shown to protect plants from herbivory, we investigate here the potential...

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Published in:Current biology 2011-09, Vol.21 (17), p.1440-1449
Main Authors: El Mehdawi, Ali F., Quinn, Colin F., Pilon-Smits, Elizabeth A.H.
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description Soil surrounding selenium (Se) hyperaccumulator plants was shown earlier to be enriched in Se, impairing the growth of Se-sensitive plant species. Because Se levels in neighbors of hyperaccumulators were higher and Se has been shown to protect plants from herbivory, we investigate here the potential facilitating effect of Se hyperaccumulators on Se-tolerant neighboring species in the field. We measured growth and herbivory of Artemisia ludoviciana and Symphyotrichum ericoides as a function of their Se concentration and proximity to hyperaccumulators Astragalus bisulcatus and Stanleya pinnata. When growing next to hyperaccumulators, A. ludoviciana and S. ericoides contained 10- to 20-fold higher Se levels (800–2,000 mg kg −1 DW) than when growing next to nonaccumulators. The roots of both species were predominantly (70%–90%) directed toward hyperaccumulator neighbors, not toward other neighbors. Moreover, neighbors of hyperaccumulators were 2-fold bigger, showed 2-fold less herbivory damage, and harbored 3- to 4-fold fewer arthropods. When used in laboratory choice and nonchoice grasshopper herbivory experiments, Se-rich neighbors of hyperaccumulators experienced less herbivory and caused higher grasshopper Se accumulation (10-fold) and mortality (4-fold). Enhanced soil Se levels around hyperaccumulators can facilitate growth of Se-tolerant plant species through reduced herbivory and enhanced growth. This study is the first to show facilitation via enrichment with a nonessential element. It is interesting that Se enrichment of hyperaccumulator neighbors may affect competition in two ways, by reducing growth of Se-sensitive neighbors while facilitating Se-tolerant neighbors. Via these competitive and facilitating effects, Se hyperaccumulators may affect plant community composition and, consequently, higher trophic levels. ► Selenium hyperaccumulators can facilitate the growth of Se-tolerant neighbors ► Neighbors of Se hyperaccumulator plants were 10- to 20-fold enriched with Se ► The Se-enriched neighbors were 2-fold bigger and enjoyed reduced herbivory ► Se-rich neighbors caused higher grasshopper Se accumulation and mortality
doi_str_mv 10.1016/j.cub.2011.07.033
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Because Se levels in neighbors of hyperaccumulators were higher and Se has been shown to protect plants from herbivory, we investigate here the potential facilitating effect of Se hyperaccumulators on Se-tolerant neighboring species in the field. We measured growth and herbivory of Artemisia ludoviciana and Symphyotrichum ericoides as a function of their Se concentration and proximity to hyperaccumulators Astragalus bisulcatus and Stanleya pinnata. When growing next to hyperaccumulators, A. ludoviciana and S. ericoides contained 10- to 20-fold higher Se levels (800–2,000 mg kg −1 DW) than when growing next to nonaccumulators. The roots of both species were predominantly (70%–90%) directed toward hyperaccumulator neighbors, not toward other neighbors. Moreover, neighbors of hyperaccumulators were 2-fold bigger, showed 2-fold less herbivory damage, and harbored 3- to 4-fold fewer arthropods. 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Via these competitive and facilitating effects, Se hyperaccumulators may affect plant community composition and, consequently, higher trophic levels. ► Selenium hyperaccumulators can facilitate the growth of Se-tolerant neighbors ► Neighbors of Se hyperaccumulator plants were 10- to 20-fold enriched with Se ► The Se-enriched neighbors were 2-fold bigger and enjoyed reduced herbivory ► Se-rich neighbors caused higher grasshopper Se accumulation and mortality</description><identifier>ISSN: 0960-9822</identifier><identifier>EISSN: 1879-0445</identifier><identifier>DOI: 10.1016/j.cub.2011.07.033</identifier><identifier>PMID: 21856156</identifier><language>eng</language><publisher>England: Elsevier Inc</publisher><subject>Animals ; Artemisia ludoviciana ; Arthropoda ; arthropods ; Asteraceae - growth &amp; development ; Asteraceae - metabolism ; Astragalus bisulcatus ; Astragalus Plant - growth &amp; development ; Astragalus Plant - metabolism ; botanical composition ; Brassicaceae - growth &amp; development ; Brassicaceae - metabolism ; Colorado ; Food Preferences ; grasshoppers ; Grasshoppers - metabolism ; Grasshoppers - physiology ; herbivores ; Herbivory ; hyperaccumulators ; mortality ; Plant Leaves - growth &amp; development ; Plant Leaves - metabolism ; Plant Roots - growth &amp; development ; Plant Roots - metabolism ; Population Dynamics ; roots ; selenium ; Selenium - analysis ; Selenium - metabolism ; soil ; Soil - chemistry ; Stanleya ; Stanleya pinnata ; Symphyotrichum ericoides</subject><ispartof>Current biology, 2011-09, Vol.21 (17), p.1440-1449</ispartof><rights>2011 Elsevier Ltd</rights><rights>Copyright © 2011 Elsevier Ltd. 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Because Se levels in neighbors of hyperaccumulators were higher and Se has been shown to protect plants from herbivory, we investigate here the potential facilitating effect of Se hyperaccumulators on Se-tolerant neighboring species in the field. We measured growth and herbivory of Artemisia ludoviciana and Symphyotrichum ericoides as a function of their Se concentration and proximity to hyperaccumulators Astragalus bisulcatus and Stanleya pinnata. When growing next to hyperaccumulators, A. ludoviciana and S. ericoides contained 10- to 20-fold higher Se levels (800–2,000 mg kg −1 DW) than when growing next to nonaccumulators. The roots of both species were predominantly (70%–90%) directed toward hyperaccumulator neighbors, not toward other neighbors. Moreover, neighbors of hyperaccumulators were 2-fold bigger, showed 2-fold less herbivory damage, and harbored 3- to 4-fold fewer arthropods. When used in laboratory choice and nonchoice grasshopper herbivory experiments, Se-rich neighbors of hyperaccumulators experienced less herbivory and caused higher grasshopper Se accumulation (10-fold) and mortality (4-fold). Enhanced soil Se levels around hyperaccumulators can facilitate growth of Se-tolerant plant species through reduced herbivory and enhanced growth. This study is the first to show facilitation via enrichment with a nonessential element. It is interesting that Se enrichment of hyperaccumulator neighbors may affect competition in two ways, by reducing growth of Se-sensitive neighbors while facilitating Se-tolerant neighbors. Via these competitive and facilitating effects, Se hyperaccumulators may affect plant community composition and, consequently, higher trophic levels. ► Selenium hyperaccumulators can facilitate the growth of Se-tolerant neighbors ► Neighbors of Se hyperaccumulator plants were 10- to 20-fold enriched with Se ► The Se-enriched neighbors were 2-fold bigger and enjoyed reduced herbivory ► Se-rich neighbors caused higher grasshopper Se accumulation and mortality</description><subject>Animals</subject><subject>Artemisia ludoviciana</subject><subject>Arthropoda</subject><subject>arthropods</subject><subject>Asteraceae - growth &amp; development</subject><subject>Asteraceae - metabolism</subject><subject>Astragalus bisulcatus</subject><subject>Astragalus Plant - growth &amp; development</subject><subject>Astragalus Plant - metabolism</subject><subject>botanical composition</subject><subject>Brassicaceae - growth &amp; development</subject><subject>Brassicaceae - metabolism</subject><subject>Colorado</subject><subject>Food Preferences</subject><subject>grasshoppers</subject><subject>Grasshoppers - metabolism</subject><subject>Grasshoppers - physiology</subject><subject>herbivores</subject><subject>Herbivory</subject><subject>hyperaccumulators</subject><subject>mortality</subject><subject>Plant Leaves - growth &amp; development</subject><subject>Plant Leaves - metabolism</subject><subject>Plant Roots - growth &amp; development</subject><subject>Plant Roots - metabolism</subject><subject>Population Dynamics</subject><subject>roots</subject><subject>selenium</subject><subject>Selenium - analysis</subject><subject>Selenium - metabolism</subject><subject>soil</subject><subject>Soil - chemistry</subject><subject>Stanleya</subject><subject>Stanleya pinnata</subject><subject>Symphyotrichum ericoides</subject><issn>0960-9822</issn><issn>1879-0445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><recordid>eNqFkU1vEzEQhi0EoqHwA7jA3jjtMmOvv8QJVS2pVAGi7dlyvJPGYT-CvRsp_56N0nIspznMM69G78PYe4QKAdXnbRWmVcUBsQJdgRAv2AKNtiXUtXzJFmAVlNZwfsbe5LwFQG6ses3OOBqpUKoF-31LLfVx6orlYUfJhzB1U-vHIeXiyofYxtGPVDxR5d3QzlQ_Ft8pPmxWR2wfffFzcxgH6lMMm47mre-b4hc1U6CmWFJaxf2QDm_Zq7VvM717nOfs_ury7mJZ3vz4dn3x9aYMtcSx9MIqi1zahhCtBtCCk1-TlJqjksFLDJq0NByEhZo3xkqtGiMF17IxQpyzT6fcXRr-TJRH18UcqG19T8OUnUUDtUaO_yWNBaWVUGYm8USGNOScaO12KXY-HRyCO8pwWzfLcEcZDrSbZcw3Hx7Tp1VHzb-Lp_Zn4OMJWPvB-YcUs7u_nRMkAAgj8Bjx5UTQ3Nc-UnI5ROrnWmOiMLpmiM888BcRtqMO</recordid><startdate>20110913</startdate><enddate>20110913</enddate><creator>El Mehdawi, Ali F.</creator><creator>Quinn, Colin F.</creator><creator>Pilon-Smits, Elizabeth A.H.</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><scope>FBQ</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7SN</scope><scope>C1K</scope></search><sort><creationdate>20110913</creationdate><title>Selenium Hyperaccumulators Facilitate Selenium-Tolerant Neighbors via Phytoenrichment and Reduced Herbivory</title><author>El Mehdawi, Ali F. ; 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development</topic><topic>Plant Leaves - metabolism</topic><topic>Plant Roots - growth &amp; development</topic><topic>Plant Roots - metabolism</topic><topic>Population Dynamics</topic><topic>roots</topic><topic>selenium</topic><topic>Selenium - analysis</topic><topic>Selenium - metabolism</topic><topic>soil</topic><topic>Soil - chemistry</topic><topic>Stanleya</topic><topic>Stanleya pinnata</topic><topic>Symphyotrichum ericoides</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>El Mehdawi, Ali F.</creatorcontrib><creatorcontrib>Quinn, Colin F.</creatorcontrib><creatorcontrib>Pilon-Smits, Elizabeth A.H.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Ecology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><jtitle>Current biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>El Mehdawi, Ali F.</au><au>Quinn, Colin F.</au><au>Pilon-Smits, Elizabeth A.H.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Selenium Hyperaccumulators Facilitate Selenium-Tolerant Neighbors via Phytoenrichment and Reduced Herbivory</atitle><jtitle>Current biology</jtitle><addtitle>Curr Biol</addtitle><date>2011-09-13</date><risdate>2011</risdate><volume>21</volume><issue>17</issue><spage>1440</spage><epage>1449</epage><pages>1440-1449</pages><issn>0960-9822</issn><eissn>1879-0445</eissn><abstract>Soil surrounding selenium (Se) hyperaccumulator plants was shown earlier to be enriched in Se, impairing the growth of Se-sensitive plant species. Because Se levels in neighbors of hyperaccumulators were higher and Se has been shown to protect plants from herbivory, we investigate here the potential facilitating effect of Se hyperaccumulators on Se-tolerant neighboring species in the field. We measured growth and herbivory of Artemisia ludoviciana and Symphyotrichum ericoides as a function of their Se concentration and proximity to hyperaccumulators Astragalus bisulcatus and Stanleya pinnata. When growing next to hyperaccumulators, A. ludoviciana and S. ericoides contained 10- to 20-fold higher Se levels (800–2,000 mg kg −1 DW) than when growing next to nonaccumulators. The roots of both species were predominantly (70%–90%) directed toward hyperaccumulator neighbors, not toward other neighbors. Moreover, neighbors of hyperaccumulators were 2-fold bigger, showed 2-fold less herbivory damage, and harbored 3- to 4-fold fewer arthropods. When used in laboratory choice and nonchoice grasshopper herbivory experiments, Se-rich neighbors of hyperaccumulators experienced less herbivory and caused higher grasshopper Se accumulation (10-fold) and mortality (4-fold). Enhanced soil Se levels around hyperaccumulators can facilitate growth of Se-tolerant plant species through reduced herbivory and enhanced growth. This study is the first to show facilitation via enrichment with a nonessential element. It is interesting that Se enrichment of hyperaccumulator neighbors may affect competition in two ways, by reducing growth of Se-sensitive neighbors while facilitating Se-tolerant neighbors. Via these competitive and facilitating effects, Se hyperaccumulators may affect plant community composition and, consequently, higher trophic levels. ► Selenium hyperaccumulators can facilitate the growth of Se-tolerant neighbors ► Neighbors of Se hyperaccumulator plants were 10- to 20-fold enriched with Se ► The Se-enriched neighbors were 2-fold bigger and enjoyed reduced herbivory ► Se-rich neighbors caused higher grasshopper Se accumulation and mortality</abstract><cop>England</cop><pub>Elsevier Inc</pub><pmid>21856156</pmid><doi>10.1016/j.cub.2011.07.033</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record>
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identifier ISSN: 0960-9822
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subjects Animals
Artemisia ludoviciana
Arthropoda
arthropods
Asteraceae - growth & development
Asteraceae - metabolism
Astragalus bisulcatus
Astragalus Plant - growth & development
Astragalus Plant - metabolism
botanical composition
Brassicaceae - growth & development
Brassicaceae - metabolism
Colorado
Food Preferences
grasshoppers
Grasshoppers - metabolism
Grasshoppers - physiology
herbivores
Herbivory
hyperaccumulators
mortality
Plant Leaves - growth & development
Plant Leaves - metabolism
Plant Roots - growth & development
Plant Roots - metabolism
Population Dynamics
roots
selenium
Selenium - analysis
Selenium - metabolism
soil
Soil - chemistry
Stanleya
Stanleya pinnata
Symphyotrichum ericoides
title Selenium Hyperaccumulators Facilitate Selenium-Tolerant Neighbors via Phytoenrichment and Reduced Herbivory
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