Time is of the essence: Direct and indirect effects of plant ontogenetic trajectories on higher trophic levels

Autores
Quintero, Carolina; Lampert, Evan C.; Bowers, M. Deane
Año de publicación
2014
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Physiological and morphological constraints during plant ontogeny affect the expression of numerous plant traits relevant to higher trophic levels, such as nutritional content and physical and chemical defenses. Yet we know little about how temporal variation in these traits can directly and/or indirectly mediate tri-trophic interactions, such as those between plants, their herbivores, and herbivore natural enemies. Using four distinct ontogenetic stages of Plantago lanceolata (Plantaginaceae) and the specialist herbivore Junonia coenia (Lepidoptera, Nymphalidae), we evaluated how ontogenetic changes in plant quality can: (1) directly alter plant-herbivore interactions through butterfly oviposition choice and caterpillar performance assays, and (2) indirectly alter herbivores susceptibility to higher trophic levels through caterpillars iridoid glycoside sequestration and immune defenses. Results showed that plant defensive traits increased over P. lanceolata development, with leaf tissues becoming tougher and plant allelochemicals (iridoid glycosides) occurring in higher amounts. Conversely, plant nutritional quality (water and nitrogen content) decreased as plants aged. These ontogenetic trajectories strongly altered both direct and indirect interactions between plants and higher trophic levels. Buckeye butterflies showed a stronger oviposition preference for younger developmental stages of P. lanceolata, laying on average 60% more eggs on juvenile than on reproductive plants. Feeding experiments with caterpillars showed that larvae feeding on juvenile plants showed faster relative growth rate and increased digestive efficiency compared with those feeding on plants in the reproductive stage. These individuals, however, acquired lower levels of sequestered chemical defenses than did those feeding on older P. lanceolata plants, potentially rendering them more susceptible to predation. Finally, host plant age altered the ability of a caterpillar to mount an immune response against simulated parasitoid eggs. Specifically, caterpillars reared on older plant life stages, and thus with higher levels of sequestered iridoid glycosides, showed a compromised immune response compared to those feeding on younger plant age classes. This study exemplifies how ontogenetic trajectories in plant traits can scale up to directly or indirectly alter tri-trophic interactions, which may have key implications for understanding temporal shifts in herbivore population and community structure.
Fil: Quintero, Carolina. State University Of Colorado-boulder; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Patagonia Norte. Instituto de Investigación en Biodiversidad y Medioambiente; Argentina. Universidad Nacional del Comahue. Centro Regional Universitario Bariloche. Laboratorio de Ecotono; Argentina
Fil: Lampert, Evan C.. University of North Georgia; Estados Unidos
Fil: Bowers, M. Deane. State University Of Colorado-boulder; Estados Unidos
Materia
Butterfly Oviposition Choice
Sequestration
Caterpillar Immune Response
Ontogeny
Tri-Trophic Interactions
Iridoid Glycosides
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/11902

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oai_identifier_str oai:ri.conicet.gov.ar:11336/11902
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network_name_str CONICET Digital (CONICET)
spelling Time is of the essence: Direct and indirect effects of plant ontogenetic trajectories on higher trophic levelsQuintero, CarolinaLampert, Evan C.Bowers, M. DeaneButterfly Oviposition ChoiceSequestrationCaterpillar Immune ResponseOntogenyTri-Trophic InteractionsIridoid Glycosideshttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Physiological and morphological constraints during plant ontogeny affect the expression of numerous plant traits relevant to higher trophic levels, such as nutritional content and physical and chemical defenses. Yet we know little about how temporal variation in these traits can directly and/or indirectly mediate tri-trophic interactions, such as those between plants, their herbivores, and herbivore natural enemies. Using four distinct ontogenetic stages of Plantago lanceolata (Plantaginaceae) and the specialist herbivore Junonia coenia (Lepidoptera, Nymphalidae), we evaluated how ontogenetic changes in plant quality can: (1) directly alter plant-herbivore interactions through butterfly oviposition choice and caterpillar performance assays, and (2) indirectly alter herbivores susceptibility to higher trophic levels through caterpillars iridoid glycoside sequestration and immune defenses. Results showed that plant defensive traits increased over P. lanceolata development, with leaf tissues becoming tougher and plant allelochemicals (iridoid glycosides) occurring in higher amounts. Conversely, plant nutritional quality (water and nitrogen content) decreased as plants aged. These ontogenetic trajectories strongly altered both direct and indirect interactions between plants and higher trophic levels. Buckeye butterflies showed a stronger oviposition preference for younger developmental stages of P. lanceolata, laying on average 60% more eggs on juvenile than on reproductive plants. Feeding experiments with caterpillars showed that larvae feeding on juvenile plants showed faster relative growth rate and increased digestive efficiency compared with those feeding on plants in the reproductive stage. These individuals, however, acquired lower levels of sequestered chemical defenses than did those feeding on older P. lanceolata plants, potentially rendering them more susceptible to predation. Finally, host plant age altered the ability of a caterpillar to mount an immune response against simulated parasitoid eggs. Specifically, caterpillars reared on older plant life stages, and thus with higher levels of sequestered iridoid glycosides, showed a compromised immune response compared to those feeding on younger plant age classes. This study exemplifies how ontogenetic trajectories in plant traits can scale up to directly or indirectly alter tri-trophic interactions, which may have key implications for understanding temporal shifts in herbivore population and community structure.Fil: Quintero, Carolina. State University Of Colorado-boulder; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Patagonia Norte. Instituto de Investigación en Biodiversidad y Medioambiente; Argentina. Universidad Nacional del Comahue. Centro Regional Universitario Bariloche. Laboratorio de Ecotono; ArgentinaFil: Lampert, Evan C.. University of North Georgia; Estados UnidosFil: Bowers, M. Deane. State University Of Colorado-boulder; Estados UnidosEcological Society Of America2014-09info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/11902Quintero, Carolina; Lampert, Evan C.; Bowers, M. Deane; Time is of the essence: Direct and indirect effects of plant ontogenetic trajectories on higher trophic levels; Ecological Society Of America; Ecology; 95; 9; 9-2014; 2589-26020012-9658enginfo:eu-repo/semantics/altIdentifier/url/http://onlinelibrary.wiley.com/doi/10.1890/13-2249.1/abstractinfo:eu-repo/semantics/altIdentifier/doi/10.1890/13-2249.1info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-29T11:22:45Zoai:ri.conicet.gov.ar:11336/11902instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-10-29 11:22:45.293CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Time is of the essence: Direct and indirect effects of plant ontogenetic trajectories on higher trophic levels
title Time is of the essence: Direct and indirect effects of plant ontogenetic trajectories on higher trophic levels
spellingShingle Time is of the essence: Direct and indirect effects of plant ontogenetic trajectories on higher trophic levels
Quintero, Carolina
Butterfly Oviposition Choice
Sequestration
Caterpillar Immune Response
Ontogeny
Tri-Trophic Interactions
Iridoid Glycosides
title_short Time is of the essence: Direct and indirect effects of plant ontogenetic trajectories on higher trophic levels
title_full Time is of the essence: Direct and indirect effects of plant ontogenetic trajectories on higher trophic levels
title_fullStr Time is of the essence: Direct and indirect effects of plant ontogenetic trajectories on higher trophic levels
title_full_unstemmed Time is of the essence: Direct and indirect effects of plant ontogenetic trajectories on higher trophic levels
title_sort Time is of the essence: Direct and indirect effects of plant ontogenetic trajectories on higher trophic levels
dc.creator.none.fl_str_mv Quintero, Carolina
Lampert, Evan C.
Bowers, M. Deane
author Quintero, Carolina
author_facet Quintero, Carolina
Lampert, Evan C.
Bowers, M. Deane
author_role author
author2 Lampert, Evan C.
Bowers, M. Deane
author2_role author
author
dc.subject.none.fl_str_mv Butterfly Oviposition Choice
Sequestration
Caterpillar Immune Response
Ontogeny
Tri-Trophic Interactions
Iridoid Glycosides
topic Butterfly Oviposition Choice
Sequestration
Caterpillar Immune Response
Ontogeny
Tri-Trophic Interactions
Iridoid Glycosides
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Physiological and morphological constraints during plant ontogeny affect the expression of numerous plant traits relevant to higher trophic levels, such as nutritional content and physical and chemical defenses. Yet we know little about how temporal variation in these traits can directly and/or indirectly mediate tri-trophic interactions, such as those between plants, their herbivores, and herbivore natural enemies. Using four distinct ontogenetic stages of Plantago lanceolata (Plantaginaceae) and the specialist herbivore Junonia coenia (Lepidoptera, Nymphalidae), we evaluated how ontogenetic changes in plant quality can: (1) directly alter plant-herbivore interactions through butterfly oviposition choice and caterpillar performance assays, and (2) indirectly alter herbivores susceptibility to higher trophic levels through caterpillars iridoid glycoside sequestration and immune defenses. Results showed that plant defensive traits increased over P. lanceolata development, with leaf tissues becoming tougher and plant allelochemicals (iridoid glycosides) occurring in higher amounts. Conversely, plant nutritional quality (water and nitrogen content) decreased as plants aged. These ontogenetic trajectories strongly altered both direct and indirect interactions between plants and higher trophic levels. Buckeye butterflies showed a stronger oviposition preference for younger developmental stages of P. lanceolata, laying on average 60% more eggs on juvenile than on reproductive plants. Feeding experiments with caterpillars showed that larvae feeding on juvenile plants showed faster relative growth rate and increased digestive efficiency compared with those feeding on plants in the reproductive stage. These individuals, however, acquired lower levels of sequestered chemical defenses than did those feeding on older P. lanceolata plants, potentially rendering them more susceptible to predation. Finally, host plant age altered the ability of a caterpillar to mount an immune response against simulated parasitoid eggs. Specifically, caterpillars reared on older plant life stages, and thus with higher levels of sequestered iridoid glycosides, showed a compromised immune response compared to those feeding on younger plant age classes. This study exemplifies how ontogenetic trajectories in plant traits can scale up to directly or indirectly alter tri-trophic interactions, which may have key implications for understanding temporal shifts in herbivore population and community structure.
Fil: Quintero, Carolina. State University Of Colorado-boulder; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Patagonia Norte. Instituto de Investigación en Biodiversidad y Medioambiente; Argentina. Universidad Nacional del Comahue. Centro Regional Universitario Bariloche. Laboratorio de Ecotono; Argentina
Fil: Lampert, Evan C.. University of North Georgia; Estados Unidos
Fil: Bowers, M. Deane. State University Of Colorado-boulder; Estados Unidos
description Physiological and morphological constraints during plant ontogeny affect the expression of numerous plant traits relevant to higher trophic levels, such as nutritional content and physical and chemical defenses. Yet we know little about how temporal variation in these traits can directly and/or indirectly mediate tri-trophic interactions, such as those between plants, their herbivores, and herbivore natural enemies. Using four distinct ontogenetic stages of Plantago lanceolata (Plantaginaceae) and the specialist herbivore Junonia coenia (Lepidoptera, Nymphalidae), we evaluated how ontogenetic changes in plant quality can: (1) directly alter plant-herbivore interactions through butterfly oviposition choice and caterpillar performance assays, and (2) indirectly alter herbivores susceptibility to higher trophic levels through caterpillars iridoid glycoside sequestration and immune defenses. Results showed that plant defensive traits increased over P. lanceolata development, with leaf tissues becoming tougher and plant allelochemicals (iridoid glycosides) occurring in higher amounts. Conversely, plant nutritional quality (water and nitrogen content) decreased as plants aged. These ontogenetic trajectories strongly altered both direct and indirect interactions between plants and higher trophic levels. Buckeye butterflies showed a stronger oviposition preference for younger developmental stages of P. lanceolata, laying on average 60% more eggs on juvenile than on reproductive plants. Feeding experiments with caterpillars showed that larvae feeding on juvenile plants showed faster relative growth rate and increased digestive efficiency compared with those feeding on plants in the reproductive stage. These individuals, however, acquired lower levels of sequestered chemical defenses than did those feeding on older P. lanceolata plants, potentially rendering them more susceptible to predation. Finally, host plant age altered the ability of a caterpillar to mount an immune response against simulated parasitoid eggs. Specifically, caterpillars reared on older plant life stages, and thus with higher levels of sequestered iridoid glycosides, showed a compromised immune response compared to those feeding on younger plant age classes. This study exemplifies how ontogenetic trajectories in plant traits can scale up to directly or indirectly alter tri-trophic interactions, which may have key implications for understanding temporal shifts in herbivore population and community structure.
publishDate 2014
dc.date.none.fl_str_mv 2014-09
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/11902
Quintero, Carolina; Lampert, Evan C.; Bowers, M. Deane; Time is of the essence: Direct and indirect effects of plant ontogenetic trajectories on higher trophic levels; Ecological Society Of America; Ecology; 95; 9; 9-2014; 2589-2602
0012-9658
url http://hdl.handle.net/11336/11902
identifier_str_mv Quintero, Carolina; Lampert, Evan C.; Bowers, M. Deane; Time is of the essence: Direct and indirect effects of plant ontogenetic trajectories on higher trophic levels; Ecological Society Of America; Ecology; 95; 9; 9-2014; 2589-2602
0012-9658
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://onlinelibrary.wiley.com/doi/10.1890/13-2249.1/abstract
info:eu-repo/semantics/altIdentifier/doi/10.1890/13-2249.1
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Ecological Society Of America
publisher.none.fl_str_mv Ecological Society Of America
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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