Subannual phenology and the effect of staggered fruit ripening on dispersal competition

Seed dispersal mutualisms evolve in complex communities of plants and frugivorous animals, within which indirect interactions such as competition and facilitation can occur. Many tropical plants reproduce subannually in multiple episodes per year. Yet, the consequences of episodic reproduction on in...

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Veröffentlicht in:Biotropica 2022-01, Vol.54 (1), p.31-41
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description Seed dispersal mutualisms evolve in complex communities of plants and frugivorous animals, within which indirect interactions such as competition and facilitation can occur. Many tropical plants reproduce subannually in multiple episodes per year. Yet, the consequences of episodic reproduction on interactions with seed dispersers remain largely unexplored. We studied Guarea guidonia (Meliaceae), a subannually reproducing tree, to examine temporal variation in seed dispersal within a tropical forested landscape in the central Dominican Republic. We hypothesized that foraging by dispersers would (a) increase with daily ripe fruit set on focal trees, (b) decrease with increasing ripe fruit biomass of neighboring plants, and (c) decrease in response to the fruiting periods of other taxa at the landscape scale. Over 18 months, we tracked the phenology of 24 focal trees and quantified foraging during fruiting phases through repeated observations, simultaneously measuring seed dispersal in traps beneath isolated bird perches across the study landscape. Date was the only clear predictor of frugivore visitation, with early and late peaks in activity during the 5‐month fruiting period. The midseason decline in foraging at focal trees matched a decline in Guarea dispersal to seed traps independently of fruit abundance. Declines in Guarea dispersal were inversely related to peak dispersal of higher quality lipid‐rich fruiting species. Our results suggest that multiple flowering episodes and subsequent asynchronous fruit ripening of low‐quality fruits can reduce competitive pressure from other higher quality fruiting species, implying that this potential bet‐hedging strategy may be an overlooked factor in the evolution of subannual reproduction. in Spanish is available with online material. Resumen La dispersión de semillas por animales frugívoros es una interacción ecológica mutualista que evoluciona en comunidades de animales y plantas complejas, que también se puede ver afectada por interacciones indirectas tales como la competencia y la facilitación. Muchas plantas tropicales se reproducen de manera subanual, con múltiples episodios de floración y fructificación durante el año. Sin embargo, las consecuencias que la reproducción en episodios subanuales tiene para las interacciones con los dispersores siguen sin estar comprendidas. Hemos usado como especie de estudio Guarea guidonia (Meliaceae), un árbol que se reproduce de manera subanual, para investigar la variaci
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Many tropical plants reproduce subannually in multiple episodes per year. Yet, the consequences of episodic reproduction on interactions with seed dispersers remain largely unexplored. We studied Guarea guidonia (Meliaceae), a subannually reproducing tree, to examine temporal variation in seed dispersal within a tropical forested landscape in the central Dominican Republic. We hypothesized that foraging by dispersers would (a) increase with daily ripe fruit set on focal trees, (b) decrease with increasing ripe fruit biomass of neighboring plants, and (c) decrease in response to the fruiting periods of other taxa at the landscape scale. Over 18 months, we tracked the phenology of 24 focal trees and quantified foraging during fruiting phases through repeated observations, simultaneously measuring seed dispersal in traps beneath isolated bird perches across the study landscape. Date was the only clear predictor of frugivore visitation, with early and late peaks in activity during the 5‐month fruiting period. The midseason decline in foraging at focal trees matched a decline in Guarea dispersal to seed traps independently of fruit abundance. Declines in Guarea dispersal were inversely related to peak dispersal of higher quality lipid‐rich fruiting species. Our results suggest that multiple flowering episodes and subsequent asynchronous fruit ripening of low‐quality fruits can reduce competitive pressure from other higher quality fruiting species, implying that this potential bet‐hedging strategy may be an overlooked factor in the evolution of subannual reproduction. in Spanish is available with online material. Resumen La dispersión de semillas por animales frugívoros es una interacción ecológica mutualista que evoluciona en comunidades de animales y plantas complejas, que también se puede ver afectada por interacciones indirectas tales como la competencia y la facilitación. Muchas plantas tropicales se reproducen de manera subanual, con múltiples episodios de floración y fructificación durante el año. Sin embargo, las consecuencias que la reproducción en episodios subanuales tiene para las interacciones con los dispersores siguen sin estar comprendidas. Hemos usado como especie de estudio Guarea guidonia (Meliaceae), un árbol que se reproduce de manera subanual, para investigar la variación temporal en la dispersión de semillas en un bosque tropical húmedo de la región central de la República Dominicana. Nuestra hipótesis era que la tasa de visitas y dispersión de semillas por los dispersores (a) aumentaría con la cantidad diaria de frutos maduros en los árboles focales, (b) disminuiría con el aumento de biomasa de los frutos maduros de las plantas vecinas, y (c) disminuiría durante los picos de fructificación de otros taxones vegetales a escala de paisaje. A lo largo de 18 meses, hemos seguido la fenología de 24 árboles focales de Guarea y hemos cuantificado mediante observaciones repetidas la tasa de visitas durante la fructificación, midiendo también de forma simultánea la dispersión de semillas en trampas colocadas debajo de perchas aisladas a lo largo del área de estudio. La fecha fue el único predictor claro de la frecuencia de visitas de aves frugívoras, con picos de actividad al principio y al final de los cinco meses de fructificación. El número de semillas de Guarea recogidas en las trampas disminuyó a mitad del período de la fructificación, independientemente de la abundancia de frutos. El descenso de la dispersión de Guarea tuvo una relación inversa con el pico de dispersión de semillas de otras especies con frutos de mayor calidad nutritiva y contenido lipídico. Los resultados sugieren que en el caso de frutos de baja calidad nutritiva, los múltiples episodios de floración y la consecuente maduración asíncrona pueden reducir la presión competitiva por parte de otras especies con frutos de mayor calidad, lo cual implica una potencial estrategia de minimización de riesgos que hasta ahora no se había considerado como un factor en la evolución de la reproducción subanual. In a study of the phenology and seed dispersal of a population of tropical tree (Guarea guidonia) in the Dominican Republic, we find that subannual flowering leads to a prolonged period of fruit ripening. Date, rather than the fruit abundance on focal trees or in neighborhood plots, was the strongest predictor of frugivore visitation, with early and late peaks in activity during the 5‐month fruiting period. The midseason decline in foraging at focal trees matched a decline in Guarea dispersal to seed traps independently of fruit abundance, and declines in Guarea dispersal were inversely related to peak dispersal of higher quality lipid‐rich fruiting species. Our results suggest that multiple flowering episodes and subsequent asynchronous fruit ripening of low‐quality fruits can reduce competitive pressure from other higher quality fruiting species, implying that this potential bet‐hedging strategy may be an overlooked factor in the evolution of subannual reproduction.</description><identifier>ISSN: 0006-3606</identifier><identifier>EISSN: 1744-7429</identifier><identifier>DOI: 10.1111/btp.13024</identifier><language>eng</language><publisher>Hoboken: Wiley Subscription Services, Inc</publisher><subject>Biological competition ; bosque tropical húmedo ; competencia ; Competition ; Dispersion ; dispersión de semillas ; Dominican Republic ; fenología subanual ; Flowering ; Foraging ; frugivory ; frugivoría ; Fruit set ; Fruits ; Guarea ; Guarea guidonia ; Lipids ; Meliaceae ; Phenology ; Reproduction ; República Dominicana ; Ripening ; Seed dispersal ; Seeds ; subannual phenology ; Temporal variations ; Traps ; Trees ; Tropical climate ; Tropical forests ; Tropical plants ; tropical wet forest</subject><ispartof>Biotropica, 2022-01, Vol.54 (1), p.31-41</ispartof><rights>2021 The Association for Tropical Biology and Conservation</rights><rights>Copyright © 2022 The Association for Tropical Biology and Conservation</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c2124-bcffa616d6065ab8e1fb01602df47b711748ecedd9e139a7b6b4e913479394583</citedby><cites>FETCH-LOGICAL-c2124-bcffa616d6065ab8e1fb01602df47b711748ecedd9e139a7b6b4e913479394583</cites><orcidid>0000-0002-9414-5758 ; 0000-0002-5841-8157</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fbtp.13024$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fbtp.13024$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids></links><search><creatorcontrib>Schubert, Spencer C.</creatorcontrib><creatorcontrib>Walters, Eric L.</creatorcontrib><title>Subannual phenology and the effect of staggered fruit ripening on dispersal competition</title><title>Biotropica</title><description>Seed dispersal mutualisms evolve in complex communities of plants and frugivorous animals, within which indirect interactions such as competition and facilitation can occur. Many tropical plants reproduce subannually in multiple episodes per year. Yet, the consequences of episodic reproduction on interactions with seed dispersers remain largely unexplored. We studied Guarea guidonia (Meliaceae), a subannually reproducing tree, to examine temporal variation in seed dispersal within a tropical forested landscape in the central Dominican Republic. We hypothesized that foraging by dispersers would (a) increase with daily ripe fruit set on focal trees, (b) decrease with increasing ripe fruit biomass of neighboring plants, and (c) decrease in response to the fruiting periods of other taxa at the landscape scale. Over 18 months, we tracked the phenology of 24 focal trees and quantified foraging during fruiting phases through repeated observations, simultaneously measuring seed dispersal in traps beneath isolated bird perches across the study landscape. Date was the only clear predictor of frugivore visitation, with early and late peaks in activity during the 5‐month fruiting period. The midseason decline in foraging at focal trees matched a decline in Guarea dispersal to seed traps independently of fruit abundance. Declines in Guarea dispersal were inversely related to peak dispersal of higher quality lipid‐rich fruiting species. Our results suggest that multiple flowering episodes and subsequent asynchronous fruit ripening of low‐quality fruits can reduce competitive pressure from other higher quality fruiting species, implying that this potential bet‐hedging strategy may be an overlooked factor in the evolution of subannual reproduction. in Spanish is available with online material. Resumen La dispersión de semillas por animales frugívoros es una interacción ecológica mutualista que evoluciona en comunidades de animales y plantas complejas, que también se puede ver afectada por interacciones indirectas tales como la competencia y la facilitación. Muchas plantas tropicales se reproducen de manera subanual, con múltiples episodios de floración y fructificación durante el año. Sin embargo, las consecuencias que la reproducción en episodios subanuales tiene para las interacciones con los dispersores siguen sin estar comprendidas. Hemos usado como especie de estudio Guarea guidonia (Meliaceae), un árbol que se reproduce de manera subanual, para investigar la variación temporal en la dispersión de semillas en un bosque tropical húmedo de la región central de la República Dominicana. Nuestra hipótesis era que la tasa de visitas y dispersión de semillas por los dispersores (a) aumentaría con la cantidad diaria de frutos maduros en los árboles focales, (b) disminuiría con el aumento de biomasa de los frutos maduros de las plantas vecinas, y (c) disminuiría durante los picos de fructificación de otros taxones vegetales a escala de paisaje. A lo largo de 18 meses, hemos seguido la fenología de 24 árboles focales de Guarea y hemos cuantificado mediante observaciones repetidas la tasa de visitas durante la fructificación, midiendo también de forma simultánea la dispersión de semillas en trampas colocadas debajo de perchas aisladas a lo largo del área de estudio. La fecha fue el único predictor claro de la frecuencia de visitas de aves frugívoras, con picos de actividad al principio y al final de los cinco meses de fructificación. El número de semillas de Guarea recogidas en las trampas disminuyó a mitad del período de la fructificación, independientemente de la abundancia de frutos. El descenso de la dispersión de Guarea tuvo una relación inversa con el pico de dispersión de semillas de otras especies con frutos de mayor calidad nutritiva y contenido lipídico. Los resultados sugieren que en el caso de frutos de baja calidad nutritiva, los múltiples episodios de floración y la consecuente maduración asíncrona pueden reducir la presión competitiva por parte de otras especies con frutos de mayor calidad, lo cual implica una potencial estrategia de minimización de riesgos que hasta ahora no se había considerado como un factor en la evolución de la reproducción subanual. In a study of the phenology and seed dispersal of a population of tropical tree (Guarea guidonia) in the Dominican Republic, we find that subannual flowering leads to a prolonged period of fruit ripening. Date, rather than the fruit abundance on focal trees or in neighborhood plots, was the strongest predictor of frugivore visitation, with early and late peaks in activity during the 5‐month fruiting period. The midseason decline in foraging at focal trees matched a decline in Guarea dispersal to seed traps independently of fruit abundance, and declines in Guarea dispersal were inversely related to peak dispersal of higher quality lipid‐rich fruiting species. Our results suggest that multiple flowering episodes and subsequent asynchronous fruit ripening of low‐quality fruits can reduce competitive pressure from other higher quality fruiting species, implying that this potential bet‐hedging strategy may be an overlooked factor in the evolution of subannual reproduction.</description><subject>Biological competition</subject><subject>bosque tropical húmedo</subject><subject>competencia</subject><subject>Competition</subject><subject>Dispersion</subject><subject>dispersión de semillas</subject><subject>Dominican Republic</subject><subject>fenología subanual</subject><subject>Flowering</subject><subject>Foraging</subject><subject>frugivory</subject><subject>frugivoría</subject><subject>Fruit set</subject><subject>Fruits</subject><subject>Guarea</subject><subject>Guarea guidonia</subject><subject>Lipids</subject><subject>Meliaceae</subject><subject>Phenology</subject><subject>Reproduction</subject><subject>República Dominicana</subject><subject>Ripening</subject><subject>Seed dispersal</subject><subject>Seeds</subject><subject>subannual phenology</subject><subject>Temporal variations</subject><subject>Traps</subject><subject>Trees</subject><subject>Tropical climate</subject><subject>Tropical forests</subject><subject>Tropical plants</subject><subject>tropical wet forest</subject><issn>0006-3606</issn><issn>1744-7429</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp1kE9LxDAQxYMouK4e_AYBTx66m6Rpuj2q-A8WFFzxGJJ20u3STWqSIvvtjdarcxkGfvPmzUPokpIFTbXUcVjQnDB-hGa05DwrOauO0YwQIrJcEHGKzkLYpbEqCJ-hj7dRK2tH1eNhC9b1rj1gZRsct4DBGKgjdgaHqNoWPDTY-LGL2HcD2M622FncdGEAH5JC7fYDxC52zp6jE6P6ABd_fY7eH-43d0_Z-uXx-e5mndWMMp7p2hglqGiSs0LpFVCjCRWENYaXuqTphRXU0DQV0LxSpRaaQ0VzXlZ5xYtVPkdXk-7g3ecIIcqdG71NJyUTjDFKSSESdT1RtXcheDBy8N1e-YOkRP7kJlNu8je3xC4n9qvr4fA_KG83r9PGN2ydb2Q</recordid><startdate>202201</startdate><enddate>202201</enddate><creator>Schubert, Spencer C.</creator><creator>Walters, Eric L.</creator><general>Wiley Subscription Services, Inc</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>P64</scope><scope>SOI</scope><orcidid>https://orcid.org/0000-0002-9414-5758</orcidid><orcidid>https://orcid.org/0000-0002-5841-8157</orcidid></search><sort><creationdate>202201</creationdate><title>Subannual phenology and the effect of staggered fruit ripening on dispersal competition</title><author>Schubert, Spencer C. ; Walters, Eric L.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c2124-bcffa616d6065ab8e1fb01602df47b711748ecedd9e139a7b6b4e913479394583</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Biological competition</topic><topic>bosque tropical húmedo</topic><topic>competencia</topic><topic>Competition</topic><topic>Dispersion</topic><topic>dispersión de semillas</topic><topic>Dominican Republic</topic><topic>fenología subanual</topic><topic>Flowering</topic><topic>Foraging</topic><topic>frugivory</topic><topic>frugivoría</topic><topic>Fruit set</topic><topic>Fruits</topic><topic>Guarea</topic><topic>Guarea guidonia</topic><topic>Lipids</topic><topic>Meliaceae</topic><topic>Phenology</topic><topic>Reproduction</topic><topic>República Dominicana</topic><topic>Ripening</topic><topic>Seed dispersal</topic><topic>Seeds</topic><topic>subannual phenology</topic><topic>Temporal variations</topic><topic>Traps</topic><topic>Trees</topic><topic>Tropical climate</topic><topic>Tropical forests</topic><topic>Tropical plants</topic><topic>tropical wet forest</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Schubert, Spencer C.</creatorcontrib><creatorcontrib>Walters, Eric L.</creatorcontrib><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment 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 &amp; Fisheries Abstracts (ASFA) 1: Biological Sciences &amp; Living Resources</collection><collection>Aquatic Science &amp; Fisheries Abstracts (ASFA) Professional</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><jtitle>Biotropica</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Schubert, Spencer C.</au><au>Walters, Eric L.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Subannual phenology and the effect of staggered fruit ripening on dispersal competition</atitle><jtitle>Biotropica</jtitle><date>2022-01</date><risdate>2022</risdate><volume>54</volume><issue>1</issue><spage>31</spage><epage>41</epage><pages>31-41</pages><issn>0006-3606</issn><eissn>1744-7429</eissn><abstract>Seed dispersal mutualisms evolve in complex communities of plants and frugivorous animals, within which indirect interactions such as competition and facilitation can occur. Many tropical plants reproduce subannually in multiple episodes per year. Yet, the consequences of episodic reproduction on interactions with seed dispersers remain largely unexplored. We studied Guarea guidonia (Meliaceae), a subannually reproducing tree, to examine temporal variation in seed dispersal within a tropical forested landscape in the central Dominican Republic. We hypothesized that foraging by dispersers would (a) increase with daily ripe fruit set on focal trees, (b) decrease with increasing ripe fruit biomass of neighboring plants, and (c) decrease in response to the fruiting periods of other taxa at the landscape scale. Over 18 months, we tracked the phenology of 24 focal trees and quantified foraging during fruiting phases through repeated observations, simultaneously measuring seed dispersal in traps beneath isolated bird perches across the study landscape. Date was the only clear predictor of frugivore visitation, with early and late peaks in activity during the 5‐month fruiting period. The midseason decline in foraging at focal trees matched a decline in Guarea dispersal to seed traps independently of fruit abundance. Declines in Guarea dispersal were inversely related to peak dispersal of higher quality lipid‐rich fruiting species. Our results suggest that multiple flowering episodes and subsequent asynchronous fruit ripening of low‐quality fruits can reduce competitive pressure from other higher quality fruiting species, implying that this potential bet‐hedging strategy may be an overlooked factor in the evolution of subannual reproduction. in Spanish is available with online material. Resumen La dispersión de semillas por animales frugívoros es una interacción ecológica mutualista que evoluciona en comunidades de animales y plantas complejas, que también se puede ver afectada por interacciones indirectas tales como la competencia y la facilitación. Muchas plantas tropicales se reproducen de manera subanual, con múltiples episodios de floración y fructificación durante el año. Sin embargo, las consecuencias que la reproducción en episodios subanuales tiene para las interacciones con los dispersores siguen sin estar comprendidas. Hemos usado como especie de estudio Guarea guidonia (Meliaceae), un árbol que se reproduce de manera subanual, para investigar la variación temporal en la dispersión de semillas en un bosque tropical húmedo de la región central de la República Dominicana. Nuestra hipótesis era que la tasa de visitas y dispersión de semillas por los dispersores (a) aumentaría con la cantidad diaria de frutos maduros en los árboles focales, (b) disminuiría con el aumento de biomasa de los frutos maduros de las plantas vecinas, y (c) disminuiría durante los picos de fructificación de otros taxones vegetales a escala de paisaje. A lo largo de 18 meses, hemos seguido la fenología de 24 árboles focales de Guarea y hemos cuantificado mediante observaciones repetidas la tasa de visitas durante la fructificación, midiendo también de forma simultánea la dispersión de semillas en trampas colocadas debajo de perchas aisladas a lo largo del área de estudio. La fecha fue el único predictor claro de la frecuencia de visitas de aves frugívoras, con picos de actividad al principio y al final de los cinco meses de fructificación. El número de semillas de Guarea recogidas en las trampas disminuyó a mitad del período de la fructificación, independientemente de la abundancia de frutos. El descenso de la dispersión de Guarea tuvo una relación inversa con el pico de dispersión de semillas de otras especies con frutos de mayor calidad nutritiva y contenido lipídico. Los resultados sugieren que en el caso de frutos de baja calidad nutritiva, los múltiples episodios de floración y la consecuente maduración asíncrona pueden reducir la presión competitiva por parte de otras especies con frutos de mayor calidad, lo cual implica una potencial estrategia de minimización de riesgos que hasta ahora no se había considerado como un factor en la evolución de la reproducción subanual. In a study of the phenology and seed dispersal of a population of tropical tree (Guarea guidonia) in the Dominican Republic, we find that subannual flowering leads to a prolonged period of fruit ripening. Date, rather than the fruit abundance on focal trees or in neighborhood plots, was the strongest predictor of frugivore visitation, with early and late peaks in activity during the 5‐month fruiting period. The midseason decline in foraging at focal trees matched a decline in Guarea dispersal to seed traps independently of fruit abundance, and declines in Guarea dispersal were inversely related to peak dispersal of higher quality lipid‐rich fruiting species. Our results suggest that multiple flowering episodes and subsequent asynchronous fruit ripening of low‐quality fruits can reduce competitive pressure from other higher quality fruiting species, implying that this potential bet‐hedging strategy may be an overlooked factor in the evolution of subannual reproduction.</abstract><cop>Hoboken</cop><pub>Wiley Subscription Services, Inc</pub><doi>10.1111/btp.13024</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-9414-5758</orcidid><orcidid>https://orcid.org/0000-0002-5841-8157</orcidid></addata></record>
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identifier ISSN: 0006-3606
ispartof Biotropica, 2022-01, Vol.54 (1), p.31-41
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1744-7429
language eng
recordid cdi_proquest_journals_2622211056
source Wiley Online Library Journals Frontfile Complete
subjects Biological competition
bosque tropical húmedo
competencia
Competition
Dispersion
dispersión de semillas
Dominican Republic
fenología subanual
Flowering
Foraging
frugivory
frugivoría
Fruit set
Fruits
Guarea
Guarea guidonia
Lipids
Meliaceae
Phenology
Reproduction
República Dominicana
Ripening
Seed dispersal
Seeds
subannual phenology
Temporal variations
Traps
Trees
Tropical climate
Tropical forests
Tropical plants
tropical wet forest
title Subannual phenology and the effect of staggered fruit ripening on dispersal competition
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