Handling by avian frugivores affects diaspore secondary removal

PLOS ONE, Aug 2018

The balance between the costs and benefits of fleshy fruit production depends on the feeding behavior of their seed dispersers, which might effectively disperse seeds to farther areas or drop beneath parent plants some diaspores they handle during frugivory bouts. Nevertheless, the consequences of variation in fruit handling by primary seed dispersers on the secondary removal of diaspores remains poorly understood. We conducted a field study to determine how variation in fruit handling by avian frugivores affects short-term secondary removal of Miconia irwinii (Melastomataceae) diaspores by the ground-dwelling fauna in campo rupestre vegetation, southeastern Brazil. We conducted factorial experiments manipulating: (1) different outcomes of primary fruit/seed removal by birds, (2) distances of diaspore deposition from conspecifics, and (3) the access of ants and vertebrates to diaspores. We showed that secondary removal of diaspores was highly variable at the population scale, with an overall low removal rate by the ground-dwelling fauna (13% seeds, 19% fruits). However, we found that gut-passed seeds embedded in bird feces were less removed than seeds expelled from fruits. Gut-passed seeds were more likely to be removed by ant species acting as secondary dispersers, whereas pulp-free seeds dropped by birds were likely to interact with potential seed predators, including ants and rodents. We found no clear effect of dispersal from parent plant vicinity on seed removal, but fruit removal was significantly higher near parent plants. Partially defleshed fruits were more removed than intact fruits. The removal of fruits by ant and vertebrate rescuers, including lizards and birds, might reduce the costs of interactions with less effective dispersers that drop partially defleshed fruits under parent plants. Our study highlights that variation in fruit handling by primary avian seed dispersers mediate subsequent interactions among discarded diaspores and ground-dwelling animals, potentially affecting final seed fates. Moreover, we argue that escape-related benefits of dispersal can be contingent on how primary dispersers handle and discard seeds.

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Handling by avian frugivores affects diaspore secondary removal

August Handling by avian frugivores affects diaspore secondary removal Tadeu J. Guerra 1 2 João V. S. Messeder 1 2 Andre J. Arruda 1 2 Lisieux F. Fuzessy 1 2 Roberta L. C. Dayrell 1 2 Frederico S. Neves 0 2 Fernando A. O. Silveira 1 2 0 Departamento de Biologia Geral, Universidade Federal de Minas GeraisÐBelo Horizonte , Brazil 1 Departamento de BotaÃnica, Universidade Federal de Minas GeraisÐBelo Horizonte , Brazil 2 Editor: William Oki Wong, Indiana University Bloomington , UNITED STATES The balance between the costs and benefits of fleshy fruit production depends on the feeding behavior of their seed dispersers, which might effectively disperse seeds to farther areas or drop beneath parent plants some diaspores they handle during frugivory bouts. Nevertheless, the consequences of variation in fruit handling by primary seed dispersers on the secondary removal of diaspores remains poorly understood. We conducted a field study to determine how variation in fruit handling by avian frugivores affects short-term secondary removal of Miconia irwinii (Melastomataceae) diaspores by the ground-dwelling fauna in campo rupestre vegetation, southeastern Brazil. We conducted factorial experiments manipulating: (1) different outcomes of primary fruit/seed removal by birds, (2) distances of diaspore deposition from conspecifics, and (3) the access of ants and vertebrates to diaspores. We showed that secondary removal of diaspores was highly variable at the population scale, with an overall low removal rate by the ground-dwelling fauna (13% seeds, 19% fruits). However, we found that gut-passed seeds embedded in bird feces were less removed than seeds expelled from fruits. Gut-passed seeds were more likely to be removed by ant species acting as secondary dispersers, whereas pulp-free seeds dropped by birds were likely to interact with potential seed predators, including ants and rodents. We found no clear effect of dispersal from parent plant vicinity on seed removal, but fruit removal was significantly higher near parent plants. Partially defleshed fruits were more removed than intact fruits. The removal of fruits by ant and vertebrate rescuers, including lizards and birds, might reduce the costs of interactions with less effective dispersers that drop partially defleshed fruits under parent plants. Our study highlights that variation in fruit handling by primary avian seed dispersers mediate subsequent interactions among discarded diaspores and ground-dwelling animals, potentially affecting final seed fates. Moreover, we argue that escape-related benefits of dispersal can be contingent on how primary dispersers handle and discard seeds. - Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: Financial support was provided by FundacËão de Amparo a Pesquisa do Estado de Minas Gerais FAPEMIG (Grant#: APQ00382-17). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Also that TJ Guerra, AJ Arruda, LF Fuzessy and RLC Dayrell received scholarships from CAPES, JVS Messeder received a scholarship from FAPEMIG and FAO Silveira and FS Neves received a research productivity grant from CNPq. Introduction One of the main benefits of seed dispersal relates to escape from density-dependent attack by pathogens and predators near parent plants [1±3]. Endozoochory, in particular, involves fruit consumption and seed passage through vertebrate guts, which also may benefit plants by enhancing seed germination through coat scarification and release from germination inhibitors [ 4,5 ]. Frugivores benefit plants when they act as legitimate seed dispersers, those able to ingest seeds embedded within the fruit pulp, to defecate or regurgitate viable seeds in safe sites far from parent plants [3]. However, plants also have to cope with the costs of interacting with seed predators or with frugivores that consume the fruit pulp while dropping the diaspores at the proximity of parent trees, thus acting as ineffective seed dispersers [ 6,7 ]. Therefore, interactions with multiple frugivore species varying in their effectiveness as seed dispersers encompass both costs and benefits to fruiting plants. The fate of seeds dispersed by frugivores also depends on their secondary displacements after reaching the soil [ 8 ]. Seed predators or secondary dispersers may rearrange the spatial distribution of diaspores handled and discarded by primary dispersers, thereby directly affecting their fate [9±11]. For instance, birds are the primary seed dispersers of a large number of plant species in Neotropical ecosystems [ 12 ] and ants frequently interact with fallen diaspores of ornithochoric plants across different vegetation types [13±17]. Ants might remove seeds defecated in sites distant from the parent plants [ 13,15 ] or even rescue diaspores dropped beneath parent plants by avian frugivores [ 18,19 ]. (...truncated)


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Tadeu J. Guerra, João V. S. Messeder, André J. Arruda, Lisieux F. Fuzessy, Roberta L. C. Dayrell, Frederico S. Neves, Fernando A. O. Silveira. Handling by avian frugivores affects diaspore secondary removal, PLOS ONE, 2018, Volume 13, Issue 8, DOI: 10.1371/journal.pone.0202435