Handling by avian frugivores affects diaspore secondary removal

Abstract

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.

Topsoil disturbance reshapes diaspore interactions with ground‐foraging animals in a megadiverse grassland

“…In fact, it is sustained by the significant differences found between treatments (vertebrate-exclosure vs. control) in both preserved and disturbed sites, with higher removal rates for all species in the control treatment, meaning that vertebrates do remove between 5% and 16% of diaspores depending on site type and plant species. Guerra et al (2018) showed that vertebrates can be important as secondary seed dispersers and seed predators in campo rupestre. Therefore, these results call for con- The predominance of short dispersal distances (<5 cm) in our experiments are in accord with evidence showing ants as short-distance seed dispersers (Camargo, Martins, Feitosa, & Christianini, 2016, Christianini & Oliveira, 2010Gómez & Espadaler, 2013;Guerra et al, 2018).…”

“…Guerra et al (2018) showed that vertebrates can be important as secondary seed dispersers and seed predators in campo rupestre. Therefore, these results call for con- The predominance of short dispersal distances (<5 cm) in our experiments are in accord with evidence showing ants as short-distance seed dispersers (Camargo, Martins, Feitosa, & Christianini, 2016, Christianini & Oliveira, 2010Gómez & Espadaler, 2013;Guerra et al, 2018). The majority of species observed are small ant species, suggesting that disperser body size is a key trait determining the outcomes of ant-plant interactions (Magalhães et al, 2018;Warren & Giladi, 2014).…”

“…Ants are well-known as seed predators (Costa, Vasconcelos, & Bruna, 2017;Retana, Pico, & Rodrigo, 2004), but they can also play an important role as seed dispersers in Neotropical savannas (Christianini & Oliveira, 2009, often improving seed survival and germination by feeding upon fruit pulp and cleaning seeds, which become less vulnerable to pathogen attack (Christianini, Mayhé-Nunes, & Oliveira, 2007;Passos & Oliveira, 2003). Even though most diaspores in Neotropical savannas do not present any apparent characteristics that promote ant dispersal (Christianini & Oliveira, 2010), evidence suggests ants to be important seed dispersers of non-myrmecochorous plant species (Christianini et al, 2007;Christianini & Oliveira, 2009Guerra et al, 2018;Leal & Oliveira, 1998;Lima, Oliveira, & Silveira, 2013 Hopper, Silveira, & Fiedler, 2016), encompasses old-growth fire-prone tropical grasslands, associated with extremely poor soils on ancient mountaintops that harbours a highly diversified flora with remarkable levels of plant endemism (Colli-Silva, Vasconcelos, & Pirani, 2019;Echternacht, Trovó, Oliveira, & Pirani, 2011;Silveira et al, 2016). Nevertheless, over the past decades, the vegetation dynamics in these unique landscapes have been hampered by anthropogenic disturbances, especially topsoil removal associated with quarrying and mining activities (Fernandes et al, 2018;Silveira et al, 2016).…”

Intrinsic and extrinsic drivers of intraspecific variation in seed dispersal are diverse and pervasive

“…Rodríguez-Pérez et al 2005; Reid and Armesto 2011; Haurez et al 2018) and in post-dispersal interactions with seed predators and secondary dispersers (e.g. Fricke et al 2016; Pan et al 2016; Guerra et al 2018).…”

Ants as diaspore removers of non‐myrmecochorous plants: a meta‐analysis

“…Overall, the ants can benefit plants on diaspore dispersal in many ways such as by the number of diaspores removed, diaspore removal distance and diaspore fate (Giladi , Leal et al , Griffiths et al , Fernandes et al ). However, the magnitude of these benefits is conditioned by several factors, both biotic and abiotic (Manzaneda et al , Gallegos et al , Guerra et al , Magalhães et al ). We can highlight four main factors that can directly affect the number of diaspores removed by ants, which include ant body size, diaspore size, plant growth form and habitat features.…”