Abstract
The inability of small-gaped animals to consume very large fruits may limit seed dispersal of the respective plants. This has often been shown for large-fruited plant species that remain poorly dispersed when large-gaped animal species are lost due to anthropogenic pressure. Little is known about whether gape-size limitations similarly influence seed dispersal of small-fruited plant species that can show a large variation in fruit size within species. In this study, fruit sizes of 15 plant species were compared with the gape sizes of their 41 animal dispersers in the temperate, old-growth Białowieża Forest, Poland. The effect of gape-size limitations on fruit consumption was assessed at the plant species level, and for a subset of nine plant species, also at the individual level, and subindividual level (i.e., fruits of the same plant individual). In addition, for the species subset, fruit-seed trait relationships were investigated to determine whether a restricted access of small-gaped animals to large fruits results in the dispersal of fewer or smaller seeds per fruit. Fruit sizes widely varied among plant species (74.2%), considerably at the subindividual level (17.1%), and to the smallest extent among plant individuals (8.7%). Key disperser species should be able to consume fruits of all plant species and all individuals (except those of the largest-fruited plant species), even if they are able to consume only 28-55% of available fruits. Fruit and seed traits were positively correlated in eight out of nine plant species, indicating that gape size limitations will result in 49% fewer (in one) or 16–21% smaller seeds (in three plant species) dispersed per fruit by small-gaped than by large-gaped main dispersers, respectively. Our results show that a large subindividual variation in fruit size is characteristic for small-fruited plant species, and increases their connectedness with frugivores at the level of plants species and individuals. Simultaneously, however, the large variation in fruit size leads to gape-size limitations that may induce selective pressures on fruit size if large-gaped dispersers become extinct. This study emphasizes the mechanisms by which gape-size limitation at the species, individual and subindividual level shape plant-frugivore interactions and the co-evolution of small-fruited plants.
Highlights
The fleshy fruits of plants are an important food source for many animals (Snow and Snow, 1988; Jordano, 2014; Albrecht et al, 2018b; Quintero et al, 2020; González-Varo et al, 2021)
Because animals can poorly feed on fruits that are larger than their gape (Levey, 1987; Rey et al, 1997), the diversity of dispersing animals decreases with increasing fruit size, such that large-fruited plant species are dispersed only by a few large-gaped animals (Janzen and Martin, 1982; Guimarães et al, 2008)
Trait variation in fruit diameter was largely explained by differences among plant species (VCspecies = 1.87, 95% confidence intervals (95%CIs): 0.84–6.99)
Summary
The fleshy fruits of plants are an important food source for many animals (Snow and Snow, 1988; Jordano, 2014; Albrecht et al, 2018b; Quintero et al, 2020; González-Varo et al, 2021). The reliance of a plant species on large-gaped animals for seed dispersal may result in strong population declines, once their main dispersers become functionally lost This has been observed especially in the tropics (e.g., Galetti et al, 2013; Kurten, 2013; Correa et al, 2015; Lim et al, 2020) and on islands (e.g., Pérez-Méndez et al, 2016; Brodie, 2017; Case and Tarwater, 2020), where, following anthropogenic pressure, the inability of simplified, downsized animal communities to consume large fruits limits the regeneration of the respective plants (Terborgh et al, 2008; Brodie et al, 2009). The diameters of the vast majority of fruits and gapes are < 1.2 cm (Wheelwright, 1985; Wenny et al, 2016), and the extent to which gape-size limitations determine the interactions between small-fruited plants and small-gaped seed dispersers is unclear
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