Within-Species Trait Variation Can Lead to Size Limitations in Seed Dispersal of Small-Fruited Plants

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.

Common seed dispersers contribute most to the persistence of a fleshy-fruited tree

“…In a second scenario, we tested if the animal community can keep up the effectiveness of seed dispersal when one of the four common disperser species goes extinct, and the remaining community compensates the reduced fruit removal (i.e., interaction compensation of extinct species). Our simulations showed that animals would be fully able to quantitatively compensate the interactions of lost dispersers in the IPM, because morphological mismatches between plants and their dispersers rarely occur at the species-level in small-fruited plants 76 , 77 .…”

“…In addition, before species are lost, the environment has changed in its structure and with it the effectiveness of ecological interactions 15 , 87 . Therefore, dietary preferences of animals and cryptic functional loss of interactions, rather than morphological mismatches 76 , can be expected to limit the ability of the remaining species to compensate interactions after the loss of common species in our study system. Moreover, the loss of certain animals could affect population processes that are beyond the scope of this study, for instance range expansion 32 , 88 , gene flow 89 , and plant migration in response to climate change 17 , 18 .…”

“…The ash-alder floodplain forests ( Fraxino-Alnetum community) of the Białowieża Forest are home to a diverse community of at least fifteen woody, fleshy-fruited plant species and at least 41 frugivorous animal species. The frugivore community consists of small-bodied passerines (e.g., Sylvia atricapilla, Erithacus rubecula , Turdus merula ), forest specialists (e.g., Tetrastes bonasia ), and mammals of different size (e.g., Dryomys nitedula , Martes martes , Bison bonasus ) 51 , 53 , 76 .

Fig.

…”

Consequences of intraspecific variation in seed size: does the presence of small seeds reduce predation on large ones?

“…Also, medium-sized seeds were cached more frequently across all treatments. The reason for preferences for medium-sized seeds may be that for a small granivore the largest acorns might be inconvenient to handle or simply too large to carry due to gape limitation (Muñoz and Bonal 2008;Rehling et al 2021). Moreover, granivores face a trade-off between energetic benefits and handling time that rises with seed size (Muñoz and Bonal 2008;Stephens and Krebs 2019), which may lead to preference for harvesting and caching of medium-sized seeds rather than large and small ones (Wang et al 2013).…”

Latitudinal gradients of reproductive traits in Japanese woody plants

“…Therefore, the large‐scale variability in reproductive trait expression might already trace these recently established anthropogenic gradients. It has been hypothesized that fragmented landscapes accumulate phenotypes with lower dispersal ability (Riba et al, 2009), which is often linked to larger seed and fruit sizes (Rehling et al, 2021). Transferred to plant communities, we hypothesize that the proportions of plant fruit types and dispersal strategies predictably change depending on the degree of current land use and the existing dispersal barriers like agricultural areas, forest fragments, or road traffic infrastructure.…”