Dispersal-related plant traits are associated with range size in the Atlantic Forest

Aim: The efficiency of animal-mediated seed dispersal is threatened by declines of animal populations, especially in tropical forests. We hypothesise that large-seeded plants with animal-mediated dispersal tend to have limited geographic ranges and face an increased risk of extinction due to the potential decline in seed dispersal by large-bodied fruit-eating and seed-dispersing animals (frugivores)

Location: Atlantic Forest, Brazil, South America

Taxon: Angiosperms

Methods: First, we collected dispersal-related trait (dispersal syndrome, fruit size, seed size), growth form (tree, climber, other) and preferred vegetation type (open, closed) data for 1,052 Atlantic Forest plant species. Next, we integrated these with occurrence records, extinction risk assessments, and phylogenetic trees. Finally, we performed phylogenetic generalized least squares (PGLS) regressions to test the direct and interactive effects of dispersal-related traits and vegetation type on geographical range size.

Results: Large-seeded species had smaller range sizes than small-seeded species, but only for species with animal-mediated dispersal, not for those dispersed by abiotic mechanisms. However, plants with abiotic dispersal had overall smaller range sizes than plants with animal-mediated dispersal. Furthermore, we found that species restricted to forests had smaller ranges than those occurring in open or mixed vegetation. Finally, at least 29% of the Atlantic Forest flora is threatened by extinction, but this was not related to plant dispersal syndromes.

Main Conclusions: Large-seeded plants with animal-mediated dispersal may be suffering from dispersal limitation, potentially due to past and ongoing defaunation of large-bodied frugivores, leading to small range sizes. Other factors, such as deforestation and fragmentation, will probably modulate such effects of dispersal on range size, and ultimately extinction. Our study sheds light on the relationship between plant traits, mutualistic interactions and distribution that are key to the functioning of tropical forests.

Methods
Species list and traits

We followed the Brazil Flora Group (2021) to obtain a list of accepted plant species in the Atlantic Forest. We limited our selection to angiosperms native to the Atlantic Forest, resulting in a list of 14,771 species. For those species, we assembled data on nine functional traits: fruit length, fruit width, seed length, seed width, fruit type, fruit colour, growth form, plant height and dispersal syndrome (Fig. 1), as well as information on their vegetation type. We obtained trait information through a literature survey (see Appendix 1 for references) and took measurements from specimens in two Brazilian herbaria: The Botanical Garden of Rio de Janeiro Herbarium (RB) and The Museum of Biology Mello Leitão Herbarium (MBML). We conducted our literature search using Web of Science, with the following keyword search criteria: ‘dispersal syndrome OR dispersal traits OR seed dispersal OR floristic composition OR phenology AND Atlantic Forest OR Brazil’. We restricted our search to scientific articles published in English or Portuguese. When more than one trait value per species was reported, we calculated mean values for each species.

            We classified dispersal syndrome as “animal-mediated” or “abiotic”. We categorized species as having “animal-mediated” dispersal when fruits and/or seeds were described as dispersed by animals through endozoochory (seeds are ingested and pass through the digestive tract), epizoochory (fruits or seeds have structures to attach to animal fur) or zoochory (not specified how animals transport the seeds). Species for which dispersal syndrome was not explicitly described were categorized as ‘animal-mediated’ if they had fleshy fruits (i.e., fruit type ‘drupe’ or ‘berry’) and fruit colours typical for animal dispersal syndromes, i.e., orange, red or purple (Janson, 1983; Sinnott-Armstrong et al., 2018; Valenta & Nevo, 2020). We categorized species as having “abiotic” dispersal when fruits and seeds were described as dispersed by wind (anemochory), water (hydrochory) or self-dispersal (autochory) (Fig. 1).

            We also collated information on species growth form and vegetation type from the Brazil Flora Group 2020. We classified growth form as: tree, climber or other (shrub/herb/succulent, i.e., understory growth forms). Species with multiple categories including “liana” were considered climbers. In addition, we used vegetation type to classify species into three categories: forest (i.e., closed ecosystems), field (i.e., open vegetation) or mixed (when a species occurs in both open and closed systems), following Leão, Lughadha, and Reich (2020).

Phylogenetic tree

To correct for phylogenetic non-independence of species and their traits in our models (Rezende, Lavabre, Guimarães, Jordano, & Bascompte, 2007), and to perform phylogenetically-informed trait imputations, we obtained a phylogenetic tree for the Atlantic Forest species with trait data (1,505 species available in the phylogeny), based on a backbone mega-tree, the phylogeny from Smith and Brown (2018), and using the function “phylo.maker” with “scenario 1” from the “V.Phylomaker” R package (Jin & Qian, 2019) (i.e., with new tips bound to the genus- of family-level basal nodes). This phylogeny was assembled using a hierarchical clustering analysis of DNA sequences collected from GenBank, and was resolved using data from the Open Tree of Life Project, and a backbone provided by Magallón, Gómez-Acevedo, Sánchez-Reyes, and Hernández-Hernández (2015).

Trait imputation

Because data on fruit- and seed-sizes (length and width) were only available for ca. 70% of Atlantic Forest species for which we also had dispersal syndrome information, we used phylogenetic trait imputation based on a maximum likelihood method in the “phylopars” R package (Bruggeman, Heringa, & Brandt, 2009) to infer fruit and seed size data for the remaining species. This approach takes a species-by-trait matrix and assumes a Brownian motion trait evolutionary process, where trait values change stochastically along the branches of the phylogenetic tree (i.e., simulating a “random walk”), to impute a maximum likelihood trait value for each species (i.e., each tip in the phylogeny). To ensure the accuracy of the method, the trait matrix used for imputation included all numerical traits with more than 60% trait coverage for all 1,505 species in the phylogeny.

Geographical range size and threat category

To estimate geographical range sizes, we gathered species occurrence records from the Global Biodiversity Information Facility (GBIF), resulting in 1,452,901 occurrences for 1,448 species (occurrences for 73 species were missing). We selected occurrences within South America, dating from 1995 to February 2023, as occurrences before 1995 may be less accurate (Colli-Silva et al., 2020). We removed uncertain coordinates using the flagging steps in the “CoordinateCleaner” R package (Zizka et al., 2019). Specifically, we removed occurrences in the ocean or institutions (museums or universities), in capitals, country or province centroids, and occurrences with equal longitude/latitude or with zeros. The final filtered dataset included 565,667 occurrences.

To determine the geographical range size of each species, we used their occurrence records to calculate the extent of occurrence (EOO) and area of occupancy (AOO). This was achieved by using the “IUCN.eval” function from the “ConR” R package (Dauby et al., 2017). EOO is the area contained within the shortest continuous boundary that can be drawn within the sites where a species occurs, and AOO is the sum of the area of all the grid cells that contain at least one occurrence point, we used a grid cell size of 4 km2 around the coordinate point. To assess whether determinants of range size differed across continental or regional scales, we measured range size based on occurrence records (1) across South America and (2) within the Atlantic Forest boundaries. Range size was estimated for species with more than 3 coordinate records; therefore, range size estimates were inferred for 1,432 species at the South America extent and 1,384 species at the Atlantic Forest extent.