DOI: 10.5061/dryad.2fqz612wm
title: Data from: Dispersal-related plant traits are associated with range size in the Atlantic Forest

description: 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.
description: <strong>Species list and traits</strong>
 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: ‘<em>dispersal
 syndrome OR dispersal traits OR seed dispersal OR floristic composition OR
 phenology AND Atlantic Forest OR Brazil’</em>. 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 “<em>animal-mediated</em>” or
 “<em>abiotic</em>”. We categorized species as having
 “<em>animal-mediated</em>” 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
 <em>‘animal-mediated’</em> 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 <em>“abiotic” </em>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).
 <strong>Phylogenetic tree</strong>
 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 km<sup>2</sup> 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.
description: # Data from: Dispersal-related plant traits are associated with range size
 in the Atlantic Forest
 [https://doi.org/10.5061/dryad.2fqz612wm](https://doi.org/10.5061/dryad.2fqz612wm) Phylogeny, trait data, range size and extinction risk estimates of plant species in the Atlantic Forest of Brazil. See data description on how the data were obtained and assembled. ## Description of the data and file structure Three data files are uploaded: the phylogeny, and two Excel files, one with trait data (raw and processed for analyses) and one with range size and extinction risk estimates. ## Sharing/Access information Data was derived from the following sources,: Alberti, L. F., Hirt, J. A. N., Junior, D. B. F. M., Steckel, M., Tombini, C. S., & Longhi, S. J. (2000). Ciência e Natura. Ciência e Natura, 22(22), 145–160. [https://doi.org/10.5902/2179460X27116](https://doi.org/10.5902/2179460X27116) Alves-Costa, C. P., & Eterovick, P. C. (2007). Seed dispersal services by coatis (Nasua nasua, Procyonidae) and their redundancy with other frugivores in southeastern Brazil. Acta Oecologica, 32(1), 77–92. [https://doi.org/10.1016/J.ACTAO.2007.03.001](https://doi.org/10.1016/J.ACTAO.2007.03.001) Barbosa, J. I. de S., da Silva, J. A., Gomes, J. M., Marangon, Lu. C., & Feliciano, A. L. P. (2014). Florística e caracterização da síndrome de dispersão de espécies arbustiva-arbóreas em fragmento de mata atlântica, Zona da Mata Norte de Pernambuco. January, 624–627. [https://doi.org/10.12702/viii.simposfloresta.2014.230-664-1](https://doi.org/10.12702/viii.simposfloresta.2014.230-664-1) Barbosa, L. M., Shirasuna, R. T., Lima, F. C. de, & Ortiz, P. R. T. (2015). Lista de espécies indicadas para Restauração Ecológica para diversas regiões do Estado de São Paulo. In VI Simpósio de Restauração Ecológica. Barros, V. M. de S., Carvalho, P. A. de, & Marangon, H. V. (2018). Caracterização da frutificação e síndrome de dispersão de espécies arbóreas em fragmentos de Mata Atlântica em Santa Bárbara do Tugúrio e Barbacena - MG. Cadernos de Agroecologia, 13(1). [http://cadernos.aba-agroecologia.org.br/cadernos/article/view/868](http://cadernos.aba-agroecologia.org.br/cadernos/article/view/868) Bello, C., Galetti, M., Montan, D., Pizo, M. A., Mariguela, T. C., Culot, L., Bufalo, F., Labecca, F., Pedrosa, F., Constantini, R., Emer, C., Silva, W. R., da Silva, F. R., Ovaskainen, O., & Jordano, P. (2017). Atlantic frugivory: a plant–frugivore interaction data set for the Atlantic Forest. Ecology, 98(6), 1729. [https://doi.org/10.1002/ECY.1818/SUPPINFO](https://doi.org/10.1002/ECY.1818/SUPPINFO) Budke, J. C., Athayde, E. A., Giehl, E. L. H., Záchia, R. A., & Eisinger, S. M. (2005). Composição florística e estratégias de dispersão de espécies lenhosas em uma floresta ribeirinha, arroio Passo das Tropas, Santa Maria, RS, Brasil. Iheringia, Série Botânica., 60(1), 17–24. [https://isb.emnuvens.com.br/iheringia/article/view/202](https://isb.emnuvens.com.br/iheringia/article/view/202) Butt, N., & Gallagher, R. (2018). Using species traits to guide conservation actions under climate change. Climatic Change, 151(2), 317–332. [https://doi.org/10.1007/S10584-018-2294-Z/TABLES/3](https://doi.org/10.1007/S10584-018-2294-Z/TABLES/3) Carvalho, F. S., & Sartori, Â. L. B. (2015). Reproductive phenology and seed dispersal syndromes of woody species in the Brazilian Chaco. Journal of Vegetation Science, 26(2), 302–311. [https://doi.org/10.1111/JVS.12227](https://doi.org/10.1111/JVS.12227) Ciconini, G., Favaro, S. P., Roscoe, R., Miranda, C. H. B., Tapeti, C. F., Miyahira, M. A. M., Bearari, L., Galvani, F., Borsato, A. v., Colnago, L. A., & Naka, M. H. (2013). Biometry and oil contents of Acrocomia aculeata fruits from the Cerrados and Pantanal biomes in Mato Grosso do Sul, Brazil. Industrial Crops and Products, 45, 208–214. [https://doi.org/10.1016/J.INDCROP.2012.12.008](https://doi.org/10.1016/J.INDCROP.2012.12.008) Corrêa, C., Corneta, C. M., Scultori, C., & von Matter, S. (n.d.). Síndromes de dispersão em fragmentos de cerrado no município de Itirapina/SP. da Silva, H. R., de Britto-Pereira, M. C., Caramaschi, U., & de Britto-Pereira, M. C. (1989). Frugivory and Seed Dispersal by Hyla truncata, a Neotropical Treefrog. Copeia, 1989(3), 781. [https://doi.org/10.2307/1445517](https://doi.org/10.2307/1445517) da Silva, M. C. N. A., & Rodal, M. J. N. (2009). Padrões das síndromes de dispersão de plantas em áreas com diferentes graus de pluviosidade, PE, Brasil. Acta Botanica Brasilica, 23(4), 1040–1047. [https://doi.org/10.1590/S0102-33062009000400014](https://doi.org/10.1590/S0102-33062009000400014) Dahl, C., Ctvrtecka, R., Gripenberg, S., Lewis, O. T., Segar, S. T., Klimes, P., Sam, K., Rinan, D., Filip, J., Lilip, R., Kongnoo, P., Panmeng, M., Putnaul, S., Reungaew, M., Rivera, M., Barrios, H., Davies, S. J., Bunyavejchewin, S., Wright, J. S., … Basset, Y. (2019). The insect-focused classification of fruit syndromes in tropical rain forests: An inter-continental comparison. Biotropica, 51(1), 39–49. [https://doi.org/10.1111/BTP.12622](https://doi.org/10.1111/BTP.12622) Dantas, V. L., & Pausas, J. G. (2020). Megafauna biogeography explains plant functional trait variability in the tropics. Global Ecology and Biogeography, 29(8), 1288–1298. [https://doi.org/10.1111/GEB.13111](https://doi.org/10.1111/GEB.13111) David, J. P., Manakadan, R., & Ganesh, T. (2015). Frugivory and seed dispersal by birds and mammals in the coastal tropical dry evergreen forests of southern India: | Ashoka Trust for Research in Ecology and the Environment. Tropical Ecology, 56(1), 41–55. [https://www.atree.org/journal-articles/frugivory-and-seed-dispersal-birds-and-mammals-coastal-tropical-dry-evergreen](https://www.atree.org/journal-articles/frugivory-and-seed-dispersal-birds-and-mammals-coastal-tropical-dry-evergreen) de Campos, É. P., Vieira, M. F., da Silva, A. F., Martins, S. V., da Silva Carmo, F. M., Moura, V. M., & de Saboya Ribeiro, A. S. (2009). Chuva de sementes em Floresta Estacional Semidecidual em Viçosa, MG, Brasil. Acta Botanica Brasilica, 23(2), 451–458. [https://doi.org/10.1590/S0102-33062009000200017](https://doi.org/10.1590/S0102-33062009000200017) De, J. I., Barbosa, S., da Silva, J. A., Gomes, J. M., Marangon, L. C., & Feliciano, A. L. P. (n.d.). Florística e caracterização da síndrome de dispersão de espécies arbustiva-arbóreas em fragmento de mata atlântica, Zona da Mata Norte de Pernambuco. [https://doi.org/10.12702/VIII.SimposFloresta.2014.230-664-1](https://doi.org/10.12702/VIII.SimposFloresta.2014.230-664-1) de Maçaneiro, J. P., de Gasper, A. L., Galvão, F., & Schorn, L. A. (2018). Dispersion and aggregation patterns of tree species in Araucaria Forest, Southern Brazil. Anais Da Academia Brasileira de Ciências, 90(2), 2397–2408. [https://doi.org/10.1590/0001-3765201820170150](https://doi.org/10.1590/0001-3765201820170150) de Melo, B. T., Mota, T., Schlindwein, C., Antonini, Y., & Oliveira, R. (2018). Floral colour change in Byrsonima variabilis (Malpighiaceae) as a visual cue for pollen but not oil foraging by oil-collecting bees. Science of Nature, 105(7–8), 1–10. [https://doi.org/10.1007/S00114-018-1572-Y/FIGURES/5](https://doi.org/10.1007/S00114-018-1572-Y/FIGURES/5) Delmas, C. E. L., Kooyman, R. M., & Rossetto, M. (2020). Evolutionary constraints and adaptation shape the size and colour of rain forest fruits and flowers at continental scale. Global Ecology and Biogeography, 29(5), 830–841. [https://doi.org/10.1111/GEB.13065](https://doi.org/10.1111/GEB.13065) Donatti, C. I., Galetti, M., Pizo, M. A., Guimarães, P. R., & Jordano, P. (2007). Living in the land of ghosts: Fruit traits and the importance of large mammals as seed dispersers in the pantanal, Brazil. Seed Dispersal: Theory and Its Application in a Changing World, 104–123. [https://doi.org/10.1079/9781845931650.0104](https://doi.org/10.1079/9781845931650.0104) D’orazio, F. de A. E., & Catharino, E. L. M. (2013). Estrutura e florística de dois fragmentos de florestas aluviais no Vale do rio Paraíba do Sul, SP, Brasil. Hoehnea, 40(3), 567–582. [https://doi.org/10.1590/S2236-89062013000300015](https://doi.org/10.1590/S2236-89062013000300015) Duarte, L. D. S., Dos-Santos, M. M. G., Hartz, S. M., & Pillar, V. D. (2006). Role of nurse plants in Araucaria Forest expansion over grassland in south Brazil. Austral Ecology, 31(4), 520–528. [https://doi.org/10.1111/J.1442-9993.2006.01602.X](https://doi.org/10.1111/J.1442-9993.2006.01602.X) Escalante, S., Montaña, C., & Orellana, R. (2004). Demography and potential extractive use of the liana palm, Desmoncus orthacanthos Martius (Arecaceae), in southern Quintana Roo, Mexico. Forest Ecology and Management, 187(1), 3–18. [https://doi.org/10.1016/S0378-1127(03)00228-7](https://doi.org/10.1016/S0378-1127\(03\)00228-7) Faria, R. A. P. G. de, Coelho, M. de F. B., Albuquerque, M. C. de F. e, & Azevedo, R. A. B. de. (2012). Phenology of Species in the Cerrado of Mato Grosso State, Brazil - Brosimum gaudichaudii Trécul (Moraceae). Phenology and Climate Change. [https://doi.org/10.5772/34960](https://doi.org/10.5772/34960) Felippi, M., Maffra, C. R. B., Cantarelli, E. B., Araújo, M. M., & Longhi, S. J. (2012). Fenologia, morfologia e análise de sementes de Cordia trichotoma (Vell.) Arráb. ex Steud. Ciência Florestal, 22(3), 631–641. [https://doi.org/10.5902/198050986629](https://doi.org/10.5902/198050986629) Ferrari, S. F., & Rímoli, J. (2008). A Primatologia no Brasil (Vol. 9, Issue 3). [https://doi.org/10.1590/s0037-86821985000300013](https://doi.org/10.1590/s0037-86821985000300013) Fortunato, M. E. M., & Quirino, Z. G. M. (2016). Effects of fragmentation on the reproductive phenology of tree species present in edge and interior of Atlantic Forest in Paraiba. Rodriguésia, 67(3), 603–614. [https://doi.org/10.1590/2175-7860201667305](https://doi.org/10.1590/2175-7860201667305) Francisco, J. J. S., Rigueiral, L. H. G., & Scabbia, R. J. A. (2019). LEVANTAMENTO FITOSSOCIOLÓGICO NO ILHOTE DA PRAIA DE CAMBURIZINHO, SÃO SEBASTIÃO, SÃO PAULO. Revista Científica UMC. Gagetti, B. L., Piratelli, A. J., & Piña-Rodrigues, F. C. M. (2016). Fruit color preference by birds and applications to ecological restoration. Brazilian Journal of Biology = Revista Brasleira de Biologia, 76(4), 955–966. [https://doi.org/10.1590/1519-6984.05115](https://doi.org/10.1590/1519-6984.05115) Galetti, M., Moleón, M., Jordano, P., Pires, M. M., Guimarães, P. R., Pape, T., Nichols, E., Hansen, D., Olesen, J. M., Munk, M., de Mattos, J. S., Schweiger, A. H., Owen-Smith, N., Johnson, C. N., Marquis, R. J., & Svenning, J. C. (2018). Ecological and evolutionary legacy of megafauna extinctions. Biological Reviews, 93(2), 845–862. [https://doi.org/10.1111/brv.12374](https://doi.org/10.1111/brv.12374) Galetti, M., Pizo, M. A., & Morellato, L. P. C. (2011). Diversity of functional traits of fleshy fruits in a species-rich Atlantic rain forest. Biota Neotropica, 11(1), 181–193. [https://doi.org/10.1590/S1676-06032011000100019](https://doi.org/10.1590/S1676-06032011000100019) Gómez, J. M., Schupp, E. W., & Jordano, P. (2019). Synzoochory: the ecological and evolutionary relevance of a dual interaction. Biological Reviews, 94(3), 874–902. [https://doi.org/10.1111/BRV.12481](https://doi.org/10.1111/BRV.12481) Gonçalves da Silva, B., Koch, I., & Piratelli, A. J. (2020). Fruit and flower availability affect bird assemblages across two successional stages in the Atlantic Forest. Studies on Neotropical Fauna and Environment, 55(3), 203–215. [https://doi.org/10.1080/01650521.2020.1743550](https://doi.org/10.1080/01650521.2020.1743550) Grenha, V., Grenha, V., Macedo, M. V. de, Pires, A. S., & Monteiro, R. F. (2010). The role of Cerradomys Subflavus (Rodentia, Cricetidae) as seed predator and disperser of the palm Allagoptera arenaria. Mastozoología Neotropical. [https://www.biodiversitylibrary.org/part/113668](https://www.biodiversitylibrary.org/part/113668) Gressler, E., Pizo, M. A., & Morellato, L. P. C. (2006). Polinização e dispersão de sementes em Myrtaceae do Brasil. Brazilian Journal of Botany, 29(4), 509–530. [https://doi.org/10.1590/S0100-84042006000400002](https://doi.org/10.1590/S0100-84042006000400002) Guerin, N., & Durigan, G. (2015). Invasion impact by Pteridium arachnoideum (Kaulf.) Maxon (Dennstaedtiaceae) on a neotropical savanna. Acta Botanica Brasilica, 29(2), 213–222. [https://doi.org/10.1590/0102-33062014ABB3722](https://doi.org/10.1590/0102-33062014ABB3722) Guimarães, P. R., Galetti, M., & Jordano, P. (2008). Seed Dispersal Anachronisms: Rethinking the Fruits Extinct Megafauna Ate. PLOS ONE, 3(3), e1745. [https://doi.org/10.1371/JOURNAL.PONE.0001745](https://doi.org/10.1371/JOURNAL.PONE.0001745) Hawes, J. E., Vieira, I. C. G., Magnago, L. F. S., Berenguer, E., Ferreira, J., Aragão, L. E. O. C., Cardoso, A., Lees, A. C., Lennox, G. D., Tobias, J. A., Waldron, A., & Barlow, J. (2020). A large-scale assessment of plant dispersal mode and seed traits across human-modified Amazonian forests. Journal of Ecology, 108(4), 1373–1385. [https://doi.org/10.1111/1365-2745.13358](https://doi.org/10.1111/1365-2745.13358) Hernández-Brito, D., Romero-Vidal, P., Hiraldo, F., Blanco, G., Díaz-Luque, J. A., Barbosa, J. M., Symes, C. T., White, T. H., Pacífico, E. C., Sebastián-González, E., Carrete, M., & Tella, J. L. (2021). Epizoochory in Parrots as an Overlooked Yet Widespread Plant–Animal Mutualism. Plants 2021, Vol. 10, Page 760, 10(4), 760. [https://doi.org/10.3390/PLANTS10040760](https://doi.org/10.3390/PLANTS10040760) Hintze, C., Heydel, F., Hoppe, C., Cunze, S., König, A., & Tackenberg, O. (2013). D3: The Dispersal and Diaspore Database – Baseline data and statistics on seed dispersal. Perspectives in Plant Ecology, Evolution and Systematics, 15(3), 180–192. [https://doi.org/10.1016/J.PPEES.2013.02.001](https://doi.org/10.1016/J.PPEES.2013.02.001) Jacobi, C. M., & do Carmo, F. F. (2011). Life-forms, pollination and seed dispersal syndromes in plant communities on ironstone outcrops, SE Brazil. Acta Botanica Brasilica, 25(2), 395–412. [https://doi.org/10.1590/S0102-33062011000200016](https://doi.org/10.1590/S0102-33062011000200016) Jara-Guerrero, A., de la Cruz, M., & Méndez, M. (2011). Seed Dispersal Spectrum of Woody Species in South Ecuadorian Dry Forests: Environmental Correlates and the Effect of Considering Species Abundance. Biotropica, 43(6), 722–730. [https://doi.org/10.1111/J.1744-7429.2011.00754.X](https://doi.org/10.1111/J.1744-7429.2011.00754.X) Kelly, D. L., Tanner, E. V. J., Lughadha, E. M. N., & Kapos, V. (1994). Floristics and Biogeography of a Rain Forest in the Venezuelan Andes. Journal of Biogeography, 21(4), 421. [https://doi.org/10.2307/2845760](https://doi.org/10.2307/2845760) Kimmel, T. M., do Nascimento, L. M., Piechowski, D., Sampaio, E. V. S. B., Rodal, M. J. N., & Gottsberger, G. (2010). Pollination and seed dispersal modes of woody species of 12-year-old secondary  forest in the Atlantic Forest region of Pernambuco, NE Brazil. Flora-Morphology, Distribution, Functional Ecology of Plants, 205(8), 540–547. [https://doi.org/10.1016/J.FLORA.2009.12.022](https://doi.org/10.1016/J.FLORA.2009.12.022) Kuhlmann, M., & Ribeiro, J. F. (2016a). Evolution of seed dispersal in the Cerrado biome: ecological and phylogenetic considerations. Acta Botanica Brasilica, 30(2), 271–282. [https://doi.org/10.1590/0102-33062015ABB0331](https://doi.org/10.1590/0102-33062015ABB0331) Kuhlmann, M., & Ribeiro, J. F. (2016b). Fruits and frugivores of the brazilian cerrado: Ecological and phylogenetic considerations. Acta Botanica Brasilica, 30(3), 495–507. [https://doi.org/10.1590/0102-33062016abb0192](https://doi.org/10.1590/0102-33062016abb0192) Laurindo, R. D. S., & Vizentin-Bugoni, J. (2020). Diversity of fruits in Artibeus lituratus diet in urban and natural habitats in Brazil: a review. Journal of Tropical Ecology, 36(2), 65–71. [https://doi.org/10.1017/S0266467419000373](https://doi.org/10.1017/S0266467419000373) Lenzi, M., Eduardo Graipel, M., Zarur de Matos, J., Martins Fraga, A., Inácio Orth, A., San Vicente del Raspeig, C., & Vicente, S. (2012). Dispersão zoocórica e hidrocórica marítima de Opuntia monacantha (Willd.) Haw. (Cactaceae). Biotemas, 25(1), 47–53. [https://doi.org/10.5007/2175-7925.2012V25N1P47](https://doi.org/10.5007/2175-7925.2012V25N1P47) Liebsch, D., Bos Mikich, S., Fernando, R., Possette, S., Osmar, E., & Ribas, S. (2009). Levantamento florístico e síndromes de dispersão em remanescentes de Floresta Ombrófila Mista na região centro-sul do estado do Paraná. Hoehnea, 36(2), 233–248. [https://doi.org/10.1590/S2236-89062009000200002](https://doi.org/10.1590/S2236-89062009000200002) Lima, M. E. L. L., Cordeiro, I., & Moreno, P. R. (2011). Estrutura do componente arbóreo em Floresta Ombrófila Densa Montana no Parque Natural Municipal Nascentes de Paranapiacaba (PNMNP), Santo André, SP, Brasil. Hoehnea, 38(1), 73–96. [https://doi.org/10.1590/S2236-89062011000100007](https://doi.org/10.1590/S2236-89062011000100007) Lomáscolo, S. B., Levey, D. J., Kimball, R. T., Bolker, B. M., & Alborn, H. T. (2010). Dispersers shape fruit diversity in Ficus (Moraceae). Proceedings of the National Academy of Sciences of the United States of America, 107(33), 14668–14672. [https://doi.org/10.1073/PNAS.1008773107/-/DCSUPPLEMENTAL](https://doi.org/10.1073/PNAS.1008773107/-/DCSUPPLEMENTAL) Lorenzi, Harri; Hermes Moreira de Souza; Judas Tadeu de Medeiros Costa; Luiz Sérgio Coelho de Cerqueira; Evandro Ferreira: Palmeiras brasileiras e exóticas cultivadas. Instituto Plantarum, Nova Odessa, 2004 ISBN 85-86714-20-8 Lucas-Filho, M. D., Silva, G. C., Cortes, S. F., Mares-Guia, T. R., Perpétua Ferraz, V., Serra, C. P., & Braga, F. C. (2010). ACE inhibition by astilbin isolated from Erythroxylum gonocladum (Mart.) O.E. Schulz. Phytomedicine : International Journal of Phytotherapy and Phytopharmacology, 17(5), 383–387. [https://doi.org/10.1016/J.PHYMED.2009.09.008](https://doi.org/10.1016/J.PHYMED.2009.09.008) Luiz Da Costa Moreira, A., Pereira Queiroz, E., & Magalhães Pigozzo, C. (2009). SÍNDROMES DE DISPERSÃO DE FRUTOS E SEMENTES DO FRAGMENTO URBANO (19o BC) DE MATA ATLÂNTICA, CABULA, SALVADOR, BAHIA. Candombá - Revista Virtual, 5(1), 13–25. Martins, R. (2005). Florística, estrutura fitossociológica e interações interespecíficas de um remanescente de floresta ombrófila densa como subsídio para a recuperação de áreas degradadas pela mineração de carvão, Siderópolis,SC. [https://repositorio.ufsc.br/handle/123456789/103027](https://repositorio.ufsc.br/handle/123456789/103027) Naniwadekar, R., Gopal, A., Page, N., Ghuman, S., Ramachandran, V., & Joshi, J. (2021). Large frugivores matter more on an island: Insights from island-mainland comparison of plant–frugivore communities. Ecology and Evolution, 11(3), 1399–1412. [https://doi.org/10.1002/ECE3.7151](https://doi.org/10.1002/ECE3.7151) Noguchi, D. K., Nunes, G. P., & Sartori, Â. L. B. (2009). Florística e síndromes de dispersão de espécies arbóreas em remanescentes de Chaco de Porto Murtinho, Mato Grosso do Sul, Brasil. Rodriguésia, 60(2), 353–365. [https://doi.org/10.1590/2175-7860200960208](https://doi.org/10.1590/2175-7860200960208) Oliveira, E. V. da S., & Landim, M. F. (2020). Dunes in the North coast of Sergipe, Brazil: plant species and their ecological traits. Rodriguésia, 71. [https://doi.org/10.1590/2175-7860202071021](https://doi.org/10.1590/2175-7860202071021) Oliveira, L. S. B., Marangon, L. C., Feliciano, A. L. P., Lima, A. S. de, Cardoso, M. de O., & Silva, V. F. da. (2011). Florística, classificação sucessional e síndromes de dispersão em um remanescente de Floresta Atlântica, Moreno-PE. Revista Brasileira de Ciências Agrárias, 6(3), 502–507. [https://doi.org/10.5039/agraria.v6i3a1384](https://doi.org/10.5039/agraria.v6i3a1384) Onstein, R. E., Kissling, W. D., Chatrou, L. W., Couvreur, T. L. P., Morlon, H., & Sauquet, H. (2019). Which frugivory-related traits facilitated historical long-distance dispersal in the custard apple family (Annonaceae)? Journal of Biogeography, 46(8), 1874–1888. [https://doi.org/10.1111/JBI.13552](https://doi.org/10.1111/JBI.13552) Osuri, A. M., Ratnam, J., Varma, V., Alvarez-Loayza, P., Astaiza, J. H., Bradford, M., Fletcher, C., Ndoundou-Hockemba, M., Jansen, P. A., Kenfack, D., Marshall, A. R., Ramesh, B. R., Rovero, F., & Sankaran, M. (2016). Contrasting effects of defaunation on aboveground carbon storage across the global tropics. Nature Communications, 7. [https://doi.org/10.1038/NCOMMS11351](https://doi.org/10.1038/NCOMMS11351) Oyama, S. de O., de Souza, L. A., Muneratto, J. C., & Albiero, A. L. M. (2010). Morphological and anatomical features of the flowers and fruits during the development of Chamissoa altissima (Jacq.) Kunth (Amaranthaceae). Brazilian Archives of Biology and Technology, 53(6), 1425–1432. [https://doi.org/10.1590/S1516-89132010000600019](https://doi.org/10.1590/S1516-89132010000600019) Pereira, L. D., Silva, D. F. P., Reis, E. F., Pinto, J. F. N., Assunção, H. F., Machado, C. G., Gomes, F. R., Carneiro, L. C., Cruz, S. C. S., & Costa, C. H. M. (2019). Characterization of Bushy Cashew (Anacardium humile A. St.-Hil.) in the State of Goiás, Brazil. Journal of Agricultural Science, 11(5), 194. [https://doi.org/10.5539/JAS.V11N5P183](https://doi.org/10.5539/JAS.V11N5P183) Pessoa, M. S., Hambuckers, A., Benchimol, M., Rocha-Santos, L., Bomfim, J. A., Faria, D., & Cazetta, E. (2017). Deforestation drives functional diversity and fruit quality changes in a tropical tree assemblage. Perspectives in Plant Ecology, Evolution and Systematics, 28, 78–86. [https://doi.org/10.1016/J.PPEES.2017.09.001](https://doi.org/10.1016/J.PPEES.2017.09.001) Pires, C. dos S., Nascimento, A. D., & Jr., E. B. de A. (2021). DISPERSÃO DE FRUTOS E SEMENTES DO COMPONENTE LENHOSO NAS DUNAS DA PRAIA DE SÃO MARCOS, SÃO LUÍS, MARANHÃO, NORDESTE DO BRASIL. Biota Amazônia (Biote Amazonie, Biota Amazonia, Amazonian Biota), 11(1), 68–74. [https://doi.org/10.18561/2179-5746/BIOTAAMAZONIA.V11N1P68-74](https://doi.org/10.18561/2179-5746/BIOTAAMAZONIA.V11N1P68-74) Pivello, V. R., Petenon, D., de Jesus, F. M., Meirelles, S. T., Vidal, M. M., Alonso, R. D. A. S., Franco, G. A. D. C., & Metzger, J. P. (2006). Chuva de sementes em fragmentos de Floresta Atlântica (São Paulo, SP, Brasil), sob diferentes situações de conectividade, estrutura florestal e proximidade da borda. Acta Botanica Brasilica, 20(4), 845–859. [https://doi.org/10.1590/S0102-33062006000400010](https://doi.org/10.1590/S0102-33062006000400010) Pizo, M. A., Silva, W. R., Galetti, M., & Laps, R. (2002). Frugivory in cotingas of the Atlantic Forest of southeast Brazil. Ararajuba, 177–185. [https://repositorio.unesp.br/handle/11449/67107](https://repositorio.unesp.br/handle/11449/67107) Possette, R. F. da S., Mikich, S. B., Hatschbach, G. G., Ribas, O. dos S., & Liebsch, D. (2015). Floristic composition and dispersal syndromes in Araucaria Forest remnants in the municipality of Colombo, Paraná state, Brazil. Check List 11(5): 1-14, 11(5), 1–14. [https://doi.org/10.15560/11.5.1771](https://doi.org/10.15560/11.5.1771) Ramos-Robles, M., Dáttilo, W., Díaz-Castelazo, C., & Andresen, E. (2018). Fruit traits and temporal abundance shape plant-frugivore interaction networks in a seasonal tropical forest. The Science of Nature, 105(3–4). [https://doi.org/10.1007/S00114-018-1556-Y](https://doi.org/10.1007/S00114-018-1556-Y) Reginato, M., Vasconcelos, T. N. C., Kriebel, R., & Simões, A. O. (2020). Is dispersal mode a driver of diversification and geographical distribution in the tropical plant family Melastomataceae? Molecular Phylogenetics and Evolution, 148, 106815. [https://doi.org/10.1016/J.YMPEV.2020.106815](https://doi.org/10.1016/J.YMPEV.2020.106815) Rego, S. S., Nogueira, A. C., Medeiros, A. C. de S., Petkowicz, C. L. de O., & Santos, Á. F. dos. (2013). Physiological behaviour of Blepharocalyx salicifolius and Casearia decandra seeds on the tolerance to dehydration. Journal of Seed Science, 35(3), 323–330. [https://doi.org/10.1590/s2317-15372013000300008](https://doi.org/10.1590/s2317-15372013000300008) Ribeiro, S. P., Londe, V., Bueno, A. P., Barbosa, J. S., Corrêa, T. L., Soeltl, T., Maia, M., Pinto, V. D., de França Dueli, G., de Sousa, H. C., Kozovits, A. R., & Nalini, H. A. (2017). Plant defense against leaf herbivory based on metal accumulation: examples from a tropical high altitude ecosystem. Plant Species Biology, 32(2), 147–155. [https://doi.org/10.1111/1442-1984.12136](https://doi.org/10.1111/1442-1984.12136) Rocha, M. J. R. da, Cupertino-Eisenlohr, M. A., Leoni, L. S., Silva, A. G. da, & Nappo, M. E. (2017). Floristic and ecological attributes of a Seasonal Semideciduous Atlantic Forest in a key area for conservation of the Zona da Mata region of Minas Gerais State, Brazil1. Hoehnea, 44(1), 29–43. [https://doi.org/10.1590/2236-8906-38/2016](https://doi.org/10.1590/2236-8906-38/2016) Sánchez, M. S., Giannini, N. P., & Barquez, R. M. (2012). Bat frugivory in two subtropical rain forests of Northern Argentina: Testing hypotheses of fruit selection in the Neotropics. Mammalian Biology, 77(1), 22–31. [https://doi.org/10.1016/J.MAMBIO.2011.06.002](https://doi.org/10.1016/J.MAMBIO.2011.06.002) Sansevero, J. B. B., Prieto, P. V., de Moraes, L. F. D., & Rodrigues, P. J. F. P. (2011). Natural Regeneration in Plantations of Native Trees in Lowland Brazilian Atlantic Forest: Community Structure, Diversity, and Dispersal Syndromes. Restoration Ecology, 19(3), 379–389. [https://doi.org/10.1111/J.1526-100X.2009.00556.X](https://doi.org/10.1111/J.1526-100X.2009.00556.X) Santos, E. N., Caxambu, M. G., da Silva, A. R., Hoppen, M. I., & Villagra, B. L. P. (2014). Trepadeiras da Floresta Estacional Semidecídua no Estado do Paraná, Brasil (pp. 107–119). Saravy, F. P., Jorgina De Freitas, P., Lage, M. A., Leite, S. J., Braga, L. F., Marcílio, E., & Sousa, P. (2003). SÍNDROME DE DISPERSÃO EM ESTRATOS ARBÓREOS EM UM FRAGMENTO DE FLORESTA OMBRÓFILA ABERTA E DENSA EM ALTA FLORESTA-MT 1. Revista Do Programa de Ciências Agro-Ambientais, Alta Floresta, 2(1), 1–12. Sebastián-González, E. (2017). Drivers of species’ role in avian seed-dispersal mutualistic networks. Journal of Animal Ecology, 86(4), 878–887. [https://doi.org/10.1111/1365-2656.12686](https://doi.org/10.1111/1365-2656.12686) Silva, R. K. S. da, Feliciano, A. L. P., Marangon, L. C., Lima, R. B. de A., & Santos, W. B. dos. (2012). Estrutura e síndromes de dispersão de espécies arbóreas em um trecho de mata ciliar, Sirinhaém, Pernambuco, Brasil. Pesquisa Florestal Brasileira, 32(69), 1–12. [https://doi.org/10.4336/2012.PFB.32.69.01](https://doi.org/10.4336/2012.PFB.32.69.01) Spina, A. P., Ferreira, W. M., & Filho, H. D. F. L. (2001). Floração, frutificação e síndromes de dispersão de uma comunidade de floresta de brejo na região de Campinas (SP). Acta Botanica Brasilica, 15(3), 349–368. [https://doi.org/10.1590/S0102-33062001000300006](https://doi.org/10.1590/S0102-33062001000300006) Staggemeier, V. G., Cazetta, E., & Morellato, L. P. C. (2017). Hyperdominance in fruit production in the Brazilian Atlantic rain forest: the functional role of plants in sustaining frugivores. Biotropica, 49(1), 71–82. [https://doi.org/10.1111/BTP.12358](https://doi.org/10.1111/BTP.12358) Stefanello, D., Fernandes-Bulhão, C., & Martins, S. V. (2009). Síndromes de dispersão de sementes em três trechos de vegetação ciliar (nascente, meio e foz) ao longo do rio Pindaíba, MT. Revista Árvore, 33(6), 1051–1061. [https://doi.org/10.1590/S0100-67622009000600008](https://doi.org/10.1590/S0100-67622009000600008) Stefanello, D., Ivanauskas, N. M., Martins, S. V., Silva, E., & Kunz, S. H. (2010). Síndromes de dispersão de diásporos das espécies de trechos de vegetação ciliar do rio das Pacas, Querência - MT. Acta Amazonica, 40(1), 141–150. [https://doi.org/10.1590/S0044-59672010000100018](https://doi.org/10.1590/S0044-59672010000100018) Terra-Araujo, M. H., Faria, A. D. D., & Swenson, U. (2016). A Taxonomic Update of Neotropical Pradosia (Sapotaceae, Chrysophylloideae). Systematic Botany, 41(3), 634–650. [https://doi.org/10.1600/036364416X692389](https://doi.org/10.1600/036364416X692389) Vale, V. S. do, Schiavini, I., Oliveira, A. P. de, Custódio, O., Neto, D., & Gusson, A. E. (2013). Functional groups in a semideciduous seasonal forest in Southeastern Brazil. Biotemas, 26(2), 45–58. [https://doi.org/10.5007/2175-7925.2013V26N2P45](https://doi.org/10.5007/2175-7925.2013V26N2P45) Venzke, T. S., Martins, S. V., Neri, A. V., & Kunz, S. H. (2014). Síndromes de dispersão de sementes em estágios sucessionais de mata ciliar, no extremo sul da Mata Atlântica, Arroio do Padre, RS, Brasil. Revista Árvore, 38(3), 403–413. [https://doi.org/10.1590/S0100-67622014000300002](https://doi.org/10.1590/S0100-67622014000300002) Vidal, M. M., Hasui, E., Pizo, M. A., Tamashiro, J. Y., Silva, W. R., & Guimarães, P. R. (2014). Frugivores at higher risk of extinction are the key elements of a mutualistic network. Ecology, 95(12), 3440–3447. [https://doi.org/10.1890/13-1584.1](https://doi.org/10.1890/13-1584.1) Yamamoto, L. F., Kinoshita, L. S., & Martins, F. R. (2007). Síndromes de polinização e de dispersão em fragmentos da Floresta Estacional Semidecídua Montana, SP, Brasil. Acta Botanica Brasilica, 21(3), 553–573. [https://doi.org/10.1590/S0102-33062007000300005](https://doi.org/10.1590/S0102-33062007000300005) Yuka Zama, M., Bovolenta, Y. R., de Souza Carvalho, E., Rodrigues, D. R., Gomes De Araujo, C., Aparecida Da, M., Sorace, F., & Gimenes Luz, D. (2012). Florística e síndromes de dispersão de espécies arbustivo-arbóreas no Parque Estadual Mata São Francisco, PR, Brasil. Hoehnea, 39(3), 369–378. [https://doi.org/10.1590/S2236-89062012000300002](https://doi.org/10.1590/S2236-89062012000300002) Zanne, A. E., Tank, D. C., Cornwell, W. K., Eastman, J. M., Smith, S. A., Fitzjohn, R. G., McGlinn, D. J., O’Meara, B. C., Moles, A. T., Reich, P. B., Royer, D. L., Soltis, D. E., Stevens, P. F., Westoby, M., Wright, I. J., Aarssen, L., Bertin, R. I., Calaminus, A., Govaerts, R., … Beaulieu, J. M. (2013). Three keys to the radiation of angiosperms into freezing environments. Nature 2013 506:7486, 506(7486), 89–92. [https://doi.org/10.1038/nature12872](https://doi.org/10.1038/nature12872) Websites, Online Floras and Online Database: Fern, K., Fern, A., Morris, R., 2021. Useful Tropical Plants Database. Accessed on September 2021, URL: [http://tropical.theferns.info](http://tropical.theferns.info) Flora Malesiana 2022, accessed in on 04 February 4, 2022 URL:  [https://portal.cybertaxonomy.org/flora-malesiana/](https://portal.cybertaxonomy.org/flora-malesiana/)