Beyond the forest canopy: contrasting strategies of frugivory and seed dispersal across tropical forest-savanna-grassland gradients

Beyond the forest canopy: contrasting strategies of frugivory and seed dispersal across tropical forest-savanna-grassland gradients | Authorea try { document.documentElement.classList.add('js'); } catch (e) { } var _gaq = _gaq || []; _gaq.push(['_setAccount', 'G-8VDV14Y67G']); _gaq.push(['_trackPageview']); (function() { var ga = document.createElement('script'); ga.type = 'text/javascript'; ga.async = true; ga.src = ('https:' == document.location.protocol ? 'https://ssl' : 'http://www') + '.google-analytics.com/ga.js'; var s = document.getElementsByTagName('script')[0]; s.parentNode.insertBefore(ga, s); })(); Skip to main content Preprints Collections Wiley Open Research IET Open Research Ecological Society of Japan All Collections About About Authorea FAQs Contact Us Quick Search anywhere Search for preprint articles, keywords, etc. Search Search ADVANCED SEARCH SCROLL This is a preprint and has not been peer reviewed. Data may be preliminary. 20 August 2025 V1 Latest version Share on Beyond the forest canopy: contrasting strategies of frugivory and seed dispersal across tropical forest-savanna-grassland gradients Authors : Pedro Anselmo , Maria Regiolli Godoi 0009-0001-1226-288X , Davi Oliveira , Fernando Santos , Victor Bonifácio , Theo Karam , Marco Pizo , Alexander Christianini , Fernando Silveira 0000-0001-9700-7521 [email protected] , and Lisieux Fuzessy 0000-0001-9599-9782 Authors Info & Affiliations https://doi.org/10.22541/au.175567327.79992548/v1 646 views 292 downloads Contents Abstract Information & Authors Metrics & Citations View Options References Figures Tables Media Share Abstract Frugivory and seed dispersal play critical roles in plant reproduction, population dynamics, ecosystem functioning, while contributing to ecological restoration and climate change mitigation. However, current research largely focused on tropical forests, leaving significant gaps in our understanding of these processes in open biomes such as tropical savannas and grasslands. Using a database of seed dispersal syndromes and seed dispersal distances across 103 Neotropical sites, 51 fruit-frugivore interaction networks, and fruit traits for 1,068 plant species and 247 frugivores, we explored: 1) variation in the proportion of vertebrate-dispersed seed syndromes, 2) primary seed dispersal distances; 3) fruit and seed sizes; nestedness, modularity and specialization in fruit-frugivore networks; and 5) frugivory degree in birds across forest-savanna-grassland gradients. We showed consistent cross-biome variation in most studied aspects of frugivory and seed dispersal, with tropical forests characterized by the dominance of zoochory, longer primary dispersal distances, and interaction networks involving specialized and large frugivores. In turn, Neotropical savannas and grasslands are characterized by predominantly abiotic seed dispersal (which was linked to growth-forms), shorter dispersal distances (phylomatry) and interaction networks composed by plants producing smaller diaspores. We argue that application of forest-derived paradigms to savannas and grasslands can be problematic and that rethinking and tailoring conceptual frameworks for seed dispersal in open biomes can enhance our broad understanding of vital processes across tropical biomes. Assessing how dispersal processes vary across biomes will be essential for predicting how genotypes, populations and communities respond to changing climates and defaunation, and to what extent restoration of fruit-frugivores interactions can contribute to biodiversity and ecosystem resilience. Introduction Frugivory and seed dispersal is a key multi-step ecological process that plays critical roles in plant reproduction, population dynamics, and ecosystem functioning. By enabling propagules to escape sibling competition and natural enemies (herbivores and pathogens) near parent plants, facilitating directed dispersal, colonization of new areas, and promoting the maintenance of genetic diversity, seed dispersal plays a central role in shaping vegetation structure and resilience (Levin et al. 2003, Howe & Miriti 2004, Beckman & Sullivan 2023). In recent years, these processes have gained increasing attention in the context of ecosystem management and restoration, particularly under the pressures posed by the Anthropocene. For example, evidence of a growing seed dispersal crisis in European forests (Mendes et al. 2024) and the role of fruit-frugivore networks in accelerating forest regeneration (Genes & Dirzo 2022, Landim et al. 2024), highlight the urgent need to understand, preserve and restore seed dispersal interactions. By fostering forest recovery, effective seed dispersal may contribute to carbon sequestration and climate mitigation globally (Bello et al. 2024). Despite recent advances, most research on frugivory and seed dispersal has focused disproportionately on tropical forests, leaving significant gaps in our understanding of these processes in open biomes such as tropical savannas and grasslands (Liu et al. 2022). This forest-centric bias limits our ability to generalize ecological theories across biomes and may hinder the development of effective conservation and restoration strategies for ecosystems that differ markedly in structure, climate, and disturbance regimes. For example, savannas and grasslands, which together cover roughly 40% of Earth’s terrestrial surface, operate under fundamentally different ecological constraints than forests. These open biomes are shaped by dynamic interactions among edaphic conditions, herbivory, and seasonal fires (Scholes & Archer 1997, Veldman et al. 2015, Dinerstein et al. 2017). While fire is frequently detrimental to tropical forest structure and regeneration (Brando et al. 2012), it is a natural and often essential driver of biodiversity and resilience in open biomes (Buisson et al. 2019). These differences raise important questions as to what extent do forest-derived paradigms apply to savannas and grasslands, and whether different ecological frameworks are required to understand the roles and outcomes of seed dispersal across biomes. Contrasting ecological, structural, and functional aspects between forests and open biomes provide several independent lines of evidence suggesting that knowledge on frugivory and seed dispersal developed in tropical forests may have a limited impact on our understanding of seed dispersal in tropical savannas and grasslands. First, 70-90% of woody tropical forest species depend on frugivores for seed dispersal, but reliance on frugivores decreases and abiotic dispersal increases with increasing biome canopy openness (Juliott et al. 2001, Jordano 2014). Second, tropical forests are characterized by dense, closed-canopy vegetation producing shaded understories, and relatively stable microclimates, which largely influence plant regeneration ecology and frugivore behavior (Raoelinjanakolona et al. 2023). In contrast, open ecosystems are characterized by greater light availability, shade-intolerant species, seasonal drought, and a natural disturbance regime including herbivory and fires (Bond & Midgley 2001, Buisson et al . 2019), all of which modulate seed dispersal dynamics (Parr et al. 2007, Darosci et al. 2017, Maruyama et al . 2019, Keith et al. 2020). For example, fire reduces seed removal by ants in tropical forests (Paolucci et al. 2016) while it increases seed removal and dispersal distance by ants in savannas (Parr et al. 2007). Third, whereas forest regeneration relies primarily on seedling recruitment via the regeneration niche (Grubb 1977, but see Rodrigues et al. 2004), many plants, especially herbs and shrubs, from savannas and grasslands predominantly regenerate at short distances via resprouting from belowground organs (Buisson et al. 2019, Zupo et al. 2020, Pilon et al. 2021), constituting the so-called persistence niche (Bond and Midgley 2001). Fourth, despite similar biodiversity levels, the taxonomic, phylogenetic, and functional composition markedly differs in forests and open biomes (Purificação et al. 2014, Borges-Matos et al. 2016, Kuhlmann and Ribeiro 2016, Murphy et al. 2016, Sobral and Cianciaruso 2016). Tropical forest frugivore assemblages are typically characterized by a broader functional and taxonomic diversity of large, primarily fruit-eating vertebrates such as toucans, cotingas, manakins, monkeys and bats (Galetti & Pizo 1996, Jordano 2014), while frugivore communities in open biomes often include generalised frugivores, which can exert differential selective pressures on seed traits compared to specialized frugivores (Maruyama et al. 2019, Kuhlmann and Ribeiro 2016). Finally, the ecological consequences of seed dispersal may differ across biomes. In forests, seed dispersal enhances seedling establishment by reducing density-dependent mortality near parental plants, the Janzen-Connell effect (Comita et al. 2014). However, both density- and distance-dependent mortality show large context-dependent variation, suggesting that the Janzen-Connell model may not be as pervasive in open biomes because density- and distance-dependent mortality in trees are not common in shrubs and herbs (Song et al. 2021). Considering the costs and trade-offs associated with dispersal (Bonte et al. 2012), both theoretical and empirical evidence predict divergences in the causes and consequences of seed dispersal between forests and open biomes. As a consequence of such cross-biome differences, fruit and frugivore traits are expected to modulate the architecture of fruit-frugivore networks by modifying the potential for trait matching, a key mechanism driving interaction probability and network structure (Moran-López et al. 2025). For example, fruit and seed traits may reflect distinct selective pressures imposed by frugivores along forest-to-open biome gradients (Ordano et al. 2017, Valenta & Nevo 2020, Fuzessy et al. 2022). In tropical forests, the presence of large-bodied frugivores and less disturbed, shaded environments often favors larger fruits that offer greater nutritional rewards and contain larger seeds (Moles et al. 2007). In contrast, savannas and grasslands are shaped by strong environmental filters such as seasonal drought and fires, edaphic factors, and herbivory, alongside a reduced or absent assemblage of specialized frugivores. Altogether, these conditions tend to select for smaller, often dry diaspores and lighter seeds adapted to abiotic dispersal or dispersal by generalist vertebrates (Bello Carvalho et al. 2023). Therefore, cross-biome differences in fruit and seed size may reflect divergent adaptive syndromes shaped by biome-specific dispersal vectors and environmental constraints. This pattern may result in high trait diversity in both plants and frugivores promoting more specialized interactions and network modularity, supported by a greater availability of specialized frugivores in forests (Fuzessy et al. 2021). However, as trait spaces become more constrained resulting from fruit size and frugivore diversity toward grasslands, generalized and less specialized interaction networks are expected. A better understanding of how fruit-frugivore interactions affect seed fate and plant establishment across biomes is essential for predicting vegetation dynamics and ecosystem responses to environmental change. Yet, the degree to which current forest-derived paradigms apply to open biomes is beginning to emerge (Bond 2019). Here, we examined how frugivory and seed dispersal ecology changes across tropical forest-savanna-grassland gradients. We reviewed the literature on key dimensions of frugivory and seed dispersal using the Neotropics as an example, where most research on these topics is available (Dugger et al. 2019). Through a systematic review and comparative approach, we examined the extent to which current seed dispersal frameworks apply beyond tropical forests. We estimated cross-biome variation in seed dispersal syndromes, fruit and seed trait spaces, maximum seed dispersal distance, changes in the architecture of fruit-frugivore interaction networks, and the proportion of specialized frugivores across Neotropical forest-savanna-grassland gradients. Specifically, we tested the following hypotheses: 1) The proportion of vertebrate-dispersed seed syndromes decreases along the gradient from forest to savanna to grassland, indicating a shift toward abiotic dispersal mechanisms in more open habitats; 2) Fruit and seed sizes decreases along the gradient from forest to savanna to grasslands; 3) Primary seed dispersal distances decrease along the gradient from forest to savanna to grasslands; 4) Fruit-frugivore interaction networks become more nested, less modular and less specialized from forest to grassland; 5) The frugivory degree decreases from forest to savanna to grassland, tracking the decrease in fleshy-fruited plant species and structural habitat complexity. Material and Methods Seed dispersal syndromes across the forest-to-open biome gradient We conducted a systematic review using the Web of Science (1945-2024) platform using the following keywords: ‘dispersal syndrome*, tropical forest’, ‘dispersal syndrome*, tropical savanna’, ‘dispersal syndrome*, cerrado’, ‘dispersal syndrome*, tropical grassland, ‘dispersal syndrome*, shrubland, ‘dispersal syndrome*, open ecosystem. Papers conducted in the Neotropics were selected based on the following criteria: 1) provide sufficient information on the study area to assign the data to one of the three vegetation types (forest, savanna, grassland); and 2) report the percentage of each syndrome at the plant community-level or provide a list of plant species with the associated dispersal syndrome, allowing us to calculate the proportion for each study. Areas of monoculture and crop plantations were excluded, as well as dry and temperate forests, and restinga ecosystems (Supporting Information). When papers failed to provide information on vegetation type, we used the dominant growth-form to classify vegetation type as follows: trees for forests, shrubs for savannas and herbs for grasslands. We excluded observations without species-level identification. We corrected and updated plant taxonomy using the lcvplant package (Freiberg et al. 2019). We supplemented the database with the growth-form of each species with data extracted from the plant growth form dataset for the New World (Engemann et al. 2016). Based on the original papers, we broadly classified dispersal syndrome into zoochory, autochory, or anemochory (following van der Pijl 1982). Data for other syndromes were not considered here. To test for differences in the proportion of dispersal syndromes among vegetation types, we used a Generalized Linear Model (GLM) with quasi-binomial distribution to account for overdispersion. In the model, each replicate corresponded to a sampling unit (e.g. site) for which dispersal syndrome proportions were available. Therefore, a single study potentially provides multiple replicates in the database. The association between the growth-form (epiphyte, herb, liana, shrub and tree) and dispersal syndrome was assessed using a Chi-square test. Due to low expected frequencies, p-values were calculated using a simulation approach of 2500 replicates, using the Chisq.test function in R. Residuals were calculated to evaluate which specific combinations of growth-forms and dispersal syndromes contributed most to the observed association. Absolute residual values greater than two indicate significant deviations from the expected frequencies (Hartig 2022). Fruit and seed trait spaces across the forest-to-open biome gradient To evaluate differences in fruit and seed traits among vegetation types, we used the Neofrugivory dataset—a comprehensive database comprising 419 fruit-frugivore interaction studies and trait records encompassing 2,375 plant species and 758 vertebrate species from the Neotropics (Fuzessy & Pizo, 2025). We retrieved the coordinates from each site provided in the original papers and converted them to decimal degrees in SIRGAS 2000 datum to classify vegetation type into the Ecoregions (ecoregions.appspot.com; Dinerstein et al. 2017). All sites were then clustered into forest, savanna or grassland. Inconsistent coordinates (wrong coordinates, centroids, capitals, outliers and coordinates at the sea), were removed using the CoordinateCleaner package (Zizka et al. 2019). We retrieved and log-transformed data from fruit length, fruit width, seed length, seed width, and seed diameter and compared values among vegetation types using GLMs followed by the Tukey test. We also ran a principal coordinate analysis (PCoA) to explore the dissimilarities among fruit and seed trait spaces among biomes. We also broke down the analyses for the 10 most common families in the database to account for phylogenetic relatedness. Primary seed dispersal distance across the forest-to-open biome gradient To estimate the maximum seed dispersal distances in each vegetation type, we used a predictive model developed by Tamme et al. (2014). Data were retrieved from species included in our database of seed dispersal syndromes as described above. Tamme et al. (2024) provide multiple models with predictive power depending on the availability of plant functional traits. We modelled maximum primary seed dispersal distances based on growth-form, dispersal syndrome, and seed mass. Using this model, we were able to predict 54% of maximum primary seed dispersal distance. Species taxonomy (Order and Family) were considered as a random variable in the model. Data on growth-form and dispersal syndrome were obtained as described above, while dry seed mass was sourced from TRY (Kattge et al. 2020; Supporting Information). Due to model limitations, we excluded lianas and epiphytes, thereby restricting growth-form to trees, shrubs and herbs. Dispersal syndrome previously classified as zoochory, autochory and anemochory (following van der Pijl 1982) were included in the model as ”animal”, ”wind.none” and ”wind.special”, respectively. The modifications were made to fit the model categories described as: animal, seeds dispersed by vertebrates; wind.none, seeds usually dispersed by wind but with no adaptation for this dispersal vector; wind.special, seeds with adaptations for wind dispersion, such as wings and plumes (Tamme et al. 2014). Ant-mediated and ballistic categories were not included in the model. In some cases, we had multiple entries with different traits and vegetation category combinations. For instance, Amburana cearensis was found to have two dispersal syndromes (wind.none and wind.special), and occurred in two vegetation types (savanna and forest), resulting in three distinct combinations: wind.none and forest, wind.special and forest, and wind.special and savanna. These combinations were treated as independent entries in the model. Duplicate entries with identical information about growth-form, dispersal syndrome, seed mass and vegetation occurrence were removed from the model using the unique function from R software (R Core Team, 2025). To test whether the maximum primary seed dispersal distance varies with vegetation type, we ran a GLM with a Gaussian distribution. Residual homogeneity and distribution were assessed with the DHARMa R package (Hartig 2022). Differences between vegetation types were determined using the Tukey test, in the emmeans R package (Lenth 2024). The architecture of fruit-frugivore interaction networks across the forest-to-open biome gradient To explore changes in the architecture of fruit-frugivore interaction networks across the vegetation gradient, we searched for openly-available data published in papers indexed in the Interaction Web DataBase (http://www.ecologia.ib.usp.br/iwdb/) and in the Web of Life (Ecological Networks Database, https://www.web-of-life.es/), in May of 2024. We excluded networks with only binary interactions and kept weighted networks to extract weighted-based metrics. To compare network metrics among vegetation types, we first checked if the network sizes were comparable using linear models to check for any statistical differences between the size of each matrix partner. When not available, we calculated sampling completeness for each network as an index of sampling effort, by dividing the observed richness of pairwise plant-disperser interactions using an estimated richness of links calculated with Chao 1 estimator (Chao 1984), and the frequency of each interaction as equivalent to abundance (Vizentin-Bugoni et al. 2016). To explore the influence of network size and vegetation type on network structural metrics we fitted linear models including interaction terms between the predictors. We did this for each metric using the lm function in R software (R Core Team 2025). The statistical significance of model terms was assessed through Type II Analysis of Variance using the Anova function from the car package (Fox & Weisberg 2019). This approach provides a robust evaluation of main effects and interactions, particularly appropriate when predictors are correlated. Additionally, we checked model assumptions — residual normality and homoscedasticity — through graphical inspection of residuals and, when necessary, through appropriate statistical tests. Normality of residuals was assessed using Q-Q plots and the Shapiro-Wilk test (shapiro.test(), while homoscedasticity was evaluated using residual vs. fitted plots and formally tested with the Breusch-Pagan test (bptest() from the Zeileis & Hothorn 2002). All visual inspections were additionally supported by diagnostic plots using the autoplot() function from the ggfortify package (Tang et al. 2016). All analyses were conducted in the R programming language (version 4.3.1), with additional support from the ggplot2 package for data visualization (Wickham 2016) and dplyr for data manipulation (Wickham et al. 2023). Because we had few networks for grasslands, we merged savannas and grasslands into open biomes and compared network metrics against forests. When metrics were not provided in the original article, we extracted data to calculate network metrics — modularity (Qw), weighted nestedness (wNODF), and specialization (H2’). Qw expresses the extent to which networks are organized into modules of preferentially interacting species. Qw was estimated using the DIRTLPAwb+ optimization algorithm (Becket 2016) that rearranges the way communities can be partitioned within the observed interaction matrix, aiming to identify the conformation of species groups (i.e., modules) that maximizes interactions within the modules in relation to interactions between modules, leading to optimal Qw values. Since our goal was to compare modularity across vegetation types, we did not compare Qw values with null models. wNODF describes the presence of a core of generalist species interacting among them and a group of specialists, generating ordered subsets of interactions (Almeida-Neto & Ulrich 2011). wNODF identifies whether sequential columns or rows (i.e., species within the matrix) are sorted by decreasing marginal totals, with more weight given to frequent interactions. H2’ quantifies the partitioning of interactions among species relative to an expectation derived from their availability in the community [i.e., the selectiveness of interactions (Blüthgen et al. 2006)]. H2’ is calculated by measuring the divergence between the observed interaction frequencies and random expectation of interaction when assuming that species interact with partners following their availability (where availability is estimated as species marginal totals), then normalized to a 0 to 1 scale, showing how selectively species interact. While higher values of nestedness indicate the prevalence of generalist core species performing most interactions, higher values of modularity and specialization indicate that interactions are partitioned among specific partners (Maruyama et al. 2024). Frugivory degree across the forest-to-open biome gradient To explore variation in the degree of frugivory in frugivores across the grassland–savanna–forest gradient, we selected the percentage of fruit consumption among the multiple definitions (Carlo et al. 2025) due to data availability. We focused on birds, the most commonly primary vertebrate seed dispersers globally for which extensive trait data are available (Şekercioğlu 2006, Tobias et al. 2022). We compiled data on frugivorous bird species from 33 studies describing the structure of fruit–frugivore interaction networks (see above). We excluded synonyms, species identified only at the genus level, and species lacking trait data. In studies recording species in more than one vegetation type (e.g. forest and savanna), we duplicated the record (one for each vegetation). For each bird species, we extracted the percentage of fruit consumption from the EltonTraits (Wilman et al. 2014). In addition to diet composition, we also recorded morphological traits—body mass, beak length, and beak width—from the AVONET (Tobias et al. 2022). These traits are functionally relevant to frugivory: body size and beak morphology constrain the types and sizes of fruits a bird can consume and disperse, influencing its role in fruit–frugivore networks (Dehling et al. 2016, Bender et al. 2018). Including these traits allowed us to assess whether changes in frugivore specialization across biomes are associated with morphological shifts in bird assemblages, potentially driven by defaunation, habitat structure, or resource availability. We ran a Kruskal-Wallis model in R to compare frugivory percentages, body mass, beak length and beak width values among vegetation types (Conover 1999). The vegetation type was treated as the predictor variable with fixed effects and the response variable was the percentage of frugivory in each vegetation type. A Principal Component Analysis (PCA) was performed to reduce the dimensionality of the bird functional traits and identify the main variations among vegetation types (Jolliffe 2002). The analysis included the following variables: percentage of frugivory, beak length, beak width, and body mass. The data were standardized to a mean of zero and a standard deviation of one to ensure that all variables had the same influence on the analysis, regardless of their units of measurement. The PCA was conducted using the PCA function from the FactoMineR package in R (Lê et al. 2008), and the results were visualized using the factoextra package (Kassambara & Mundt 2020). Individuals were grouped by vegetation type and 95% confidence ellipses were drawn around the groups to visualize the variability between environments. We applied PERMANOVA to test for significant differences in multivariate trait composition among groups identified in the PCA (Anderson, 2001). This approach allows assessing whether the variation summarized by the principal components differs significantly across predefined groups, based on permutation tests of distance matrices. Finally, using the bird species from our database, we created a Venn diagram to explore the number of species shared among all vegetation types (Chen & Boutros 2011). Results Seed dispersal syndromes across the forest-to-open biome gradient Our final database comprised 58 papers with data from 103 sites (45 forests, 51 savannas, and seven grasslands), at least 3,200 species in 186 families. A significant difference in the proportion of seed dispersal syndromes was observed across the three vegetation types for zoochory (F= 21.71; df= 98; p <0.0001), anemochory (F= 19.67; df= 91; p <0.001), and autochory (F= 5.49; df= 85; p < 0.005). The proportion of animal-dispersed fruits decreased progressively along the vegetation gradient, with forests showing the highest proportion of zoochoric species compared to savannas and grasslands (Fig. 1a). The analysis of growth-forms revealed a significant relationship between growth-form and dispersal syndrome (ꭓ² = 623.87, p< 0.0003). Woody species (trees and shrubs) were predominantly dispersed by animals, with 70.1% of trees and 59.9% of shrubs relying on biotic agents for seed dispersal. Abiotic dispersal was more prominent with decreasing woodiness. Herbaceous species showed a higher proportion of autochoric (51.8%) and anemochoric (32.7%) dispersal. Lianas showed a greater reliance on wind dispersal (51.4%), compared to zoochoric and autochoric dispersal (Fig. 1b). not-yet-known not-yet-known not-yet-known unknown Fruit and seed trait spaces A total of 5,235 entries, representing 1,068 plant species, were analyzed. Of these, 4,041 entries (869 species) corresponded to forest biomes and 1,194 entries (199 species) to open biomes. All values of fruit and seed dimensions were higher in forest species compared to species from open biomes (Fig. 2 A-E). As a result, diaspores from forest species were functionally different from those in open biomes (Fig. 2F). Pair-wise comparisons of seed and fruit traits including the ten most common botanical families revealed no differences between forests and open biomes, indicating that phylogenetic relatedness had little to no influence on the overall pattern (Supporting Information). The family Urticaceae was excluded from the analysis due to inconsistencies in the compiled data between open and forested biomes. Primary seed dispersal distances Our model included 622 species (774 entries), including 519 forest species (568 entries), 92 savanna species (102 entries) and 101 grassland species (104 entries). Average maximum seed dispersal distance in forests was 455 m (± 301.6; SD), 269.9 m (± 354.4) in savannas and 88.8 m (± 211.6) in grasslands. Maximum seed dispersal distances differed among vegetation types (χ² = 148.33; df = 2; p < 0.001, Fig. 3), with significantly highest seed dispersal distances in forests, intermediate in savannas (SE = 32.1; df = 771; p < 0.001), and lowest in grasslands (SE = 41.6; df = 771; p < 0.001). The architecture of fruit-frugivore networks across the forest-to-open biome gradient We gathered information from 51 fruit-frugivore networks sampled in Brazil (22), Argentina (14), Ecuador (6), Bolivia (4), Colombia (3) and Peru (2). Forty-four networks were from forests and only seven networks were from open ecosystems (five for savannas and two for grasslands). Network size did not differ significantly between the habitat types analyzed (ꭓ²= 0.01, p>0.05; Supporting Information), indicating that network structural metrics are not attributable to systematic variations in species richness or interaction numbers across networks. Similarly, sampling completeness was comparable between habitats (ꭓ²= 2.76, p>0.05; Supporting Information), suggesting that sampling effort did not introduce significant biases in further comparisons. Neither modularity (Qw; p = 0.057) nor weighted nestedness (wNODF; p = 0.239) showed significant variation among vegetation types (Figure 4). Finally, specialization (H 2 ) significantly differed among vegetation types (F = 5.61; p = 0.022), with higher specialization values in open biomes (Figure 4). Frugivory degree across the forest-to-open biome gradient From the whole database of fruit-frugivore networks, 33 papers provided a full list of interacting species, yielding data for 247 bird species. Out of those, 11 species were missing in Elton Traits 1.0 database and were excluded from the analysis. From the total of 236 species, 152 species occur only in forests, 13 only in savannas, and only three species were exclusive to grasslands. Sixty species are shared between forests and savannas, and two species occur both in grassland and savanna. Five species occur in all tree vegetation types (Supporting Information). We found no significant differences in the proportion of frugivory degree across the vegetation gradient (x² = 1.7616, df = 2, p = 0.4144; Figure 5a). The PCA revealed that bird functional traits did not show clear patterns of variation across different vegetation types, confirmed by PERMANOVA (p = 0.478). PC1 was primarily associated with beak width, beak length and body mass, representing a gradient of body size and structure, indicating that these traits are the main drivers of variation among the birds. PC2 was mainly influenced by percentage of fruit consumption in diet, suggesting differences in diet composition across environments (Figure 5b). Birds from savannas were well distributed among the four quadrants, indicating high variation in beak dimensions and percentage of frugivory. Forest birds were also well distributed among the four quadrants, but with a lower distribution area, indicating lower variations in beak dimensions and percentage of frugivory. In contrast, grassland birds were clustered in both quadrants to the left, suggesting that these birds showed lower beak dimensions. The 95% confidence ellipses drawn around each environment group in the PCA plot indicated that there was a notable overlap between forest and savanna birds, while birds from grassland formed a more distinct cluster. This suggests that birds from grassland have more distinct functional traits compared to birds from the other two vegetation types. Discussion By integrating data on dispersal syndromes and distances across 103 sites in Neotropical forests, savannas, and grasslands, 51 fruit-frugivore interaction networks, and fruit traits for 1,068 plant species and 247 frugivores, we showed consistent cross-biome variation in dispersal syndromes, dispersal distances, fruit and dispersal trait spaces, and the architecture of fruit-frugivore interaction networks. Across the forest–savanna–grassland gradient, communities showed marked shifts in seed dispersal strategies. While tropical forests are characterized by the dominance of zoochory, longer primary seed dispersal distances, and interaction networks involving specialized frugivores and large diaspores, these traits decreased with increasing biome canopy openness. In turn, Neotropical savannas and grasslands are characterized by a continuous matrix of herbaceous cover, abiotic seed dispersal (which was linked to growth-forms), and interaction networks composed by plants producing smaller diaspores. These patterns suggest that seed dispersal ecology (Howe & Miriti 2004, Beckman & Sullivan 2023) is not uniform across biomes, and that plant reproduction is less reliant on dispersal-related processes in savannas and grasslands. These results call for rethinking and tailoring conceptual frameworks for seed dispersal in open biomes, which differ ecologically, functionally and edaphically from forests (Ratnam et al. 2011, Carvalheiro et al. 2021). Our findings indicate that forest-derived ecological models may not be easily generalizable to open biomes. For instance, the Janzen–Connell hypothesis (Janzen 1970; Connell 1971) highlights the role of seed dispersal in mitigating density-dependent mortality near parent plants in forests. However, our results suggest that this mechanism may be less influential in open biomes where seeds are dispersed to shorter distances. In these biomes, the costs of long-distance dispersal may outweigh the benefits of escaping sibling competition and/or natural enemies (Bonte et al. 2012). As a result, natural selection may favor dispersal strategies that favor establishment close to the parent plant (phylomatry) where recruitment can be limited more by abiotic filters than by biotic interactions (Cheplick 2022, Hopper et al. 2021, Teste & Laliberté 2021). The observed shift from zoochory to abiotic dispersal across the forest-to-open biome gradient likely reduces both the frequency and ecological importance of distance- and density-dependent effects. Nevertheless, Janzen–Connell effects are not exclusive to animal-dispersed species: wind-dispersed trees and temperate species can also exhibit such patterns (Augspurger & Franson 1993, Steinitz et al. 2011, Nathan et al. 2002). Still, the evidence suggests that these effects are generally weaker or more context-dependent in herbaceous and shrubby vegetation typical of open biomes (Pausas et al. 2018, Buisson et al. 2019, Song et al. 2021, Pilon et al. 2021). Our results also offer new perspectives to our understanding of dispersal–colonization trade-offs (Levins & Culver 1971, Miller et al. 2024). In closed forests, this model has been widely adopted to help explain successional trajectories, where early colonizers evolved high dispersal ability, while later colonizers invest on competitive traits. However, in disturbance-adapted open biomes, this dynamics may differ. In open biomes, traits that confer persistence, including resprouting, fire-stimulated reproduction, and long-lived seed banks may be more critical for regeneration than dispersal (Hoffmann 1999, Bond & Midgley 2001, Carbone et al. 2025), so much that the persistence niche may outweigh the colonization niche. As a consequence, natural selection may favor the evolution of regeneration near parental plants rather than colonization of new areas, challenging classical assumptions based on seed arrival and establishment. As expected, diaspore dimensions decreased towards grasslands, suggesting that trait variation across biomes supports functional shifts. Regardless of phylogenetic relatedness, forest species tend to produce larger fleshy fruits adapted to attract large-bodied frugivores (Moran et al. 2025), which ultimately increases the chances of long-distance dispersal (Fuzessy et al. 2022). In contrast, small diaspores, typically or herbaceous and overlooked herbs, dominate open biomes. However, this apparent pattern may reflect not only environmental filtering (drought, fire, herbivory, soil fertility), but also methodological limitations and defaunation. Large-seeded genera such as Caryocar , Hymenaea , Diospyros , and several palms are present in savannas but may be underrepresented in interaction networks due to the extirpation of large frugivores (Vidal et al. 2013), and sampling biases—such as the limited detectability of mammals and bats in focal observations, particularly in open ecosystems. Key dispersers like rheas, which consume large fruits, are also frequently overlooked (Jacques et al. 2025). Thus, current network patterns may underrepresent interactions involving large-seeded species, and may mask the potential for trait matching and longer dispersal events in open biomes, a topic that should be addressed by future studies. Interestingly, interaction networks in open biomes exhibited higher specialization despite lower mutualistic diversity. This pattern may be an artefact, also reflecting defaunation-driven partner loss (Guimarães et al. 2008), or sampling limitations rather than true ecological specialization. Forest networks, in contrast, were more generalized, particularly where large-bodied frugivores persist (Fuzessy et al. 2021). The convergence of frugivore trait spaces across biomes may be a legacy of functional homogenization following the non-random loss of large, functionally distinctive dispersers (Vidal et al. 2013). This homogenization may obscure historically distinct interaction structures and processes. As a result, their disappearance can lead to a convergence toward smaller, more generalist assemblages across biomes. Defaunation may erode biome-specific trait distributions and interaction structures, thereby masking historically distinct ecological processes and patterns. Despite consistent cross-biome variation in dispersal syndromes, distances and diaspore sizes, we found an unexpected functional overlap in frugivore functional traits across the gradient. However, such patterns may also be the product of widespread defaunation which may obscure higher preference for fruits in forests, where vertebrates more frequently act as primary frugivores. In contrast, savannas and grasslands rely more on generalists and non-classical dispersers such as rodents, ungulates, ants, insectivores and large flightless birds (Renison et al. 2010, Goebel et al. 2023, Fuzessy et al. 2024, Jacques et al. 2025). These species may sustain dispersal services through alternative pathways, including scatter-hoarding by rodents, which promotes seed burial and delayed germination; endozoochory by generalist herbivores that incidentally consume and disperse seeds, and secondary dispersal by ants, especially relevant for small diaspores in open habitats (Janzen 1984, Camargo et al. 2019, Azevedo et al. 2024). In addition, large flightless birds such as rheas ( Rhea americana ) can act as long-distance dispersers but are often absent from defaunated landscapes (Renison et al. 2010, Jacques et al. 2025). Fire-induced seed release and wind-assisted movement may also contribute to dispersal in open biomes, particularly among graminoids and forbs. Although these mechanisms differ in efficiency and selectivity compared to vertebrate frugivory in forests, they may maintain essential dispersal functions under disturbance or defaunation. In degraded Atlantic Forest landscapes, habitat heterogeneity (e.g., mosaics of agriculture and pasture) favors functionally distinct bird assemblages dominated by generalists, while forest specialists decline (Fuzessy et al. 2024). Although the present study focuses on natural, rather than anthropogenic gradients, it suggests that structural heterogeneity in open biomes (e.g., patchy vegetation, fire-disturbed areas) may similarly filter for generalist dispersers. Crucially, our results do not imply that seed dispersal is unimportant in savannas and grasslands. On the contrary, studies in the Cerrado show that dispersal shapes population genetic structure (Collevatti et al. 2001, Melo Jr et al. 2012), mediates seed and seedling limitation (Salazar et al. 2012a, 2012b, Mariano et al. 2019), and predation-mediated recruitment dynamics (Ferreira et al. 2011). Our findings suggest that the mechanisms and selective pressures driving seed dispersal in open biomes appear to differ markedly from those in forests. In disturbance-driven environments, the persistence niche – underpinned by traits that enable individuals to regenerate in situ – becomes more critical than the regeneration niche via seed dispersal. This is supported by a recent meta-analysis showing that fire promotes reproductive success in wind-dispersed, perennial forbs and graminoids, while having non-significant effect on trees and vertebrate-dispersed species (Carbone et al. 2025). Together, these findings underscores that seed dispersal in open biomes operates under distinct ecological pressures, and that conservation and restoration strategies must be informed by a more nuanced understanding of biome-specific regeneration dynamics. For example, in Neotropical vegetation mosaics, reproductive phenology peaks at different times of the year across distinct vegetation types, creating habitat complementarity providing year-round resources for dispersers transitioning across the mosaic (Cardoso et al. 2025). Caveats While our systematic review provides broad and novel insights into seed dispersal across Neotropical biomes, several important limitations should be considered when interpreting the results. First, our analysis is largely focused in the Neotropical savannas and grasslands, and may not fully capture dispersal patterns in Palaeotropical open biomes, where evolutionary histories and ecological processes differ substantially (Pires et al. 2014, Bunney et al. 2017). Second, our classification of dispersal syndromes was based on morphological traits, which may not always accurately reflect actual dispersal vectors (Green et al. 2022, González-Varo et al. 2024). For instance, the dispersal of autochorous fruits by generalist herbivores such as mammalian browsers and grazers (Janzen 1984, Azevedo et al. 2024, Hoffmann et al. 2025) may have gone undetected, particularly in defaunated landscapes such as in our case. Third, our estimates of dispersal distances are limited to primary dispersal and do not incorporate secondary dispersal, which moves seeds farther from maternal plants (van der Wall & Longland 2004). Fourth, the use of coarse dietary categories in EltonTraits—especially the lack of clear distinctions between frugivory and granivory—and the absence of nutritional data in NeoFrugivory may have obscured meaningful cross-biome variation in frugivore–fruit interactions. While these limitations are important to acknowledge, our comparative approach remains robust at this ecological scale. Future studies should aim to fill these gaps through targeted fieldwork in underrepresented biomes and by applying standardized methodologies to measure dispersal mechanisms and interaction outcomes more precisely. Conclusions Our understanding of seed dispersal ecology has been overwhelmingly shaped by research conducted in forest ecosystems, leading to frameworks that do not fully capture the complexities of tropical savannas and grasslands. These open biomes are megadiverse and threatened, cover harbor great biodiversity. Despite that, open biomes are underrepresented in the frugivory and seed dispersal literature (Liu et al. 2022), undermining our capacity to understand, protect and restore their diversity and functioning. Our findings highlight the need to expand theoretical frameworks to better accommodate the diversity of dispersal strategies and interaction patterns in Neotropical savannas and grasslands and, especially their consequences in the Anthropocene. As global change accelerates, land use changes intensifies, and defaunation increases, understanding how dispersal processes vary across biomes is essential for predicting plant responses, protecting ecological interactions, and informing restoration programs (Fricke et al. 2025). 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F., Pausas, J. G. & Fidelis, A. 2020. Post-fire regeneration strategies in a frequently burned Cerrado community. J. Veg. Sci. 32(1): e12968. https://doi.org/10.1111/jvs.12968. Figure captions Figure 1. Proportion of zoochory, anemochory and autochory across Neotropical forest-savanna-grassland gradients: forest (n = 45), savanna (n = 51), and grassland (n=7). The bloxpots represent the distribution of each dispersal syndrome proportion within each vegetation type in a given site (a) and according to plant growth-form (b). The analysis encompasses data from 1830 species within 162 plant families: epiphytes (n = 30), herbs (n = 283), lianas (n =61), shrub (n =376), and trees (n = 1145). Figure 2. Fruit and seed traits across Neotropical forests and open biomes (savannas and grasslands). Pairwise comparisons are shown in A-E and Principal Component Analysis is shown in F. Figure 3. Estimated maximum primary seed dispersal distances across Neotropical forest, savannas and grasslands following Tamme et al. (2014). Sample sizes refer to the number of entries of each vegetation type in the model, and asterisks represent significant differences between the vegetation types . Figure 4. Boxplots comparing fruit-frugivore network metrics between closed (Neotropics forests) and open vegetation (savannas and grasslands). n.s. Indicates non-significant differences between vegetation types and asterisks represent significant values (p Figure 5. Percentage of fruit consumption in the diet of birds in Neotropical forest-savanna-grassland gradients. A - shows the percentage of frugivory in 236 species of Neotropical bird frugivores. B - Bird frugivore-related functional traits across forests, savannas and grasslands. The first two principal components (PC1 and PC2) explained 86.4% of total variance. Figure S1. Prisma flowchart following guidelines in Page et al. (2021) and O’Dea et al. (2021). Figure S2. Fruit and seed traits across Neotropical forests and open biomes (savannas and grasslands) distributed in the 10 plant families with available data. Figures S3. Boxplot showing no significant differences in network sizes (A) and the sampling completeness (B) between closed- and open-canopy vegetation types in the Neotropics. Figure S4. Venn diagram depicting the distribution of 236 bird frugivores across Neotropical forest-savanna-grassland gradients. Information & Authors Information Version history V1 Version 1 20 August 2025 Copyright This work is licensed under a Non Exclusive No Reuse License. Keywords dispersal syndrome dispersal vectors fruit size fruit-frugivore networks phylomatry seed size Authors Affiliations Pedro Anselmo Federal University of Minas Gerais View all articles by this author Maria Regiolli Godoi 0009-0001-1226-288X Universidade Federal de Minas Gerais View all articles by this author Davi Oliveira Federal University of Minas Gerais View all articles by this author Fernando Santos Federal University of Minas Gerais View all articles by this author Victor Bonifácio Federal University of Minas Gerais View all articles by this author Theo Karam Federal University of Minas Gerais View all articles by this author Marco Pizo Universidade Estadual Paulista (UNESP) View all articles by this author Alexander Christianini View all articles by this author Fernando Silveira 0000-0001-9700-7521 [email protected] Universidade Federal de Minas Gerais View all articles by this author Lisieux Fuzessy 0000-0001-9599-9782 Universidade Federal de Viçosa View all articles by this author Metrics & Citations Metrics Article Usage 646 views 292 downloads .FvxKWukQNSOunydq8rnd { width: 100px; } Citations Download citation Pedro Anselmo, Maria Regiolli Godoi, Davi Oliveira, et al. Beyond the forest canopy: contrasting strategies of frugivory and seed dispersal across tropical forest-savanna-grassland gradients. Authorea . 20 August 2025. DOI: https://doi.org/10.22541/au.175567327.79992548/v1 If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download. For more information or tips please see 'Downloading to a citation manager' in the Help menu . Format Please select one from the list RIS (ProCite, Reference Manager) EndNote BibTex Medlars RefWorks Direct import Tips for downloading citations document.getElementById('citMgrHelpLink').addEventListener('click', function() { popupHelp(this.href); return false; }); $(".js__slcInclude").on("change", function(e){ if ($(this).val() == 'refworks') $('#direct').prop("checked", false); $('#direct').prop("disabled", ($(this).val() == 'refworks')); }); Cited by Fernando A. O. Silveira, João Vitor S. Messeder, Lisieux F. Fuzessy, Fruit traits: the ugly duckling in the whole spectrum of plant form and function, New Phytologist, 250 , 4, (2001-2006), (2026). https://doi.org/10.1111/nph.71008 Crossref Loading... View Options View options PDF View PDF Figures Tables Media Share Share Share article link Copy Link Copied! Copying failed. 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