DOI: 10.5061/dryad.5dv41ns6d
title: Data from: Frugivore diversity increases evenness in the seed rain on deforested tropical landscapes

description: The diversity of tropical forests is strongly shaped by mutualistic
 interactions involving plants and frugivores that disperse their seeds.
 However, it is little known how decreases in the diversity of frugivores
 can affect seed dispersal patterns, plant community composition and
 species' coexistence in tropical forest landscapes. Here, we
 investigated the effects of bird frugivore diversity on seed dispersal of
 rare plant species and on the magnitude of equalizing effects on the seed
 rain in open areas within 12 fragmented landscapes in the Brazilian
 Atlantic Forest. We monitored the production of bird-dispersed seeds and
 bird abundance in forest fragments, and sampled the seed rain and the
 activity of birds attracted to experimental tree nuclei established in
 neighboring pastures. The activity of frugivores in tree nuclei was
 positively correlated with the diversity of birds recorded in nearby
 forest fragments, and the seed rain diversity increased with frugivore
 activity. The proportion of seeds dispersed more frequently than expected
 by chance in tree nuclei increased linearly with the species'
 richness of birds. The richness and abundance of active frugivores in
 deforested areas promoted a seed rain with evenness and diversity up to
 five times greater than the seed pool available in forest fragments due to
 the proportional increase in the dispersal of rare plant species and a
 concomitant proportional decrease in the dispersal of dominant fruiting
 plants. Furthermore, every additional bird species detected in a site was
 associated with a 10% increase in the equalizing effect on dispersed
 seeds’ relative abundance. Our results show that the aggregated behavior
 of avian frugivore communities on deforested areas results in higher
 species richness in the seed rain of plant communities and underscore the
 urgency to reduce bird species' loss and the simplification of their
 communities in tropical landscapes.
description: <i>Study sites</i> The study was
 conducted in 12 sites of the Paranapanema municipality in São Paulo,
 southeastern Brazil (23°23' S, 48°43' W, Fig. 1). The sites were
 located in private farms with cattle pastures and &gt; 30-year-old
 fragments of secondary semideciduous forests ranged from 12.2 to 98.8 ha.
 The study area is located within the second most threatened
 biogeographical zone (&lt;7% forest cover remaining) of the Atlantic
 Forest (Ribeiro et al. 2009), a global hotspot for biodiversity
 conservation and tropical rainforest restoration (Laurance 2009,
 Brancalion et al. 2019). The local climate is Köppen type Cfa, humid
 subtropical, with hot summer (Alvares et al. 2013). Average annual
 rainfall, concentrated in the wet summer season (December to March), is
 1.407,9 mm, while mean annual temperature is 18 °C (Cielo-Filho et al.
 2009). <i>Tree nuclei in
 pastures</i> In December 2016 we established at
 each site eight 4.5 x 4.5 m plots in cattle pastures to sample bird visits
 and the seed rain. Plots were established at 10 and 50 m from the nearest
 forest fragment (Fig. 1). We used plots at these distances because there
 was not much difference in the parameters of the seed rain between plots
 at 10 or 50 m from the forest fragments (see Camargo et al. 2020). At each
 distance class, we established four plots: three with a tree planted and
 one Control with no tree. Plots were fenced with barbwire to keep cattle
 off, grasses inside plots were mowed and mechanically controlled
 throughout the experiment. At the center of each plot, we planted one
 pioneer tree of reproductive age at least 1.5 m in height to form small
 tree nuclei on pastures. We planted pioneer trees with different
 functional characteristics of fruits to maximize interactions with the
 bird community: <i>Heliocarpus popayanensis</i> Kunth with
 wind-dispersed seeds, <i>Acnistus arborescens</i> Schltdl.
 with fleshy fruits composed of 48.3% of carbohydrates, 7.9% of proteins
 and 0.04% of lipids, and <i>Trema micrantha</i> (L.) Blume
 with fleshy fruits composed of 48.8% of lipid, 10.7% of proteins and 2.2%
 of carbohydrates. <i>Bird activity in tree
 nuclei</i> From October 2017 to November 2018 we
 recorded bird activity in the experimental plots of tree nuclei in the
 pastures using direct focal observations and video recording. Each plot
 was observed once a month by one observer (PHSA Camargo) using a pair of
 binoculars from a distance of 50 m for 20 min, during morning hours
 (07:30–10:30), totaling 13.3 h of focal observations per site. We
 complemented these focal observations with 22 camera-traps. Each
 camera-trap operated 24 h/day for a total of 59,152.9 h. In addition, we
 also used six GoPro Hero 3 cameras that filmed for about 2 h before
 batteries were depleted, totaling 193.5 h of filming. All the cameras were
 rotated, and the sampling efforts of focal observations and filming were
 equally distributed among the plots and sites to prevent sampling bias.
 For more details see Camargo et al. (2020).
 <i>Seed rain</i> To sample seed
 rain we used one 0.25 m² seed trap lined with a 0.2 mm nylon mesh placed
 at the center of each tree nuclei plot. We applied Formifuu® to the legs
 of the traps to prevent ant access and covered the traps with a wire
 screen (2.5 x 2.5 cm mesh) to exclude vertebrate seed predators. Seeds
 were collected monthly from the traps and counted and identified to the
 lowest taxonomic level possible in the laboratory with the aid of a
 dissecting scope, available reference books and reference seed collections
 for the local flora. We did not include in the analysis the number of
 grass seeds or those from the pioneer tree species planted in a particular
 plot (as they may have originated <i>in situ</i>).
 <i>Fruit abundance in forest fragments</i>
 To quantify the abundances of bird-dispersed fruits in forest
 fragments, we systematically established 10 5 x 5 m vegetation inventory
 plots at each forest fragment, totaling 250 m² sampled in each study site
 (Fig. 1). Overall, we marked a total of 1827 plants including trees,
 shrubs, vines, herbs, mistletoes; mean ± SD of 152.25 ± 21.09 individuals
 per site and 7.30 ± 15.96 individuals per species), of which 72.5% (n =
 1324) corresponded to 187 bird-dispersed species (38.3 ± 10.2 species per
 site). From October 2017 to November 2018, we counted monthly the number
 of ripe fruits of all bird-dispersed species monitored within forest
 plots. Whenever possible, we directly counted all fruits without
 extrapolation, but for large trees with a large fruiting crop, we counted
 fruits in 3-5 branches or portions of the canopy and extrapolated to the
 rest of the canopy area bearing fruit. For each species, we average the
 fruit per individual and calculated the fruit density per plot. Then, we
 extrapolated the average density across plots to obtain the density of
 fruits in the whole fragment (fruits/hectare). We obtained the abundance
 of seeds available in the fragment by multiplying the density of fruits by
 the average number of seeds per fruit of each species.
 <i>Bird abundance in forest
 fragments                                                                                       </i> To estimate the abundance of birds, we conducted 10-min point counts at the five vegetation sampling plots per forest fragment (Fig. 1). Bird surveys were conducted once a month between October 2017 and November 2018 from 6:00 to 7:30 when all birds visually and acoustically detected within a 50 m radius were recorded. Abundances were calculated by dividing the number of records of each species by the number of sampled point counts and averaged across months.