Land-use homogenization reduces the occurrence and diversity of frugivorous birds in a tropical biodiversity hotspot.

Understanding how human-modified landscapes maintain biodiversity and provide ecosystem services is crucial for establishing conservation practices. Given that responses to land-use are species-specific, it is crucial to understand how land-use changes may shape patterns of species diversity and persistence in human-modified landscapes. Here, we used a comprehensive data set on bird distribution from the Brazilian Atlantic Forest to understand how species richness and individual occurrences of frugivorous bird species responded to land-use spatial predictors and, subsequently, assess how ecological traits and phylogeny modulated these responses. Using Bayesian hierarchical modeling, we reveal that the richness of frugivorous birds was positively associated with the amount of native forest and negatively with both agriculture and pasture amount at the landscape scale. Conversely, the effect of these predictors on species occurrence and ecological traits was highly variable and presented a weak phylogenetic signal. Furthermore, land-use homogenization (i.e., the conversion of forest to pasture or agriculture) led to pervasive consequences for forest-dependent bird species, whereas several generalist species thrived in deforested areas, replacing those sensitive to habitat disturbances.

Tropical forest loss and geographic location drive the functional genomic diversity of an endangered palm tree.

Human activity has diminished forests in different terrestrial ecosystems. This is well illustrated in the Brazilian Atlantic Forest, which still hosts high levels of species richness and endemism, even with only 28% of its original extent remaining. The consequences of such forest loss in remaining populations can be investigated with several approaches, including the genomic perspective, which allows a broader understanding of how human disturbance influences the genetic variability in natural populations. In this context, our study investigated the genomic responses of Euterpe edulis Martius, an endangered palm tree, in forest remnants located in landscapes presenting different forest cover amount and composed by distinct bird assemblage that disperse its seeds. We sampled 22 areas of the Brazilian Atlantic Forest in four regions using SNP markers inserted into transcribed regions of the genome of E. edulis, distinguishing neutral loci from those putatively under natural selection (outlier). We demonstrate that populations show patterns of structure and genetic variability that differ between regions, as a possible reflection of deforestation and biogeographic histories. Deforested landscapes still maintain high neutral genetic diversity due to gene flow over short distances. Overall, we not only support previous evidence with microsatellite markers, but also show that deforestation can influence the genetic variability outlier, in the scenario of selective pressures imposed by these stressful environments. Based on our findings, we suggest that, to protect genetic diversity in the long term, it is necessary to reforest and enrich deforested areas, using seeds from populations in the same management target region.

Atlantic flower-invertebrate interactions: A data set of occurrence and frequency of floral visits.

Encounters between flowers and invertebrates are key events for the functioning of tropical forests. Assessing the structure of networks composed of the interactions between those partners leads to a better understanding of ecosystem functioning and the effects of environmental factors on ecological processes. Gathering such data is, however, costly and time-consuming, especially in the highly diverse tropics. We aimed to provide a comprehensive repository of available flower-invertebrate interaction information for the Atlantic Forest, a South American tropical forest domain. Data were obtained from published works and "gray literature," such as theses and dissertations, as well as self-reports by co-authors. The data set has ~18,000 interaction records forming 482 networks, each containing between one and 1061 interaction links. Each network was sampled for about 200 h or less, with few exceptions. A total of 641 plant genera within 136 different families and 39 orders were reported, with the most abundant and rich families being Asteraceae, Fabaceae, and Rubiaceae. Invertebrates interacting with these plants were all arthropods from 10 orders, 129 families, and 581 genera, comprising 2419 morphotypes (including 988 named species). Hymenoptera was the most abundant and diverse order, with at least six times more records than the second-ranked order (Lepidoptera). The complete data set shows Hymenoptera interacting with all plant orders and also shows Diptera, Lepidoptera, Coleoptera, and Hemiptera to be important nodes. Among plants, Asterales and Fabales had the highest number of interactions. The best sampled environment was forest (~8000 records), followed by pastures and crops. Savanna, grasslands, and urban environments (among others) were also reported, indicating a wide range of approaches dedicated to collecting flower-invertebrate interaction data in the Atlantic Forest domain. Nevertheless, most reported data were from forest understory or lower strata, indicating a knowledge gap about flower-invertebrate interactions at the canopy. Also, access to remote regions remains a limitation, generating sampling bias across the geographical range of the Atlantic Forest. Future studies in these continuous and hard-to-access forested areas will yield important new information regarding the interactions between flowers and invertebrates in the Atlantic Forest. There are no copyright restrictions on the data set. Please cite this data paper if the data are used in publications and teaching events.

Deterministic modelling of seed dispersal based on observed behaviours of an endemic primate in Brazil.

Plant species models are among the available tools to predict the future of ecosystems threatened by climate change, habitat loss, and degradation. However, they suffer from low to no inclusion of plant dispersal, which is necessary to predict ecosystem evolution. A variety of seed dispersal models have been conceived for anemochorous and zoochorous plant species, but the coupling between vegetation models and seed dispersal processes remains rare. The main challenge in modelling zoochoric dispersal is simulating animal movements in their complex habitat. Recent developments allow straightforward applications of hidden Markov modelling (HMM) to animal movements, which could ease generalizations when modelling zoochoric seed dispersal. We tested the use of HMM to model seed dispersal by an endangered primate in the Brazilian Atlantic forest, to demonstrate its potential simplicity to simulate seed dispersal processes. We also discuss how to adapt it to other species. We collected information on movement, fruit consumption, deposition, and habitat use of Leontopithecus chrysomelas. We analysed daily trajectories using HMM and built a deterministic Model Of Seed Transfer (MOST), which replicated, with good approximation, the primate's movement and seed deposition patterns as observed in the field. Our results suggest that the dispersal behaviour and short daily-trajectories of L. chrysomelas restrict the species' role in large-scale forest regeneration, but contribute to the prevalence of resource tree species locally, and potentially maintaining tree diversity by preventing local extinction. However, it may be possible to accurately simulate dispersal in an area, without necessarily quantifying variables that influence movement, if the movement can be broken down to step-length and turning angles, and parametrised along with the distribution of gut-transit times. For future objectives, coupling MOST with a DVM could be used to test hypotheses on tree species survival in various scenarios, simulating regeneration and growth at regional scales by including data on main dispersal agents over the area of interest, distribution of tree species, and land use data. The principal advantage of the MOST model is its functionality with data available from the literature as the variables are easy to parametrise. We suggest using the coupled model to perform experiments using only available information, but varying the numbers and species of seed dispersers, or modifying land cover or configuration to test for possible thresholds preventing the extinction of selected tree species.

The impact of anthropogenic disturbances on the genetic diversity of terrestrial species: A global meta-analysis.

Human activities are primarily responsible for habitat loss and changes in natural environments around the world. It has been suggested that populations inhabiting human-modified landscapes experience reduced gene flow, inbreeding depression, and loss of alleles due to genetic drift. However, empirical evidence shows the contrasting effects of anthropogenic disturbances on the genetic diversity of species. We performed a meta-analysis of 61 studies that compared the genetic diversity of plant and/or animal populations in disturbed and more preserved areas (316 paired comparisons) to investigate the genetic responses to different disturbance types. There is a negative effect (effect size: -0.45; 95% confidence interval: -0.61, -0.29) of disturbances on genetic diversity, in which the most detrimental effects are caused by the loss of connectivity and forest cover. The methodological approach can explain part of the heterogeneity among the genetic responses detected by primary studies: (a) studies using the number of effective alleles did not detect genetic erosion, while all other indices revealed negative responses to disturbances; and (b) only studies performed with transferred or a combination of transferred and specific microsatellites detected negative responses. The effects on animal populations are more detrimental than in plant populations. Only plant species with a shrub life form, self-incompatible reproductive systems, and biotic pollination and seed dispersal showed negative responses to disturbances. Despite heterogeneity among studies, there is an overall negative effect of disturbances on genetic diversity, which indicates that remaining populations inhabiting human-modified landscapes have reduced evolutionary potential and are prone to local extinction.

Designing optimal human-modified landscapes for forest biodiversity conservation.

Agriculture and development transform forest ecosystems to human-modified landscapes. Decades of research in ecology have generated myriad concepts for the appropriate management of these landscapes. Yet, these concepts are often contradictory and apply at different spatial scales, making the design of biodiversity-friendly landscapes challenging. Here, we combine concepts with empirical support to design optimal landscape scenarios for forest-dwelling species. The supported concepts indicate that appropriately sized landscapes should contain ≥ 40% forest cover, although higher percentages are likely needed in the tropics. Forest cover should be configured with c. 10% in a very large forest patch, and the remaining 30% in many evenly dispersed smaller patches and semi-natural treed elements (e.g. vegetation corridors). Importantly, the patches should be embedded in a high-quality matrix. The proposed landscape scenarios represent an optimal compromise between delivery of goods and services to humans and preserving most forest wildlife, and can therefore guide forest preservation and restoration strategies.

Anthropogenic Disturbances Eroding the Genetic Diversity of a Threatened Palm Tree: A Multiscale Approach.

Habitat loss and the illegal exploitation of natural resources are among the main drivers of species extinction around the world. These disturbances act at different scales, once changes in the landscape composition and configuration operate at large scales and exploitation of natural resources at local scales. Evidence suggests that both scales are capable of triggering genetic erosion in the remaining populations. However, most of the studies so far did not evaluate simultaneously the effects of these disturbances on genetic diversity and structure of plants. In this study, we used a multiple scale approach to empirically evaluate the impacts caused by local and landscape scale disturbances in the genetic diversity and structure of an endangered palm tree, Euterpe edulis. We sampled and genotyped with microsatellite markers 544 juveniles of E. edulis in 17 fragments of Atlantic Forest in Brazil. In addition, we estimated the local logging rate and the forest cover and isolation at landscape scale. We found that the palm populations have not undergone any recent bottleneck events and that only logging intensification had affected the fixation index and the number of private alleles. Additionally, we did not detect any evidence of spatial genetic structure or genetic divergence associated with environmental disturbance variables at different scales. However, we identified distinct genetic clusters, which may indicate a reduction of gene flow between fragments that were previously a continuous habitat. Our results show that local disturbances, which act directly on population size reduction, such as logging, modified the genetic diversity more rapidly, whereas genetic structure is probably more influenced by large-scale modifications. In this way, to maximize the conservation efforts of economically exploited species, we recommend to increase the inspection to reduce the illegal exploitation, and reforestation of degraded areas, in order to increase the gene flow in Atlantic Forest fragments.

Direct and cascading effects of landscape structure on tropical forest and non-forest frugivorous birds.

Global biodiversity is increasingly threatened by land-use change, but the direct and indirect drivers of species diversity in human-modified tropical landscapes are poorly known. Forest-dependent species are expected to be particularly sensitive to changes in landscape composition (e.g., forest loss) and configuration (e.g., increase of forest edges), both directly and indirectly through cascading landscape effects on local patterns of forest structure and resource availability. In contrast, non-forest-dependent species are probably more strongly related to landscape changes than to local forest patterns, as these species are able to use resources not only from the forest, but also from other landscape elements over larger spatial scales. We tested these hypotheses using structural equation modeling. In particular, we sampled 20 landscapes (115 ha each) from the Brazilian Atlantic rainforest to assess the effect of landscape-scale forest cover and amount of forest edges on the diversity of frugivorous birds, both directly and indirectly through the effect that these landscape variables may have on vegetation complexity and fruit biomass. We separately assessed the response of forest-dependent and non-forest-dependent frugivores to infer potential mechanisms underlying bird assemblages in fragmented landscapes. The diversity of forest-dependent birds mainly decreased with the simplification of vegetation complexity in more deforested landscapes, but increased with increasing fruit biomass in more forested landscapes (indirect effects). Both patterns were significant, thus supporting a strong bottom-up control, i.e., local habitat simplification and resource scarcity in highly deforested landscapes limits the maintenance of forest-dependent birds. Conversely, but as expected, non-forest-dependent birds were more strongly and directly related to landscape-scale patterns. In particular, landscapes with higher forest edge amount showed higher bird species diversity, probably because the increasing length of ecotones and interspersion/juxtaposition of different habitat types in landscapes with more forest edges can increase resource availability and foraging efficiency of non-forest-dependent birds. As the seed dispersal services offered by forest-dependent species cannot be ecologically compensated for by the proliferation of non-forest-dependent species, preventing forest loss is imperative to maintain forest-dependent birds and forest regeneration in this vanishing biodiversity hotspot.

Functional decay in tree community within tropical fragmented landscapes: Effects of landscape-scale forest cover.

As tropical rainforests are cleared, forest remnants are increasingly isolated within agricultural landscapes. Understanding how forest loss impacts on species diversity can, therefore, contribute to identifying the minimum amount of habitat required for biodiversity maintenance in human-modified landscapes. Here, we evaluate how the amount of forest cover, at the landscape scale, affects patterns of species richness, abundance, key functional traits and common taxonomic families of adult trees in twenty Brazilian Atlantic rainforest landscapes. We found that as forest cover decreases, both tree community richness and abundance decline, without exhibiting a threshold. At the family-level, species richness and abundance of the Myrtaceae and Sapotaceae were also negatively impacted by the percent forest remaining at the landscape scale. For functional traits, we found a reduction in shade-tolerant, animal-dispersed and small-seeded species following a decrease in the amount of forest retained in landscapes. These results suggest that the amount of forest in a landscape is driving non-random losses in phylogenetic and functional tree diversity in Brazil's remaining Atlantic rainforests. Our study highlights potential restraints on the conservation value of Atlantic rainforest remnants in deforested landscapes in the future.

Landscape-scale deforestation decreases gene flow distance of a keystone tropical palm, Euterpe edulis Mart (Arecaceae).

Habitat loss represents one of the main threats to tropical forests, which have reached extremely high rates of species extinction. Forest loss negatively impacts biodiversity, affecting ecological (e.g., seed dispersal) and genetic (e.g., genetic diversity and structure) processes. Therefore, understanding how deforestation influences genetic resources is strategic for conservation. Our aim was to empirically evaluate the effects of landscape-scale forest reduction on the spatial genetic structure and gene flow of Euterpe edulis Mart (Arecaceae), a palm tree considered a keystone resource for many vertebrate species. This study was carried out in nine forest remnants in the Atlantic Forest, northeastern Brazil, located in landscapes within a gradient of forest cover (19-83%). We collected leaves of 246 adults and 271 seedlings and performed genotyping using microsatellite markers. Our results showed that the palm populations had low spatial genetic structure, indicating that forest reduction did not influence this genetic parameter for neither seedlings nor adults. However, forest loss decreased the gene flow distance, which may negatively affect the genetic diversity of future generations by increasing the risk of local extinction of this keystone palm. For efficient strategies of genetic variability conservation and maintenance of gene flow in E. edulis, we recommend the maintenance of landscapes with intermediary to high levels of forest cover, that is, forest cover above 40%.

Bicolored display of Miconia albicans fruits: Evaluating visual and physiological functions of fruit colors.

PREMISE OF THE STUDY: Most bird-dispersed fruits are green when unripe and become colored and conspicuous when ripe, signaling that fruits are ready to be consumed and dispersed. The color pattern for fruits of Miconia albicans (Melastomataceae), however, is the opposite, with reddish unripe and green ripe fruits. We (1) verified the maintenance over time of its bicolored display, (2) tested the communicative function of unripe fruits, (3) tested the photoprotective role of anthocyanins in unripe fruits, and (4) verified whether green ripe fruits can assimilate carbon. METHODS: Using a paired experiment, we tested whether detection of ripe fruits was higher on infructescences with unripe and ripe fruits compared with infructescences with only ripe fruits. We also measured and compared gas exchange, chlorophyll a fluorescence, and heat dissipation of covered (to prevent anthocyanin synthesis) and uncovered ripe and unripe fruits. KEY RESULTS: Although the bicolored display was maintained over time, unripe fruits had no influence on bird detection and removal of ripe fruits. Ripe and unripe fruits did not assimilate CO2, but they respired instead. CONCLUSIONS: Since the communicative function of unripe fruits was not confirmed, seed dispersers are unlikely to select the display with bicolored fruits. Because of the absence of photosynthetic activity in ripe and unripe fruits and enhanced photoprotective mechanisms in ripe fruits rather than in unripe fruits, we could not confirm the photoprotective role of anthocyanins in unripe fruits. As an alternative hypothesis, we suggest that the bicolored fruit display could be an adaptation to diversify seed dispersal vectors instead of restricting dispersal to birds and that anthocyanins in unripe fruits may have a defense role against pathogens.

Implications of Habitat Loss on Seed Predation and Early Recruitment of a Keystone Palm in Anthropogenic Landscapes in the Brazilian Atlantic Rainforest.

Habitat loss is the main driver of the loss of global biodiversity. Knowledge on this subject, however, is highly concentrated on species richness and composition patterns, with little discussion on the consequences of habitat loss for ecological interactions. Therefore, a systemic approach is necessary to maximize the success of conservation efforts by providing more realistic information about the effects of anthropogenic disturbances on natural environmental processes. We investigated the implications of habitat loss for the early recruitment of Euterpe edulis Martius, a keystone palm in the Brazilian Atlantic Forest, in nine sampling sites located in landscapes with different percentages of forest cover (9%-83%). We conducted a paired experiment using E. Edulis seeds set up in experimental stations composed of a vertebrate exclosure versus an open treatment. We used ANCOVA models with treatments as factors to assess the influence of habitat loss on the number of germinated seeds, predation by vertebrates and invertebrates, infestation by fungi, and number of seedlings established. Habitat loss did not affect the probability of transition from a dispersed to a germinated seed. However, when seeds were protected from vertebrate removal, seedling recruitment showed a positive relationship with the amount of forest cover. Seed infestation by fungi was not significant, and seed predation was the main factor limiting seed recruitment. The loss of forest cover antagonistically affected the patterns of seed predation by vertebrates and invertebrates; predation by invertebrates was higher in less forested areas, and predation by vertebrates was higher in forested areas. When seeds were exposed to the action of all biotic mortality factors, the number of recruited seedlings was very low and unrelated to habitat loss. This result indicates that the opposite effects of seed predation by vertebrates and invertebrates mask a differential response of E. edulis recruitment to habitat loss.

How colorful are fruits? Limited color diversity in fleshy fruits on local and global scales.

The colors of fleshy fruits are considered to be a signal to seed-dispersing animals, but their diversity remains poorly understood. Using an avian color space to derive a sensory morphospace for fruit color, we tested four hypotheses of fruit color diversity: fruit colors occupy a limited area of the color space; they are less diverse than flower colors; fruit colors within localities are similar to each other; and fruit color diversity reflects phylogeny. The global fruit color diversity of 948 primarily bird-dispersed plant species and the color diversity of localities were compared with null models of random, unconstrained evolution of fruit color. Fruit color diversity was further compared with the diversity of 1300 flower colors. Tests of phylogenetic effects on fruit color were used to assess the degree of correspondence with phylogeny. Global and local fruit color diversity was limited compared with null models and fruits have achieved only half the color diversity of flowers. Interestingly, we found little indication of phylogenetic conservatism. Constraints resulting from the chemical properties of pigments probably limit global fruit and flower color diversity. Different types of selection on fruits and flowers may further explain the smaller color diversity of fruits.

Diurnal frugivores on the Bromeliaceae Aechmea depressa L.B. Sm. from Northeastern Brazil: the prominent role taken by a small forest primate / Frugívoros diurnos de Aechmea depressa L.B. Sm. (Bromeliaceae) do Nordeste do Brasil e o papel proeminente de um pequeno primata florestal

Little is known about frugivory of epiphytes. We investigated diurnal frugivores consuming Aechmea depressa, an endemic species from Southern Bahia, Brazil, through 67 hours of observation on three fruiting individuals. Infructescences were visited for 2 percent of the time and only by golden-headed lion tamarins (GHLTs; Leontopithecus chrysomelas). Aechmea depressa invests on physical defense to retain fruits for prolonged periods, however, GHLTs used their small size and dexterity to remove rigid bracts and extract fruits from the infructescence. Prior studies indicate GHLTs disperse Aechmea seeds. Given the low visitation rates and probability that few frugivores successfully manipulate A. depressa fruits, we suggest that GHLTs are extremely important to maintaining the populations of this bromeliad species.

Pouco se sabe sobre a frugivoria em plantas epífitas. Nós investigamos os frugívoros diurnos de Aechmea depressa, uma espécie endêmica do Sul da Bahia através de 67 horas de observação dos frutos de três indivíduos. As infrutescências foram visitadas em 2 por cento do tempo somente por micos-leão-da-cara-dourada (MLCD; Leontopithecus chrysomelas). Aechmea depressa investe na defesa física para reter seus frutos por períodos prolongados entretanto, o MLCD utiliza seu pequeno tamanho e extrema destreza para remover as brácteas rígidas e extrair os frutos da infrutescência. Estudos prévios indicam que os MLCDs dispersam sementes de espécies de Aechmea. Baseando-se na baixa taxa de visitação e na probabilidade de que poucos frugívoros manipulem adequadamente os frutos de A. depressa, nós sugerimos que os MLCD sejam extremamente importantes para manter as populações desta espécie de Bromeliaceae.

The Crab-eating Fox (Cerdocyon thous) as a secondary seed disperser of Eugenia umbelliflora (Myrtaceae) in a Restinga forest of southeastern Brazil / O chachorro do mato (Cerdocyon thous) como dispersor secundário de Eugenia umbelliflora (Myrtaceae) em uma floresta de Restinga no sudeste do Brasil

The crab-eating fox (Cerdocyon thous) exhibits a very generalist habit and fruits compose a large proportion of its diet. However, few studies evaluated the importance of this animal as seed disperser. In the Restinga forest, in the Atlantic forest of Brazil, C. thous consumes fruits of Eugenia umbelliflora, a Myrtaceae species, which is dispersed chiefly by birds. This study evaluated the effects of gut transit on seed germination, and size selection of E. umbelliflora fruits by the crab-eating fox. We did not find differences on germination rates between seeds dispersed by foxes and control ones, but seeds dispersed by foxes germinated faster, which may be important for plant recruitment. Seeds consumed by C. thous were smaller than those available on the ground, indicating selection for small fruits. Regardless of the selection of small fruits, C. thous appears to be an important secondary disperser of E. umbelliflora, distributing large quantities of viable seeds of this Myrtaceae in the Restinga forest.

O cachorro do mato (Cerdocyon thous) tem um hábito bastante generalista e frutos compõem uma grande proporção de sua dieta. No entanto, poucos estudos avaliaram a importância deste animal como dispersor de sementes. Na floresta de restinga da Mata Atlântica brasileira C. thous consome frutos de Eugenia umbelliflora, uma espécie de Myrtaceae, que é dispersa principalmente por aves. Este estudo avaliou o efeito da passagem das sementes pelo tubo digestivo na germinação das sementes e a seleção de tamanho de frutos de E. umbelliflora pelo cachorro do mato. Não houve diferença nas taxas de germinação entre as sementes dispersas pelo cachorro do mato e as sementes controle, mas as sementes dispersas pelo cachorro germinaram mais rápido, o que pode ser importante para o recrutamento das plantas. As sementes consumidas pelo cachorro do mato foram menores do que as sementes disponíveis no solo, indicando seleção por frutos menores. Apesar de selecionarem frutos menores, o cachorro do mato parece ser um importante dispersor secundário de E. umbelliflora, distribuindo grandes quantidades de sementes viáveis desta espécie de Myrtaceae na restinga.

Geographic patterns in fruit colour diversity: do leaves constrain the colour of fleshy fruits?

We tested for geographic patterns in fruit colour diversity. Fruit colours are thought to promote detection by seed dispersers. Because seed dispersers differ in their spectral sensitivities, we predicted that fruit colour diversity would be higher in regions with higher seed disperser diversity (i.e. the tropics). We collected reflectance data on 232 fruiting plant species and their natural backgrounds in seven localities in Europe, North and South America, and analysed fruit colour diversity according to the visual system of birds-the primary consumer types of these fruits. We found no evidence that fruit colours are either more conspicuous or more diverse in tropical areas characterised by higher seed disperser diversity. Instead, fruit colour diversity was lowest in central Brazil, suggesting that fruit colours may be more diverse in temperate regions. Although we found little evidence for geographic variation in fruit hues, the spectral properties of fruits were positively associated with the spectral properties of backgrounds. This result implies that fruit colours may be influenced by selection on the reflectance properties of leaves, thus constraining the evolution of fruit colour. Overall, the results suggest that fruit colours in the tropics are neither more diverse nor more conspicuous than temperate fruits, and that fruit colours may be influenced by correlated selection on leaf reflectance properties.

Does attraction to frugivores or defense against pathogens shape fruit pulp composition?

Fruit traits evolve in response to an evolutionary triad between plants, seed dispersers, and antagonists that consume fruits but do not disperse seeds. The defense trade-off hypothesis predicts that the composition of nutrients and of secondary compounds in fruit pulp is shaped by a trade-off between defense against antagonists and attraction to seed dispersers. The removal rate model of this hypothesis predicts a negative relationship between nutrients and secondary compounds, whereas the toxin-titration model predicts a positive relationship. To test these alternative models, we evaluated whether the contents of nutrients and secondary compounds can be used to predict fruit removal by mutualists and pathogens in 14 bird-dispersed plants on a subtropical island in São Paulo state, southeastern Brazil. We selected eight to ten individuals of each species and prevented fruit removal by covering four branches with a net and left fruits on four other branches available to both, vertebrate fruit consumers and pathogens. The persistence of ripe fruits was drastically different among species for bagged and open fruits, and all fruit species persisted longer when protected against seed dispersers. We found that those fruits that are quickly removed by vertebrates are nutrient-rich, but although the attack rate of pathogens is also high, these fruits have low contents of quantitative defenses such as tannins and phenols. Thus, we suggest that the fruit removal rate by seed dispersers is the primary factor selecting the levels of fruit defense. Likewise, nutrient-poor fruits have low removal of seed dispersers and low probability of attack by pathogens. These species retain ripe fruits in an intact condition for a prolonged period because they are highly defended by secondary compounds, which reduce overall attractiveness. However, this strategy might be advantageous for plants that depend on rare or unreliable dispersers.