MelastomaTRAITs 1.0: A database of functional traits in Melastomataceae, a large pantropical angiosperm family.

The recent availability of open-access repositories of functional traits has revolutionized trait-based approaches in ecology and evolution. Nevertheless, the underrepresentation of tropical regions and lineages remains a pervasive bias in plant functional trait databases, which constrains large-scale assessments of plant ecology, evolution, and biogeography. Here, we present MelastomaTRAITs 1.0, a comprehensive and updatable database of functional traits for the pantropical Melastomataceae, the ninth-largest angiosperm family with 177 genera and more than 5800 species. Melastomataceae encompass species with a wide diversity of growth forms (herbs, shrubs, trees, epiphytes, and woody climbers), habitats (including tropical forests, savannas, grasslands, and wetlands from sea level to montane areas above the treeline), ecological strategies (from pioneer, edge-adapted and invasive species to shade-tolerant understory species), geographic distribution (from microendemic to continental-wide distribution), reproductive, pollination, and seed dispersal systems. MelastomaTRAITs builds on 581 references, such as taxonomic monographs, ecological research, and unpublished data, and includes four whole-plant traits, six leaf traits, 11 flower traits, 18 fruit traits, and 27 seed traits for 2520 species distributed in 144 genera across all 21 tribes. Most data come from the Neotropics where the family is most species-rich. Miconieae (the largest tribe) contains the highest number of trait records (49.6%) and species (41.1%) records. The trait types with the most information in the database were whole-plant traits, flowers, and leaf traits. With the breadth of functional traits recorded, our database helps to fill a gap in information for tropical plants and will significantly improve our capacity for large-scale trait-based syntheses across levels of organization, plant-animal interactions, regeneration ecology, and thereby support conservation and restoration programs. There are no copyright restrictions on the dataset; please cite this data paper when reusing the data.

Meta-analyses of reproductive changes in angiosperm populations in response to elevation reveal a lack of global patterns.

BACKGROUND AND AIMS: Elevation is a major factor shaping plant populations on a global scale. At the same time, reproductive traits play a major role in plant fitness. With increasing altitude and increasingly harsh conditions, decreases in pollinator visitation rates, sexual investment, seed set, and heterozygosity (due to increased selfing) are expected. In response, selection and/or phenotypic plasticity could lead to an increase in plants' floral displays to increase their attractiveness to pollinators and compensates for the negative fitness impacts of reduced pollinator activity. A large body of literature tests these hypotheses at the among-species level, but empirical evidence at the population level (i.e., wihin-species), where adaptive change may occur, is still limited to species-specific studies. Unravelling the global patterns of change in the reproductive traits, flower visitation rates and heterozygosity of plant populations across variable environmental conditions, especially climate can help us to understand how species are able to cope with shifting conditions associated with global change, particularly in mountains. Here, we used meta-analytic approaches to assess the reproductive changes of plant populations in response to elevation on a global scale. METHODS: We used a data set with 243 paired populations of plants at 'lower' and 'higher' elevations, spanning an elevation range of 0-4380 m asl and taken from 121 angiosperm species and 115 published studies. We analyzed changes in flower number, size and longevity, pollen production, flower visitation rate, seed set and expected heterozygosity.We then tested whether the observed patterns for each trait were dependent upon plant phylogeny and various ecogeographical factors and species traits. KEY RESULTS: We found no evidence of elevation having a global effect on the reproductive traits of angiosperm populations. This null global pattern was not affected by geograph or phylogenetics. CONCLUSIONS: Our results suggest that changes in reproductive traits, flower visitation rates, and heterozygosity in plant populations across elevations are specific to each species and ecosystem. Hence, macroevolutionary (across species) and macroecological patterns of elevation of plant reproduction reported previously are apparently not simply the outcome of microevolutionary changes (within species). This apparent specificity of response across plant species poses difficulties in predicting the effects of global changes and, specifically, climatic changes, on the fate of plant species, populations, and communities.

Wings are not perfect: increased wing asymmetry in a tropical butterfly as a response to forest fragmentation.

Habitat fragmentation and ecosystem changes have the potential to affect animal populations in different ways. To effectively monitor these changes, biomonitoring tools have been developed and applied to detect changes in population structure and/or individual traits that reflect such changes. Fluctuating asymmetry (FA) represents random deviations from perfect symmetry in bilateral traits from perfect symmetry in response to genetic and/or environmental stresses. In this study, we evaluated the use of FA as a tool to monitor stress caused by forest fragmentation and edge formation, using the tropical butterfly M. helenor (Nymphalidae) as a model species. We collected adult butterflies from three fragments of Atlantic Forest in Brazil encompassing both edge and interior habitats. Four wing traits (wing length, wing width, ocelli area, and ocelli diameter) were evaluated. Butterflies captured at edge sites exhibited higher FA values for wing length and wing width compared to those captured at interior sites, whereas traits related to ocelli did not show differences between the two habitat types. Our results suggest that the differences in abiotic and biotic conditions between forest interior and edges can act as a source of stress, impacting the symmetry of flight-related traits. On the other hand, as ocelli are crucial for butterfly camouflage and counter-predator strategies, our results indicate that this trait may be more conserved. By employing FA, we identified trait-specific responses to habitat fragmentation, thus suggesting its potential as a biomarker for environmental stress that can be used in butterflies to monitor habitat quality and change.

Among-species variation in flower size determines florivory in the largest tropical wetland.

PREMISE: Flower damage caused by florivores often has negative consequences for plant reproduction. However, the factors affecting plant-florivore interactions are still poorly understood, especially the role of abiotic factors and interspecific variation in florivory within ecosystems. Thus, the patterns of florivory levels and its consequences for plant communities need to be investigated further. METHODS: We assessed the influence of abiotic factors related to climatic seasonality, of phylogenetic relationships among plants, and of functional attributes associated with attractiveness to pollinators on florivory incidence and intensity in the Pantanal, the world's largest tropical wetland. Between December 2020 and November 2021, the percentage of flowers attacked (incidence) and petal area removed (intensity) by florivores were examined in 51 species from 25 families, considering flowering season, the substrate where the plants occur, and flower attributes as potentially determining factors on florivory levels. RESULTS: Phylogeny and environmental factors did not have a significant influence on florivory. The only determinant of interspecific variation in florivory incidence and intensity was flower size, where larger flowers experienced higher florivory levels regardless of season and substrate, while flower arrangement and color were not significant factors. CONCLUSIONS: Our study is one of the first to estimate the community-wide effects of biotic and abiotic factors on both the incidence and the intensity of florivory. The magnitude of this plant-florivore interaction may reduce reproductive success and entail selective pressures on plant attractiveness to pollinators.

Climate variability and aridity modulate the role of leaf shelters for arthropods: A global experiment.

Current climate change is disrupting biotic interactions and eroding biodiversity worldwide. However, species sensitive to aridity, high temperatures, and climate variability might find shelter in microclimatic refuges, such as leaf rolls built by arthropods. To explore how the importance of leaf shelters for terrestrial arthropods changes with latitude, elevation, and climate, we conducted a distributed experiment comparing arthropods in leaf rolls versus control leaves across 52 sites along an 11,790 km latitudinal gradient. We then probed the impact of short- versus long-term climatic impacts on roll use, by comparing the relative impact of conditions during the experiment versus average, baseline conditions at the site. Leaf shelters supported larger organisms and higher arthropod biomass and species diversity than non-rolled control leaves. However, the magnitude of the leaf rolls' effect differed between long- and short-term climate conditions, metrics (species richness, biomass, and body size), and trophic groups (predators vs. herbivores). The effect of leaf rolls on predator richness was influenced only by baseline climate, increasing in magnitude in regions experiencing increased long-term aridity, regardless of latitude, elevation, and weather during the experiment. This suggests that shelter use by predators may be innate, and thus, driven by natural selection. In contrast, the effect of leaf rolls on predator biomass and predator body size decreased with increasing temperature, and increased with increasing precipitation, respectively, during the experiment. The magnitude of shelter usage by herbivores increased with the abundance of predators and decreased with increasing temperature during the experiment. Taken together, these results highlight that leaf roll use may have both proximal and ultimate causes. Projected increases in climate variability and aridity are, therefore, likely to increase the importance of biotic refugia in mitigating the effects of climate change on species persistence.

Revisiting florivory: an integrative review and global patterns of a neglected interaction.

Florivory is an ancient interaction which has rarely been quantified due to a lack of standardized protocols, thus impairing biogeographical and phylogenetic comparisons. We created a global, continuously updated, open-access database comprising 180 species and 64 families to compare floral damage between tropical and temperate plants, to examine the effects of plant traits on floral damage, and to explore the eco-evolutionary dynamics of flower-florivore interactions. Flower damage is widespread across angiosperms, but was two-fold higher in tropical vs temperate species, suggesting stronger fitness impacts in the tropics. Flowers were mostly damaged by chewers, but neither flower color nor symmetry explained differences in florivory. Herbivory and florivory levels were positively correlated within species, even though the richness of the florivore community does not affect florivory levels. We show that florivory impacts plant fitness via multiple pathways and that ignoring this interaction makes it more difficult to obtain a broad understanding of the ecology and evolution of angiosperms. Finally, we propose a standardized protocol for florivory measurements, and identify key research avenues that will help fill persistent knowledge gaps. Florivory is expected to be a central research topic in an epoch characterized by widespread decreases in insect populations that comprise both pollinators and florivores.

How much leaf area do insects eat? A data set of insect herbivory sampled globally with a standardized protocol.

Herbivory is ubiquitous. Despite being a potential driver of plant distribution and performance, herbivory remains largely undocumented. Some early attempts have been made to review, globally, how much leaf area is removed through insect feeding. Kozlov et al., in one of the most comprehensive reviews regarding global patterns of herbivory, have compiled published studies regarding foliar removal and sampled data on global herbivory levels using a standardized protocol. However, in the review by Kozlov et al., only 15 sampling sites, comprising 33 plant species, were evaluated in tropical areas around the globe. In Brazil, which ranks first in terms of plant biodiversity, with a total of 46,097 species, almost half (43%) being endemic, a single data point was sampled, covering only two plant species. In an attempt to increase knowledge regarding herbivory in tropical plant species and to provide the raw data needed to test general hypotheses related to plant-herbivore interactions across large spatial scales, we proposed a joint, collaborative network to evaluate tropical herbivory. This network allowed us to update and expand the data on insect herbivory in tropical and temperate plant species. Our data set, collected with a standardized protocol, covers 45 sampling sites from nine countries and includes leaf herbivory measurements of 57,239 leaves from 209 species of vascular plants belonging to 65 families from tropical and temperate regions. They expand previous data sets by including a total of 32 sampling sites from tropical areas around the globe, comprising 152 species, 146 of them being sampled in Brazil. For temperate areas, it includes 13 sampling sites, comprising 59 species. Thus, when compared to the most recent comprehensive review of insect herbivory (Kozlov et al.), our data set has increased the base of available data for the tropical plants more than 460% (from 33 to 152 species) and the Brazilian sampling was increased 7,300% (from 2 to 146 species). Data on precise levels of herbivory are presented for more than 57,000 leaves worldwide. There are no copyright restrictions. Please cite this paper when using the current data in publications; the authors request to be informed how the data is used in the publications.

Towards the flower economics spectrum.

Understanding how floral traits affect reproduction is key for understanding genetic diversity, speciation, and trait evolution in the face of global changes and pollinator decline. However, there has not yet been a unified framework to characterize the major trade-offs and axes of floral trait variation. Here, we propose the development of a floral economics spectrum (FES) that incorporates the multiple pathways by which floral traits can be shaped by multiple agents of selection acting on multiple flower functions. For example, while pollinator-mediated selection has been considered the primary factor affecting flower evolution, selection by nonpollinator agents can reinforce or oppose pollinator selection, and, therefore, affect floral trait variation. In addition to pollinators, the FES should consider nonpollinator biotic agents and floral physiological costs, broadening the drivers of floral traits beyond pollinators. We discuss how coordinated evolution and trade-offs among floral traits and between floral and vegetative traits may influence the distribution of floral traits across biomes and lineages, thereby influencing organismal evolution and community assembly.

Frugivory and seed dispersal in a hyperdiverse plant clade and its role as a keystone resource for the Neotropical fauna.

BACKGROUND AND AIMS: Much of our understanding of the ecology and evolution of seed dispersal in the Neotropics is founded on studies involving the animal-dispersed, hyperdiverse plant clade Miconia (Melastomataceae). Nonetheless, no formal attempt has been made to establish its relevance as a model system or indeed provide evidence of the role of frugivores as Miconia seed dispersers. METHODS: We built three Miconia databases (fruit phenology/diaspore traits, fruit-frugivore interactions and effects on seed germination after gut passage) to determine how Miconia fruiting phenology and fruit traits for >350 species interact with and shape patterns of frugivore selection. In addition, we conducted a meta-analysis evaluating the effects of animal gut passage/seed handling on Miconia germination. KEY RESULTS: Miconia produce numerous small berries that enclose numerous tiny seeds within water- and sugar-rich pulps. In addition, coexisting species provide sequential, year long availability of fruits within communities, with many species producing fruits in periods of resource scarcity. From 2396 pairwise interactions, we identified 646 animal frugivore species in five classes, 22 orders and 60 families, including birds, mammals, reptiles, fish and ants that consume Miconia fruits. Endozoochory is the main dispersal mechanism, but gut passage effects on germination were specific to animal clades; birds, monkeys and ants reduced seed germination percentages, while opossums increased it. CONCLUSIONS: The sequential fruiting phenologies and wide taxonomic and functional diversity of animal vectors associated with Miconia fruits underscore the likely keystone role that this plant clade plays in the Neotropics. By producing fruits morphologically and chemically accessible to a variety of animals, Miconia species ensure short- and long-distance seed dispersal and constitute reliable resources that sustain entire frugivore assemblages.

Opposite latitudinal patterns for bird and arthropod predation revealed in experiments with differently colored artificial prey.

The strength of biotic interactions is generally thought to increase toward the equator, but support for this hypothesis is contradictory. We explored whether predator attacks on artificial prey of eight different colors vary among climates and whether this variation affects the detection of latitudinal patterns in predation. Bird attack rates negatively correlated with model luminance in cold and temperate environments, but not in tropical environments. Bird predation on black and on white (extremes in luminance) models demonstrated different latitudinal patterns, presumably due to differences in prey conspicuousness between habitats with different light regimes. When attacks on models of all colors were combined, arthropod predation decreased, whereas bird predation increased with increasing latitude. We conclude that selection for prey coloration may vary geographically and according to predator identity, and that the importance of different predators may show contrasting patterns, thus weakening the overall latitudinal trend in top-down control of herbivorous insects.

Fluctuating Asymmetry as a Bioindicator of Environmental Stress Caused by Pollution in a Pioneer Plant Species.

Fluctuating asymmetry (FA) is a widely used tool to detect developmental instability and plants under stressful conditions are expected to exhibit increased values of asymmetry, as well as higher levels of herbivory. This study evaluated whether dust from roads can cause major deviations in the axis of symmetry of leaves of the pioneer plant species Cecropia pachystachya Trécul (Urticaceae). It was also investigated whether plants exposed to dust have greater nitrogen content and higher levels of herbivory levels. Ten leaves of 20 individuals of C. pachystachya were collected on two roads with different levels of dust deposition and a control area. FA was calculated as the size-scaled difference between the right (RW) and left (LW) leaf widths and leaf area removed was determined by the ratio between leaf area removed and total leaf area. C. pachystachya plants in areas under strong influence of dust pollution exhibited the highest FA values (0.279 cm), whereas plants in the control area exhibited the lowest. A positive relationship between levels of leaf area removed by insects and a gradient of dust pollution was also observed. Differences in foliar nitrogen concentration among sampling areas indicated differences in leaf quality and influenced herbivory levels of Cecropia. This study indicated that FA can be used as an indicator of developmental instability of plants and those individuals under the impact of road dust and pollution might be more susceptible to insect attack.

A meta-analysis of the effects of fragmentation on herbivorous insects.

We reviewed the evidence for the effects of fragmentation on insects and plants by conducting a meta-analysis for the effects of artificial forest edge formation on insect herbivore abundance, herbivore richness, and plant herbivory, with data pooled from 31 studies and 159 independent comparisons. Hedge's d was used as the metric to combine all studies. Edge formation exhibited strong effects on plant herbivory rates, as edge plants exhibited 70% more damage than interior plants. Edges also increased herbivore abundance by 14% and herbivore richness by almost 65%, and effects of edge formation were stronger for Lepidoptera (mainly caterpillars) and Orthoptera. Edge effects were also stronger for forested ecosystems compared with open habitats and for temperate regions. Because the studies here evaluated did not simultaneously evaluate bottom-up and top-down factors, the mechanisms responsible for the patterns found cannot be properly addressed, although variation in host plant chemistry, relaxation of pressure exerted by natural enemies, or both, can be suggested as potential factors explaining variation in herbivory between edge and interior habitats. Higher herbivory rates on edge habitats, as shown by our meta-analytical review, have the potential to alter community composition and should be studied in detail to unravel their effects on ecosystem functioning.

Insect herbivores of Coccoloba cereifera do not select asymmetric plants.

Fluctuating asymmetry (FA) represents small, random variations from the symmetric bilateral pattern, and it is a frequently used measurement of plant and animal stresses. Some studies have shown a relationship between FA and herbivory, suggesting that FA might be a reliable indicator of plant quality and plant susceptibility to herbivore attack. In this study, we investigated the relationship between leaf FA of Coccoloba cereifera Schwacke (Polygonaceae) and the pattern of attack by the scale insect Abgrallaspis cyanophylly Signoret (Hemiptera: Diaspididae). Thirty individuals of C. cereifera were marked and followed during 2007 in southeastern Brazil, and all leaves of three shoots per plant were sampled, numbered, and categorized as young, mature, or senescent. We measured right and left widths of all leaves after digitizing the images to determine levels of FA for each leaf sampled per plant. Individuals of A. cyanophylli were counted using a stereoscope in the laboratory to determine infestation levels. Leaves of C. cereifera exhibited true patterns of FA, as shown by the normal distribution of asymmetry values. We observed high variation in attack rates by A. cyanophylly among C. cereifera individuals, with 43.3% of plants with no insects, whereas others exhibited up to 23,000 insects. No statistically significant relationship was observed between variation in FA and variation in A. cyanophylli among plants. These results suggest that FA cannot be used as an indicator of plant quality and susceptibility to herbivore attack but suggest that herbivores themselves might act as plant stressors.

Ants on plants: a meta-analysis of the role of ants as plant biotic defenses.

We reviewed the evidence on the role of ants as plant biotic defenses, by conducting meta-analyses for the effects of experimental removal of ants on plant herbivory and fitness with data pooled from 81 studies. Effects reviewed were plant herbivory, herbivore abundance, hemipteran abundance, predator abundance, plant biomass and reproduction in studies where ants were experimentally removed (n = 273 independent comparisons). Ant removal exhibited strong effects on herbivory rates, as plants without ants suffered almost twice as much damage and exhibited 50% more herbivores than plants with ants. Ants also influenced several parameters of plant fitness, as plants without ants suffered a reduction in biomass (-23.7%), leaf production (-51.8%), and reproduction (-24.3%). Effects were much stronger in tropical regions compared to temperate ones. Tropical plants suffered almost threefold higher herbivore damage than plants from temperate regions and exhibited three times more herbivores. Ant removal in tropical plants resulted in a decrease in plant fitness of about 59%, whereas in temperate plants this reduction was not statistically significant. Ant removal effects were also more important in obligate ant-plants (=myrmecophytes) compared to plants exhibiting facultative relationships with hemiptera or those plants with extrafloral nectaries and food bodies. When only tropical plants were considered and the strength of the association between ants and plants taken into account, plants with obligate association with ants exhibited almost four times higher herbivory compared to plants with facultative associations with ants, but similar reductions in plant reproduction. The removal of a single ant species increased plant herbivory by almost three times compared to the removal of several ant species. Altogether, these results suggest that ants do act as plant biotic defenses, but the effects of their presence are more pronounced in tropical systems, especially in myrmecophytic plants.

Perfect is best: low leaf fluctuating asymmetry reduces herbivory by leaf miners.

Fluctuating asymmetry (FA) represents small, random variation from symmetry and can be used as an indicator of plant susceptibility to herbivory. We investigated the effects of FA of two oak species, Quercus laevis and Q. geminata, and the responses of three herbivore guilds: leaf miners, gallers, and chewers. To examine differences in FA and herbivory between individuals, 40 leaves from each tree were collected, and FA indices were calculated. To examine differences in FA and herbivory within-individuals, we sampled pairs of mined and unmined leaves for asymmetry measurements. Differences in growth of leaf miners between leaf types were determined by tracing 50 mines of each species on symmetric leaves and asymmetric leaves. Asymmetric leaves contained significantly lower concentrations of tannins and higher concentrations of nitrogen than symmetric leaves for both plant species. Both frequency of asymmetric leaves on plants and levels of asymmetry positively influenced the abundance of Brachys, Stilbosis and other leaf miners, but no significant relationship between asymmetry and herbivory was observed for Acrocercops. Brachys and Stilbosis mines were smaller on asymmetric leaves, but differences in mine survivorship between symmetric and asymmetric leaves were observed only for Stilbosis mines. This study indicated that leaf miners might use leaf FA as a cue to plant quality, although differential survivorship among leaf types was not observed for all species studied. Reasons for the different results between guilds are discussed.