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.

Soil contamination in nearby natural areas mirrors that in urban greenspaces worldwide.

Soil contamination is one of the main threats to ecosystem health and sustainability. Yet little is known about the extent to which soil contaminants differ between urban greenspaces and natural ecosystems. Here we show that urban greenspaces and adjacent natural areas (i.e., natural/semi-natural ecosystems) shared similar levels of multiple soil contaminants (metal(loid)s, pesticides, microplastics, and antibiotic resistance genes) across the globe. We reveal that human influence explained many forms of soil contamination worldwide. Socio-economic factors were integral to explaining the occurrence of soil contaminants worldwide. We further show that increased levels of multiple soil contaminants were linked with changes in microbial traits including genes associated with environmental stress resistance, nutrient cycling, and pathogenesis. Taken together, our work demonstrates that human-driven soil contamination in nearby natural areas mirrors that in urban greenspaces globally, and highlights that soil contaminants have the potential to cause dire consequences for ecosystem sustainability and human wellbeing.

Soil biodiversity supports the delivery of multiple ecosystem functions in urban greenspaces.

While the contribution of biodiversity to supporting multiple ecosystem functions is well established in natural ecosystems, the relationship of the above- and below-ground diversity with ecosystem multifunctionality remains virtually unknown in urban greenspaces. Here we conducted a standardized survey of urban greenspaces from 56 municipalities across six continents, aiming to investigate the relationships of plant and soil biodiversity (diversity of bacteria, fungi, protists and invertebrates, and metagenomics-based functional diversity) with 18 surrogates of ecosystem functions from nine ecosystem services. We found that soil biodiversity across biomes was significantly and positively correlated with multiple dimensions of ecosystem functions, and contributed to key ecosystem services such as microbially driven carbon pools, organic matter decomposition, plant productivity, nutrient cycling, water regulation, plant-soil mutualism, plant pathogen control and antibiotic resistance regulation. Plant diversity only indirectly influenced multifunctionality in urban greenspaces via changes in soil conditions that were associated with soil biodiversity. These findings were maintained after controlling for climate, spatial context, soil properties, vegetation and management practices. This study provides solid evidence that conserving soil biodiversity in urban greenspaces is key to supporting multiple dimensions of ecosystem functioning, which is critical for the sustainability of urban ecosystems and human wellbeing.

The global distribution and environmental drivers of the soil antibiotic resistome.

BACKGROUND: Little is known about the global distribution and environmental drivers of key microbial functional traits such as antibiotic resistance genes (ARGs). Soils are one of Earth's largest reservoirs of ARGs, which are integral for soil microbial competition, and have potential implications for plant and human health. Yet, their diversity and global patterns remain poorly described. Here, we analyzed 285 ARGs in soils from 1012 sites across all continents and created the first global atlas with the distributions of topsoil ARGs. RESULTS: We show that ARGs peaked in high latitude cold and boreal forests. Climatic seasonality and mobile genetic elements, associated with the transmission of antibiotic resistance, were also key drivers of their global distribution. Dominant ARGs were mainly related to multidrug resistance genes and efflux pump machineries. We further pinpointed the global hotspots of the diversity and proportions of soil ARGs. CONCLUSIONS: Together, our work provides the foundation for a better understanding of the ecology and global distribution of the environmental soil antibiotic resistome. Video Abstract.

Global hotspots for soil nature conservation.

Soils are the foundation of all terrestrial ecosystems1. However, unlike for plants and animals, a global assessment of hotspots for soil nature conservation is still lacking2. This hampers our ability to establish nature conservation priorities for the multiple dimensions that support the soil system: from soil biodiversity to ecosystem services. Here, to identify global hotspots for soil nature conservation, we performed a global field survey that includes observations of biodiversity (archaea, bacteria, fungi, protists and invertebrates) and functions (critical for six ecosystem services) in 615 composite samples of topsoil from a standardized survey in all continents. We found that each of the different ecological dimensions of soils-that is, species richness (alpha diversity, measured as amplicon sequence variants), community dissimilarity and ecosystem services-peaked in contrasting regions of the planet, and were associated with different environmental factors. Temperate ecosystems showed the highest species richness, whereas community dissimilarity peaked in the tropics, and colder high-latitudinal ecosystems were identified as hotspots of ecosystem services. These findings highlight the complexities that are involved in simultaneously protecting multiple ecological dimensions of soil. We further show that most of these hotspots are not adequately covered by protected areas (more than 70%), and are vulnerable in the context of several scenarios of global change. Our global estimation of priorities for soil nature conservation highlights the importance of accounting for the multidimensionality of soil biodiversity and ecosystem services to conserve soils for future generations.

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.

Global homogenization of the structure and function in the soil microbiome of urban greenspaces.

The structure and function of the soil microbiome of urban greenspaces remain largely undetermined. We conducted a global field survey in urban greenspaces and neighboring natural ecosystems across 56 cities from six continents, and found that urban soils are important hotspots for soil bacterial, protist and functional gene diversity, but support highly homogenized microbial communities worldwide. Urban greenspaces had a greater proportion of fast-growing bacteria, algae, amoebae, and fungal pathogens, but a lower proportion of ectomycorrhizal fungi than natural ecosystems. These urban ecosystems also showed higher proportions of genes associated with human pathogens, greenhouse gas emissions, faster nutrient cycling, and more intense abiotic stress than natural environments. City affluence, management practices, and climate were fundamental drivers of urban soil communities. Our work paves the way toward a more comprehensive global-scale perspective on urban greenspaces, which is integral to managing the health of these ecosystems and the well-being of human populations.

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.

Bee-Mediated Selection Favors Floral Sex Specialization in a Heterantherous Species: Strategies to Solve the Pollen Dilemma.

Animal-pollinated plants show a broad variation in floral morphology traits and gametophyte production within populations. Thus, floral traits related to plant reproduction and sexuality are usually exposed to pollinator-mediated selection. Such selective pressures may be even stronger in heterantherous and pollen flowers, in which pollen contributes to both bee feeding and pollination, overcoming the "pollen dilemma" or the inability to perform both functions simultaneously. We describe the phenotypic gender and sexual organ morphology of flowers in two populations of Macairea radula (Melastomataceae), a heterantherous and buzz-pollinated species with pollen flowers. We estimated selection gradients on these traits through female and male fitness components. Both populations showed sizeable phenotypic gender variation, from strict hermaphrodites to increased femaleness or maleness. We found a continuous variation in style and stamen size, and this variation was correlated with corresponding shape values of both sexual organs. We detected bee-mediated selection towards short and long styles through seed number and towards intermediate degrees of heteranthery through pollen removal in one population, and selection towards increased maleness through pollen dispersal in both populations. Our results suggest that bee-mediated selection favors floral sex specialization and stylar dimorphism in M. radula, optimizing reproductive success and solving the pollen dilemma.

Water-use strategies in flowers from a neotropical savanna under contrasting environmental conditions during flowering.

Flowers require high amounts of water, which ultimately may compromise pollinator attractiveness under water limitation. Water-use and -conservation strategies in leaves from hot and dry ecosystems are well documented, yet little is known about mechanisms of water allocation in flowers, particularly in tropical savanna ecosystems. We evaluated traits related to corolla water status in two Kielmeyera species that differ in flowering phenology and flower size: larger-flowered K. regalis blooms during the rainy summer and smaller-flowered K. coriacea blooms during the dry winter. To test the hypothesis that water demand in corollas increases with increasing vapor pressure deficit (VPD), we analyzed interspecific differences in corolla stomatal conductance and density, water content, and fresh and dry mass per unit area. We also performed hand-pollination and pollinator-exclusion experiments to determine variation in floral longevity. Corolla transpiration rates were higher in K. coriacea (157 vs 95 g·H2O·m-2·h-1 for K. coriacea and K. regalis, respectively), and increased with VPD in both species. Stomatal density was 25-fold higher in K. coriacea, and corolla fresh and dry mass per unit of area were 47% and 21% higher, respectively, in K. coriacea, due to thick pectin-rich cell walls. The high pectin content increases water content in corollas of K. coriacea. Regardless of pollination, flowers lasted one day in K. coriacea and three in K. regalis. Our study suggests structure-function relationships of floral traits with flowering season, and that K. coriacea displays small and short-lived corollas with high water content to buffer the high evaporative demand during the dry period.

Reproductive assurance weakens pollinator-mediated selection on flower size in an annual mixed-mating species.

BACKGROUND AND AIMS: In animal-pollinated plants, direct and indirect selection for large and small flowers in predominantly outcrossing and selfing species, respectively, is a common consequence of pollen limitation (PL). However, many hermaphroditic species show a mixed-mating system known as delayed selfing, which provides reproductive assurance (RA) only when outcrossing is not realized. Although RA is expected to reduce pollinator-mediated selection towards larger flowers, the consequences of delayed selfing for selection on flower size in mixed-mating species remain overlooked. We investigated whether RA weakens selection on flower size in Tuberaria guttata, a mixed-mating annual herb. METHODS: We related pollinator visitation rates to flower size and measured seed production in emasculated, hand cross-pollinated and intact (control) flowers in three natural populations. For each population, we estimated variation in PL and RA across individuals differing in flower size and phenotypic selection on this trait. KEY RESULTS: Pollinator visitation increased and RA decreased with flower size in all populations. Increasing RA diminished but did not fully alleviate PL, because of early-acting inbreeding depression. In the least-visited and most pollen-limited population, RA increased seed production by >200 %, intensely counteracting the strong pollinator-mediated selection for larger corollas. In the most-visited population, however, RA increased seed production by an average of only 9 %. This population exhibited the largest fraction of individuals that showed a decrease in seed production due to selfing and the weakest pollinator-mediated selection on flower size. CONCLUSIONS: The results suggest that the balance between the extent of RA and outcrossing contributes to determine flower size in mixed-mating systems. Pollinator-mediated selection favours larger flowers by increasing outcrossed seeds, but the benefits of RA greatly lessen this effect, especially under severe conditions of pollen limitation. Our findings also indicate that a mixed-mating system can represent an 'evolutionary trap' under an adequate pollinator supply.

Intraspecific variation in fruit-frugivore interactions: effects of fruiting neighborhood and consequences for seed dispersal.

The extent of specialization/generalization continuum in fruit-frugivore interactions at the individual level remains poorly explored. Here, we investigated the interactions between the Neotropical treelet Miconia irwinii (Melastomataceae) and its avian seed dispersers in Brazilian campo rupestre. We built an individual-based network to derive plant degree of interaction specialization regarding disperser species. Then, we explored how intraspecific variation in interaction niche breadth relates to fruit availability on individual plants in varying densities of fruiting conspecific neighbors, and how these factors affect the quantity of viable seeds dispersed. We predicted broader interaction niche breadths for individuals with larger fruit crops in denser fruiting neighborhoods. The downscaled network included nine bird species and 15 plants, which varied nearly five-fold in their degree of interaction specialization. We found positive effects of crop size on visitation and fruit removal rates, but not on degree of interaction specialization. Conversely, we found that an increase in the density of conspecific fruiting neighbors both increased visitation rate and reduced plant degree of interaction specialization. We suggest that tracking fruit-rich patches by avian frugivore species is the main driver of density-dependent intraspecific variation in plants' interaction niche breadth. Our study shed some light on the overlooked fitness consequences of intraspecific variation in interaction niches by showing that individuals along the specialization/generalization continuum may have their seed dispersed with similar effectiveness. Our study exemplifies how individual-based networks linking plants to frugivore species that differ in their seed dispersal effectiveness can advance our understanding of intraspecific variation in the outcomes of fruit-frugivore interactions.

Assessing bias and knowledge gaps on seed ecology research: implications for conservation agenda and policy.

Sampling biases permeate ecological research and result in knowledge gaps that have vital consequences for conservation planning. The consequences of knowledge gaps on species identity and distribution (the Wallacean and Linnean shortfalls, respectively) have become apparent recently, but we know little about the extent that research biases and knowledge gaps on traits that influence species' niches (the Hutchinsonian shortfall) affect conservation policy. To examine whether knowledge of species' traits based on seed ecology is geographically, phylogenetically, and ecologically biased, we retrieved research data on seed germination, seed dormancy, seed dispersal, seed banks, seed predation, and seed removal from a database of 847 papers, 1648 species, and 5322 cases. Brazil was selected as a model system for megadiverse, undersampled countries. Kernel density maps showed that research was geographically biased towards highly populated sites, with vast areas remaining historically unexplored. We also show that research was clustered into protected areas. We detected a significant positive phylogenetic bias at genus-level, indicating research concentration in few genera and lower relative bias rates for many herbaceous genera. Unexpectedly, information on seed banking was available for only 74 (3.4%) of threatened species, which suggests that information deficits are highest for species with critical needs for ex situ conservation strategies. Tree, fleshy-fruited, and biotic dispersal species were disproportionately overstudied. Our data indicate that information deficits on seed ecology preclude our ability to effectively restore ecosystems and to safeguard endangered species. We call for a systematic improvement of environmental agenda in which policy makers and scientists target sites, clades, and functional groups historically neglected. Lessons from developed countries and collaborative efforts will be important for megadiverse, underdeveloped countries to achieve the targets of international agreements that depend on seed ecology knowledge aiming to secure biological diversity and ecosystem services.

Large and abundant flowers increase indirect costs of corollas: a study of coflowering sympatric Mediterranean species of contrasting flower size.

Large floral displays receive more pollinator visits but involve higher production and maintenance costs. This can result in indirect costs which may negatively affect functions like reproductive output. In this study, we explored the relationship between floral display and indirect costs in two pairs of coflowering sympatric Mediterranean Cistus of contrasting flower size. We hypothesized that: (1) corolla production entails direct costs in dry mass, N and P, (2) corollas entail significant indirect costs in terms of fruit set and seed production, (3) indirect costs increase with floral display, (4) indirect costs are greater in larger-flowered sympatric species, and (5) local climatic conditions influence indirect costs. We compared fruit set and seed production of petal-removed flowers and unmanipulated control flowers and evaluated the influence of mean flower number and mean flower size on relative fruit and seed gain of petal-removed and control flowers. Fruit set and seed production were significantly higher in petal-removed flowers in all the studied species. A positive relationship was found between relative fruit gain and mean individual flower size within species. In one pair of species, fruit gain was higher in the large-flowered species, as was the correlation between fruit gain and mean number of open flowers. In the other pair, the correlation between fruit gain and mean flower size was also higher in the large-flowered species. These results reveal that Mediterranean environments impose significant constraints on floral display, counteracting advantages of large flowers from the pollination point of view with increased indirect costs of such flowers.

Impacts of changes in land use and fragmentation patterns on Atlantic coastal forests in northern Spain.

Changes in forested landscapes may have important consequences for ecosystem services and biodiversity conservation. In northern Spain, major changes in land use occurred during the second half of the 20th century, but their impacts on forests have not been quantified. We evaluated the dynamics of landscape and forest distribution patterns between 1957 and 2003 in Fragas do Eume Natural Park (northwestern Spain). We used orthoimages and a set of standard landscape metrics to determine transitions between land cover classes and to examine forest distribution patterns. Eucalypt plantations showed the greatest increase in area (197%) over time. Furthermore, transitions to eucalypt plantations were found in all major land cover classes. Forest showed a net decline of 20% in total area and represented 30% of the landscape area in 2003. Forest losses were mainly due to eucalypt plantations and the building of a water reservoir, while forest gains were due to increases in shrubland, meadows and cultivated fields which had been recolonised. Forest patch size and core area decreased, and edge length increased over time. In turn, increases were obtained in mean distance between forest patches, and in adjacency to eucalypt plantations and to a water reservoir. These results suggest an increase in forest fragmentation from 1957 to 2003, as well as a change in the nature of the habitat surrounding forest patches. This study shows that land use changes, mostly from eucalypt plantation intensification, negatively affected forested habitats, although some regeneration was ongoing through ecological succession from land abandonment.