Characterization Factors to Assess Land Use Impacts on Pollinator Abundance in Life Cycle Assessment.

While wild pollinators play a key role in global food production, their assessment is currently missing from the most commonly used environmental impact assessment method, Life Cycle Assessment (LCA). This is mainly due to constraints in data availability and compatibility with LCA inventories. To target this gap, relative pollinator abundance estimates were obtained with the use of a Delphi assessment, during which 25 experts, covering 16 nationalities and 45 countries of expertise, provided scores for low, typical, and high expected abundance associated with 24 land use categories. Based on these estimates, this study presents a set of globally generic characterization factors (CFs) that allows translating land use into relative impacts to wild pollinator abundance. The associated uncertainty of the CFs is presented along with an illustrative case to demonstrate the applicability in LCA studies. The CFs based on estimates that reached consensus during the Delphi assessment are recommended as readily applicable and allow key differences among land use types to be distinguished. The resulting CFs are proposed as the first step for incorporating pollinator impacts in LCA studies, exemplifying the use of expert elicitation methods as a useful tool to fill data gaps that constrain the characterization of key environmental impacts.

Managed honeybees decrease pollination limitation in self-compatible but not in self-incompatible crops.

Modern agriculture is becoming increasingly pollinator-dependent. However, the global stock of domesticated honeybees is growing at a slower rate than its demand, while wild bees are declining worldwide. This uneven scenario of high pollinator demand and low pollinator availability can translate into increasing pollination limitation, reducing the yield of pollinator-dependent crops. However, overall assessments of crop pollination limitation and the factors determining its magnitude are missing. Based on 52 published studies including 30 crops, we conducted a meta-analysis comparing crop yield in pollen-supplemented versus open-pollinated flowers. We assessed the overall magnitude of pollination limitation and whether this magnitude was influenced by (i) the presence/absence of managed honeybees, (ii) crop compatibility system (i.e. self-compatible/self-incompatible) and (iii) the interaction between these two factors. Overall, pollen supplementation increased yield by approximately 34%, indicating sizable pollination limitation. Deployment of managed honeybees and self-compatibility were associated with lower pollination limitation. Particularly, active honeybee management decreased pollination limitation among self-compatible but apparently not among self-incompatible crops. These findings indicate that current pollination regimes are, in general, inadequate to maximize crop yield, even when including managed honeybees, and stress the need of transforming the pollination management paradigm of agricultural landscapes.

Behavioural responses by a bumble bee to competition with a niche-constructing congener.

While feeding, foragers can alter their environment. Such alteration constitutes ecological niche construction (ENC) if it enables future benefits for the constructor and conspecific individuals. The environmental modification may also affect non-constructing, bystander species, especially if they share resources with constructor species. If so, ENC could confer the constructor species a competitive advantage by both enhancing its foraging returns and reducing those of bystander species. Expectations - (E1) ENC frequency should vary positively with the recent and current density of the constructor species, and (E2) constructors should use modifications disproportionately. In contrast, bystanders should (E3) experience intensified competition for the affected resource, and (E4) exhibit diverse, possibly mitigating, responses to ENC, depending on opportunity and relative benefits. We investigated these expectations in Argentina for competition for Fuchsia magellanica nectar between an invasive bumble bee Bombus terrestris (terr: putative constructor), which often bites holes at the bases of floral tubes to rob nectar, and native B. dahlbomii (dahl: bystander), which normally accesses Fuchsia nectar through the flower mouth (front visits). Robbing holes constitute ENC, as they persist until the 7-day flowers wilt. The dynamics of the incidence of robbed flowers, abundance of both bees and the number and types of their flower visits (front or robbing) were characterised by alternate-day surveys of plants during 2.5 months. After initially accessing Fuchsia nectar via front visits, terr switched to robbing and its abundance on Fuchsia increased 20-fold within 10 days (E2). Correspondingly, the incidence of robbed flowers varied positively with recent and past terr abundance (E1). In contrast, dahl abundance remained low and varied negatively with the incidence of robbed flowers (E3). When terr ceased visiting Fuchsia, dahl abundance increased sixfold within 10 days (E3), possibly because many dahl previously had avoided competition with terr by feeding on other plant species (E4). While terr was present, dahl on Fuchsia used front visits (tolerance) or used existing robbing holes (adoption: E4). The diverse dahl responses suggest partial compensation for competition with terr. ENC alters competitive asymmetry, favouring constructor species. However, bystander responses can partially offset this advantage, perhaps facilitating coexistence.

Los animales pueden alterar su ambiente como consecuencia del forrajeo. Esta alteración constituye una forma de construcción de nicho ecológico (CNE) cuando la misma promueve beneficios para el constructor y otros individuos de la misma especie. Esta modificación ambiental puede también afectar otras especies no involucradas directamente en la CNE, especialmente cuando comparten recursos con la especie constructora. En este caso, la CNE puede conferir una ventaja competitiva a la especie constructora, incrementado sus beneficios alimenticios en detrimento de los de las especies no constructoras. Expectativas - (E1) La frecuencia de eventos de CNE debería variar positivamente con la densidad presente y pasada de la especie constructora, y (E2) los individuos de la especie constructora deberían usar las modificaciones asociadas a la CNE en forma diferencial. Por el contrario, los individuos de las otras especies que usen el mismo recurso deberían (E3) experimentar una intensificación de la competencia, y (E4) exhibir una diversidad de respuestas, algunas que atenúen las consecuencias negativas de la CNE, lo que va a depender de la oportunidad y de los beneficios relativos. En Argentina, investigamos el cumplimiento de estas expectativas en la competencia por el néctar de Fuchsia magellanica entre el abejorro invasor, Bombus terrestris (terr: la especie constructora), quien frecuentemente agujerea la base de tubos florales para robar néctar, y el abejorro nativo B. dahlbomii (dahl: la especie afectada), quien normalmente accede al néctar de Fuchsia en forma legítima a través de la apertura de la flor (visitas frontales). Los agujeros realizados por terr constituyen un caso de CNE, ya que persisten a lo largo de la vida de la vida de la flor (aprox. 7-day). En este trabajo relevamos la incidencia de flores robadas, la abundancia de las dos especies de abejas, y el número y tipo de sus visitas florales (frontales o de robo) día por medio durante 2.5 meses. Inicialmente terr accedió las flores de Fuchsia frontalmente, pero más tarde cambió su comportamiento convirtiéndose en un robador casi exclusivo a lo largo de un período de 10 días en que su abundancia se incrementó 20 veces (E2). En consecuencia, la incidencia de flores robadas varió positivamente con la abundancia de terr presente y pasada (E1). Por el contrario, la abundancia de dahl fue baja y varió negativamente con la incidencia de flores robadas (E3). En particular, la abundancia de dahl se incrementó seis veces en un período de 10 días una vez que terr cesó de visitar las flores de Fuchsia (E3), posiblemente porque dahl evitó la competencia con terr forrajeando en otras especies de plantas (E4). Cuando terr estuvo presente, dahl visitó las flores de Fuchsia frontalmente (tolerancia) o usó los agujeros existentes (adopción de comportamiento robador: E4). Estas respuestas diversas de dahl sugieren una compensación parcial de los efectos negativos de la competencia con terr. La CNE incrementa la asimetría de la competencia, favoreciendo la especie constructora. Sin embargo, las diferentes respuestas de las especies afectadas pueden compensar parcialmente esta desventaja competitiva, tal vez facilitando la coexistencia.

Clinal versus disruptive latitudinal variation in fruit traits of a South American mistletoe.

Fruit traits have historically been interpreted as plant adaptations to their seed dispersers. On the other hand, different environmental factors, which vary spatially and temporally, can shape fruit-trait variation. The mistletoe Tristerix corymbosus has a latitudinal distribution along the South American Pacific rim that encompasses two different biomes, the matorral of central Chile and the temperate forest that extends south of the matorral. This mistletoe shows contrasting fruiting phenology (spring vs summer), fruit color (yellow vs green), and seed dispersers (birds vs marsupial) in these two biomes. We characterized geographic variation of morphological and nutritional fruit traits of T. corymbosus to evaluate which macroecological factor, biome or latitude, better explains spatial variation in these variables. For each of 22 populations, we obtained environmental data (temperature, precipitation, and canopy cover), measured fruit and seed morphology traits (size, shape, and weight), and pulp moisture and nutritional content (fiber, protein, fat, carbohydrates, ash, and caloric content). Patterns of variation for each variable were described by fitting and comparing five different simple models varying in slope, intercept or both. Fruit morphology showed a clear biome-related disruptive pattern, seed morphological traits were unrelated to either biome or latitude, whereas nutritional variables showed diverse patterns. Different environmental factors seem to affect fruit development and phenology, determining the observed fruit characteristics, with seed dispersers playing a minor role in shaping these patterns. More generally, the contrasting plant-seed disperser associations we addressed can be interpreted as the outcome of an ecological-fitting rather than of a coevolutionary process.

Safeguarding pollinators and their values to human well-being.

Wild and managed pollinators provide a wide range of benefits to society in terms of contributions to food security, farmer and beekeeper livelihoods, social and cultural values, as well as the maintenance of wider biodiversity and ecosystem stability. Pollinators face numerous threats, including changes in land-use and management intensity, climate change, pesticides and genetically modified crops, pollinator management and pathogens, and invasive alien species. There are well-documented declines in some wild and managed pollinators in several regions of the world. However, many effective policy and management responses can be implemented to safeguard pollinators and sustain pollination services.

Intentional and unintentional selection during plant domestication: herbivore damage, plant defensive traits and nutritional quality of fruit and seed crops.

Greater susceptibility to herbivory can arise as an effect of crop domestication. One proposed explanation is that defenses decreased intentionally or unintentionally during the domestication process, but evidence for this remains elusive. An alternative but nonexclusive explanation is presumed selection for higher nutritional quality. We used a metaanalytical approach to examine susceptibility to herbivores in fruit and seed crops and their wild relatives. Our analyses provide novel insights into the mechanisms of increased susceptibility by evaluating whether it can be attributed to either a reduction in herbivore defensive traits, including direct/indirect and constitutive/inducible defenses, or an increase in the nutritional content of crops. The results confirm higher herbivory and lower levels of all types of defenses in crops compared to wild relatives, although indirect defenses were more affected than direct ones. Contrary to expectations, nutritional quality was lower in crops than in wild relatives, which may enhance biomass loss to herbivores if they increase consumption to meet nutritional requirements. Our findings represent an important advance in our understanding of how changes in defensive and nutritional traits following domestication could influence, in combination or individually, crop susceptibility to herbivore attacks.

The dynamic mosaic phenotypes of flowering plants.

Ecological interaction and adaptation both depend on phenotypic characteristics. In contrast with the common conception of the 'adult' phenotype, plant bodies develop continuously during their lives. Furthermore, the different units (metamers) that comprise plant bodies are not identical copies, but vary extensively within individuals. These characteristics foster recognition of plant phenotypes as dynamic mosaics. We elaborate this conception based largely on a wide-ranging review of developmental, ecological and evolutionary studies of plant reproduction, and identify its utility in the analysis of plant form, function and diversification. An expanded phenotypic conception is warranted because dynamic mosaic features affect plant performance and evolve. Evidence demonstrates that dynamic mosaic phenotypes enable functional ontogeny, division of labour, resource and mating efficiency. In addition, dynamic mosaic features differ between individuals and experience phenotypic selection. Investigation of the characteristics and roles of dynamic and mosaic features of plant phenotypes benefits from considering within-individual variation as a function-valued trait that can be analysed with functional data methods. Phenotypic dynamics and within-individual variation arise despite an individual's genetic uniformity, and develop largely by heterogeneous gene expression and associated hormonal control. These characteristics can be heritable, so that dynamic mosaic phenotypes can evolve and diversify by natural selection.

Global agricultural productivity is threatened by increasing pollinator dependence without a parallel increase in crop diversification.

The global increase in the proportion of land cultivated with pollinator-dependent crops implies increased reliance on pollination services. Yet agricultural practices themselves can profoundly affect pollinator supply and pollination. Extensive monocultures are associated with a limited pollinator supply and reduced pollination, whereas agricultural diversification can enhance both. Therefore, areas where agricultural diversity has increased, or at least been maintained, may better sustain high and more stable productivity of pollinator-dependent crops. Given that >80% of all crops depend, to varying extents, on insect pollination, a global increase in agricultural pollinator dependence over recent decades might have led to a concomitant increase in agricultural diversification. We evaluated whether an increase in the area of pollinator-dependent crops has indeed been associated with an increase in agricultural diversity, measured here as crop diversity, at the global, regional, and country scales for the period 1961-2016. Globally, results show a relatively weak and decelerating rise in agricultural diversity over time that was largely decoupled from the strong and continually increasing trend in agricultural dependency on pollinators. At regional and country levels, there was no consistent relationship between temporal changes in pollinator dependence and crop diversification. Instead, our results show heterogeneous responses in which increasing pollinator dependence for some countries and regions has been associated with either an increase or a decrease in agricultural diversity. Particularly worrisome is a rapid expansion of pollinator-dependent oilseed crops in several countries of the Americas and Asia that has resulted in a decrease in agricultural diversity. In these regions, reliance on pollinators is increasing, yet agricultural practices that undermine pollination services are expanding. Our analysis has thereby identified world regions of particular concern where environmentally damaging practices associated with large-scale, industrial agriculture threaten key ecosystem services that underlie productivity, in addition to other benefits provided by biodiversity.

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.

Coevolution Slows the Disassembly of Mutualistic Networks.

Important groups of mutualistic species are threatened worldwide, and identifying factors that make them more or less fragile in the face of disturbance is becoming increasingly critical. Although much research has focused on identifying the ecological factors that favor the stability of communities rich in mutualists, much less has been devoted to understanding the role played by historical and contemporary evolution. Here we develop mathematical models and computer simulations of coevolving mutualistic communities that allow us to explore the importance of coevolution in stabilizing communities against anthropogenic disturbance. Our results demonstrate that communities with a long history of coevolution are substantially more robust to disturbance, losing individual species and interactions at lower rates. In addition, our results identify a novel phenomenon-coevolutionary rescue-that mitigates the impacts of ongoing anthropogenic disturbance by rewiring the network structure of the community in a way that compensates for the extinction of individual species and interactions.

The costs and benefits of pollinator dependence: empirically based simulations predict raspberry fruit quality.

Globally, agriculture increasingly depends on pollinators to produce many seed and fruit crops. However, what constitutes optimal pollination service for pollinator-dependent crops remains unanswered. We developed a simulation model to identify the optimal pollination service that maximizes fruit quality in crops. The model depicts the pollination (i.e., autonomous self-fertilization, pollen deposition) and post-pollination (i.e., pollen germination, and time from germination to ovule fertilization) processes leading to fruit and seed set and allows for negative flower-pollinator interactions, specifically pistil damage. We parameterized and validated the model based on empirical observations of commercial raspberry in western Argentina. To assess the effects of pollination intensity for fruit production, we conducted simulations over a range of visit number per flower by the two primary managed pollinators worldwide, Apis mellifera and Bombus terrestris. Simulations identified that ~15-35 visits per flower by A. mellifera or ~10-20 visits by B. terrestris provide adequate pollination and maximize raspberry fruit quality (i.e., estimated as the proportion of ovules that develop into drupelets). Visits in excess of these optima reduce simulated fruit quality, and flowers receiving >670 honey bee visits or >470 bumble bee visits would produce fruits of poorer quality than those receiving no bee visits. The simulations generated consistent, unbiased predictions of fruit quality for 12 raspberry fields. This model could be adapted easily to other animal-pollinated crops and used to guide efficient pollinator management in any agro-ecosystem.

Global decline of bumblebees is phylogenetically structured and inversely related to species range size and pathogen incidence.

Conservation biology can profit greatly from incorporating a phylogenetic perspective into analyses of patterns and drivers of species extinction risk. We applied such an approach to analyse patterns of bumblebee (Bombus) decline. We assembled a database representing approximately 43% of the circa 260 globally known species, which included species extinction risk assessments following the International Union fo Conservation of Nature Red List categories and criteria, and information on species traits presumably associated with bumblebee decline. We quantified the strength of phylogenetic signal in decline, range size, tongue length and parasite presence. Overall, about one-third of the assessed bumblebees are declining and declining species are not randomly distributed across the Bombus phylogeny. Susceptible species were over-represented in the subgenus Thoracobombus (approx. 64%) and under-represented in the subgenus Pyrobombus (approx. 6%). Phylogenetic logistic regressions revealed that species with small geographical ranges and those in which none of three internal parasites were reported (i.e. Crithidia bombi, Nosema spp. or Locustacarus buchneri) were particularly vulnerable. Bumblebee evolutionary history will be deeply eroded if most species from threatened clades, particularly those stemming from basal nodes, become finally extinct. The habitat of species with restricted distribution should be protected and the importance of pathogen tolerance/resistance as mechanisms to deal with pathogens needs urgent research.

The population ecology of male gametophytes: the link between pollination and seed production.

The fate of male gametophytes after pollen reaches stigmas links pollination to ovule fertilisation, governing subsequent siring success and seed production. Although male gametophyte performance primarily involves cellular processes, an ecological analogy may expose insights into the nature and implications of male gametophyte success. We elaborate this analogy theoretically and present empirical examples that illustrate associated insights. Specifically, we consider pollen loads on stigmas as localised populations subject to density-independent mortality and density-dependent processes as they traverse complex stylar environments. Different combinations of the timing of pollen-tube access to limiting stylar resources (simultaneous or sequential), the tube distribution among resources (repulsed or random) and the timing of density-independent mortality relative to competition (before or after) create signature relations of mean pollen-tube success and its variation among pistils to pollen receipt. Using novel nonlinear regression analyses (two-moment regression), we illustrate contrasting relations for two species, demonstrating that variety in these relations is a feature of reproductive diversity among angiosperms, rather than merely a theoretical curiosity. Thus, the details of male gametophyte ecology should shape sporophyte reproductive success and hence the dynamics and structure of angiosperm populations.

The phylogenetic structure of plant-pollinator networks increases with habitat size and isolation.

Similarity among species in traits related to ecological interactions is frequently associated with common ancestry. Thus, closely related species usually interact with ecologically similar partners, which can be reinforced by diverse co-evolutionary processes. The effect of habitat fragmentation on the phylogenetic signal in interspecific interactions and correspondence between plant and animal phylogenies is, however, unknown. Here, we address to what extent phylogenetic signal and co-phylogenetic congruence of plant-animal interactions depend on habitat size and isolation by analysing the phylogenetic structure of 12 pollination webs from isolated Pampean hills. Phylogenetic signal in interspecific interactions differed among webs, being stronger for flower-visiting insects than plants. Phylogenetic signal and overall co-phylogenetic congruence increased independently with hill size and isolation. We propose that habitat fragmentation would erode the phylogenetic structure of interaction webs. A decrease in phylogenetic signal and co-phylogenetic correspondence in plant-pollinator interactions could be associated with less reliable mutualism and erratic co-evolutionary change.

Diverse ecological relations of male gametophyte populations in stylar environments.

PREMISE OF STUDY: Pollen on a stigma represents a local population of male gametophytes vying for access to female gametophytes in the associated ovary. As in most populations, density-independent and density-dependent survival depend on intrinsic characteristics of male gametophytes and environmental (pistil) conditions. These characteristics and conditions could differ among flowers, plants, populations, and species, creating diverse male-gametophyte population dynamics, which can influence seed siring and production. METHODS: For nine species, we characterized the relations of both the mean and standard deviation of pollen-tube number at the style base to pollen receipt with nonlinear regression. Models represented asymptotic or peaked relations, providing information about the incidence and magnitude of facilitation and competition, the spatial and temporal characteristics of competition, and the intensity and relative timing of density-independent mortality. KEY RESULTS: We infer that pollen tubes of most species competed sequentially, their tips ceasing growth if earlier tubes had depleted stylar space/resources; although two species experienced simultaneous competition. Tube success of three species revealed positive density dependence (facilitation) at low density. For at least four species, density-independent mortality preceded competition. Tube success varied mostly within plants, rather than among plants or conspecific populations. Pollen quality influenced tube success for two of three species; affecting density-independent survival in one and density-dependent performance in the other. CONCLUSIONS: The diverse relations of pollen-tube success to pollen receipt evident among just nine species indicate significant contributions of the processes governing pollen germination and tube growth to the reproductive diversity of angiosperms.

Node-by-node disassembly of a mutualistic interaction web driven by species introductions.

Interaction webs summarize the diverse interactions among species in communities. The addition or loss of particular species and the alteration of key interactions can lead to the disassembly of the entire interaction web, although the nontrophic effects of species loss on interaction webs are poorly understood. We took advantage of ongoing invasions by a suite of exotic species to examine their impact in terms of the disassembly of an interaction web in Patagonia, Argentina. We found that the reduction of one species (a host of a keystone mistletoe species) resulted in diverse indirect effects that led to the disassembly of an interaction web through the loss of the mistletoe, two key seed-dispersers (a marsupial and a bird), and a pollinator (hummingbird). Our results demonstrate that the gains and losses of species are both consequences and drivers of global change that can lead to underappreciated cascading coextinctions through the disruption of mutualisms.

Hot spots of mutualistic networks.

Incorporating interactions into a biogeographical framework may serve to understand how interactions and the services they provide are distributed in space. We begin by simulating the spatiotemporal dynamics of realistic mutualistic networks inhabiting spatial networks of habitat patches. We proceed by comparing the predicted patterns with the empirical results of a set of pollination networks in isolated hills of the Argentinian Pampas. We first find that one needs to sample up to five times as much area to record interactions as would be needed to sample the same proportion of species. Secondly, we find that peripheral patches have fewer interactions and harbour less nested networks - therefore potentially less resilient communities - compared to central patches. Our results highlight the important role played by the structure of dispersal routes on the spatial distribution of community patterns. This may help to understand the formation of biodiversity hot spots.

Global growth and stability of agricultural yield decrease with pollinator dependence.

Human welfare depends on the amount and stability of agricultural production, as determined by crop yield and cultivated area. Yield increases asymptotically with the resources provided by farmers' inputs and environmentally sensitive ecosystem services. Declining yield growth with increased inputs prompts conversion of more land to cultivation, but at the risk of eroding ecosystem services. To explore the interdependence of agricultural production and its stability on ecosystem services, we present and test a general graphical model, based on Jensen's inequality, of yield-resource relations and consider implications for land conversion. For the case of animal pollination as a resource influencing crop yield, this model predicts that incomplete and variable pollen delivery reduces yield mean and stability (inverse of variability) more for crops with greater dependence on pollinators. Data collected by the Food and Agriculture Organization of the United Nations during 1961-2008 support these predictions. Specifically, crops with greater pollinator dependence had lower mean and stability in relative yield and yield growth, despite global yield increases for most crops. Lower yield growth was compensated by increased land cultivation to enhance production of pollinator-dependent crops. Area stability also decreased with pollinator dependence, as it correlated positively with yield stability among crops. These results reveal that pollen limitation hinders yield growth of pollinator-dependent crops, decreasing temporal stability of global agricultural production, while promoting compensatory land conversion to agriculture. Although we examined crop pollination, our model applies to other ecosystem services for which the benefits to human welfare decelerate as the maximum is approached.

Darwin's inflorescence syndrome is indeed associated with bee pollination.

KEY MESSAGE: A relationship between vertical acropetal inflorescences with protandrous flowers and bee pollination was hypothesized by Darwin back in 1877. Here we provide empirical evidence supporting this association across the angiosperms. Plant reproduction is not only determined by flower traits but also by the arrangement of flowers within inflorescences. Based on his observations of the orchid Spiranthes autumnalis, Darwin proposed in 1877 that bee-pollinated plants presenting protandrous flowers on vertical acropetal inflorescences, where proximal flowers open first, can exploit the stereotypical foraging behavior of their pollinators (i.e., upward movement through the inflorescence) to promote pollen exportation and reduce self-pollination. In these inflorescences, male-phase flowers lie spatially above female-phase flowers. To examine this untested hypothesis, we compiled literature information from 718 angiosperms species and evaluated the association between vertical acropetal inflorescences with protandrous flowers and bee pollination within a phylogenetic comparative framework. Results reveal that this type of inflorescence is indeed more common in species pollinated by bees. Moreover, this association does not seem to be weakened by the presence of alternative self-pollination avoidance mechanisms, like self-incompatibility, suggesting that this inflorescence type benefits mainly male rather than female fitness. Other inflorescence types placing male-phase flowers above female-phase flowers, e.g., vertical basipetal inflorescences with protogynous flowers, do not provide strong evidence of a differential association with pollination by bees. Female-biased nectar production in vertical acropetal inflorescences with protandrous flowers may reinforce the behavior of bees to fly upwards, rendering Darwin's configuration more adaptive than other inflorescence configurations.