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Buzz pollination, a type of interaction in which bees use vibrations to extract pollen from certain kinds of flowers, captures a close relationship between thousands of bee and plant species. In the last 120 years, studies of buzz pollination have contributed to our understanding of the natural history of buzz pollination, and basic properties of the vibrations produced by bees and applied to flowers in model systems. Yet, much remains to be done to establish its adaptive significance and the ecological and evolutionary dynamics of buzz pollination across diverse plant and bee systems. Here, we review for bees and plants the proximate (mechanism and ontogeny) and ultimate (adaptive significance and evolution) explanations for buzz pollination, focusing especially on integrating across these levels to synthesize and identify prominent gaps in our knowledge. Throughout, we highlight new technical and modelling approaches and the importance of considering morphology, biomechanics and behaviour in shaping our understanding of the adaptive significance of buzz pollination. We end by discussing the ecological context of buzz pollination and how a multilevel perspective can contribute to explain the proximate and evolutionary reasons for this ancient bee-plant interaction.
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Polinización , Vibración , Abejas , Animales , Polen , Flores , PlantasRESUMEN
A fundamental question in pollination ecology is how pollinators affect the evolution of different floral forms. Yet functional effects of shifts in floral form for plant and pollinator are frequently unclear. For instance, flowers that conceal pollen within tube-like anthers that are spread apart and move freely (free architecture) or are tightly joined together (joined architecture) have evolved independently across diverse plant families and are geographically widespread. Surprisingly, how their bee pollinators affect the function of both architectures remains unknown. We hypothesised that bee body size would affect foraging success and pollination differently for free and joined anther architectures. Therefore, we modified the anther architecture of a single plant species (Solanum elaeagnifolium) and used a single species of generalist bumble bee (Bombus impatiens), which varies greatly in body size. We found that on free anther architecture, larger bees were better pollinators. More pollen on their bodies was available for pollination and they deposited more pollen on stigmas. Conversely, on joined anther architecture, smaller bees were better pollinators. They collected less pollen into their pollen baskets, had more pollen on their bodies available for pollination, and deposited more pollen on stigmas. While we also found modest evidence that plants benefit more from joined versus free anther architecture, further investigation will likely reveal this also depends on pollinator traits. We discuss potential mechanisms by which pollinator size and anther architecture interact and implications for floral evolution.
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Polen , Polinización , Animales , Abejas , Tamaño Corporal , Ecología , FloresRESUMEN
How pollinators mediate microbiome assembly in the anthosphere is a major unresolved question of theoretical and applied importance in the face of anthropogenic disturbance. We addressed this question by linking visitation of diverse pollinator functional groups (bees, wasps, flies, butterflies, beetles, true bugs and other taxa) to the key properties of the floral microbiome (microbial α- and ß-diversity and microbial network) under agrochemical disturbance, using a field experiment of bactericide and fungicide treatments on cultivated strawberries that differ in flower abundance. Structural equation modelling was used to link agrochemical disturbance and flower abundance to pollinator visitation to floral microbiome properties. Our results revealed that (i) pollinator visitation influenced the α- and ß-diversity and network centrality of the floral microbiome, with different pollinator functional groups affecting different microbiome properties; (ii) flower abundance influenced the floral microbiome both directly by governing the source pool of microbes and indirectly by enhancing pollinator visitation; and (iii) agrochemical disturbance affected the floral microbiome primarily directly by fungicide, and less so indirectly via pollinator visitation. These findings improve the mechanistic understanding of floral microbiome assembly, and may be generalizable to many other plants that are visited by diverse insect pollinators in natural and managed ecosystems.
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Mariposas Diurnas , Polinización , Agroquímicos , Animales , Abejas , Ecosistema , FloresRESUMEN
Variation in pollinator quality is fundamental to the evolution of plant-pollinator mutualisms and such variation frequently results from differences in foraging behavior. Surprisingly, despite substantial intraindividual variation in pollinator foraging behavior, the consequences for pollen removal and deposition on flowers are largely unknown. We asked how two pollen foraging behaviors of a generalist pollinator (Bombus impatiens) affect removal and deposition of heterospecific and conspecific pollen, key aspects of pollinator quality, for multiple plant species. In addition, we examined how bee body size and pollen placement among body parts shaped pollen movement. We manipulated foraging behavior types using artificial flowers, which donated pollen that captive bees then deposited on three recipient plant species. While body size primarily affected donor pollen removal, foraging behavior primarily affected donor pollen deposition. How behavior affected donor pollen deposition depended on the plant species and the quantity of donor pollen on the bee's abdomen. Plant species with smaller stigmas received significantly less pollen and fewer bees successfully transferred pollen to them. For a single plant species, heterospecific pollen interfered with conspecific pollen deposition, such that more heterospecific pollen on the bee's abdomen resulted in less conspecific pollen deposition on the flower. Thus, intraindividual variation in foraging behavior and its interaction with the amount and placement of acquired pollen and with floral morphology can affect pollinator quality and may shape plant fitness via both conspecific and heterospecific pollen transfer.
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Polen , Polinización , Animales , Abejas , Flores , Plantas , SimbiosisRESUMEN
The flower is the hallmark of angiosperms and its evolution is key to their diversification. As knowledge of ecological interactions between flowers and their microbial communities (the anthosphere) expands, it becomes increasingly important to consider the evolutionary impacts of these associations and their potential eco-evolutionary dynamics. In this Viewpoint we synthesize current knowledge of the anthosphere within a multilevel selection framework and illustrate the potential for the extended floral phenotype (the phenotype expressed from the genes of the plant and its associated flower microbes) to evolve. We argue that flower microbes are an important, but understudied, axis of variation that shape floral trait evolution and angiosperm reproductive ecology. We highlight knowledge gaps and discuss approaches that are critical for gaining a deeper understanding of the role microbes play in mediating plant reproduction, ecology, and evolution.
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Bacterias/metabolismo , Evolución Biológica , Flores/fisiología , Modelos Biológicos , Fenotipo , Selección GenéticaRESUMEN
Sexual selection on male body size in species with a female-biased sexual size dimorphism is common yet often poorly understood. In particular, in the majority of bee species, the relative contribution of intrasexual competition and female choice to patterns of male body size is unknown. In this field study, we examined two possible components of male mating success with respect to body size in the solitary bee Diadasia rinconis Cockerell (Hymenoptera: Apidae): 1) ability to procure a mate and 2) the duration of copulation. We found that larger males were better able to procure mates and copulated for shorter periods of time. Although consistent with sperm competition theory, differences in copulation duration were slight; possibly, the shorter copulations of larger males instead reflect in copulo female choice. Consistent with this notion, males engaged in complex courtship while mounted, characterized for the first time in any bee in such detail via audio recordings and high-speed, high-definition video. The number of pulses in male courtship behavior was also positively associated with copulation duration and may have stimulated females to continue copulating, thereby potentially allowing smaller males to transfer a full ejaculate. Females were shown to be potentially polyandrous and although we did not observe precopulatory rejection in the field, captive females frequently rejected copulation attempts by captive males. Our work indicates that intrasexual competition selects for increased body size in a solitary bee.
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Abejas/fisiología , Conducta Sexual Animal , Animales , Arizona , Tamaño Corporal , Conducta Competitiva , Cortejo , MasculinoRESUMEN
Foraging behavior frequently plays a major role in driving the geographic distribution of animals. Buzzing to extract protein-rich pollen from flowers is a key foraging behavior used by bee species across at least 83 genera (these genera comprise â¼58% of all bee species). Although buzzing is widely recognized to affect the ecology and evolution of bees and flowering plants (e.g., buzz-pollinated flowers), global patterns and drivers of buzzing bee biogeography remain unexplored. Here, we investigate the global species distribution patterns within each bee family and how patterns and drivers differ with respect to buzzing bee species. We found that both distributional patterns and drivers of richness typically differed for buzzing species compared with hotspots for all bee species and when grouped by family. A major predictor of the distribution, but not species richness overall for buzzing members of four of the five major bee families included in analyses (Andrenidae, Halictidae, Colletidae, and to a lesser extent, Apidae), was the richness of poricidal flowering plant species, which depend on buzzing bees for pollination. Because poricidal plant richness was highest in areas with low wind and high aridity, we discuss how global hotspots of buzzing bee biodiversity are likely influenced by both biogeographic factors and plant host availability. Although we explored global patterns with state-level data, higher-resolution work is needed to explore local-level drivers of patterns. From a global perspective, buzz-pollinated plants clearly play a greater role in the ecology and evolution of buzzing bees than previously predicted.
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Polinización , Animales , Abejas/fisiología , Distribución Animal , Magnoliopsida/fisiología , Flores , BiodiversidadRESUMEN
One of the reasons why flowering plants became the most diverse group of land plants is their association with animals to reproduce. The earliest examples of this mutualism involved insects foraging for food from plants and, in the process, pollinating them. Vertebrates are latecomers to these mutualisms, but birds, in particular, present a wide variety of nectar-feeding clades that have adapted to solve similar challenges. Such challenges include surviving on small caloric rewards widely scattered across the landscape, matching their foraging strategy to nectar replenishment rate, and efficiently collecting this liquid food from well-protected chambers deep inside flowers. One particular set of convergent traits among plants and their bird pollinators has been especially well studied: the match between the shape and size of bird bills and ornithophilous flowers. Focusing on a highly specialized group, hummingbirds, we examine the expected benefits from bill-flower matching, with a strong focus on the benefits to the hummingbird and how to quantify them. Explanations for the coevolution of bill-flower matching include (1) that the evolution of traits by bird-pollinated plants, such as long and thin corollas, prevents less efficient pollinators (e.g., insects) from accessing the nectar and (2) that increased matching, as a result of reciprocal adaptation, benefits both the bird (nectar extraction efficiency) and the plant (pollen transfer). In addition to nectar-feeding, we discuss how interference and exploitative competition also play a significant role in the evolution and maintenance of trait matching. We present hummingbird-plant interactions as a model system to understand how trait matching evolves and how pollinator behavior can modify expectations based solely on morphological matching, and discuss the implications of this behavioral modulation for the maintenance of specialization. While this perspective piece directly concerns hummingbird-plant interactions, the implications are much broader. Functional trait matching is likely common in coevolutionary interactions (e.g., in predator-prey interactions), yet the physical mechanisms underlying trait matching are understudied and rarely quantified. We summarize existing methods and present novel approaches that can be used to quantify key benefits to interacting partners in a variety of ecological systems.
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Pico/anatomía & histología , Coevolución Biológica , Aves/anatomía & histología , Flores , Polinización , Animales , Flores/anatomía & histología , Néctar de las Plantas , PolenRESUMEN
In buzz-pollinated plants, bees apply thoracic vibrations to the flower, causing pollen release from anthers, often through apical pores. Bees grasp one or more anthers with their mandibles, and vibrations are transmitted to this focal anther(s), adjacent anthers, and the whole flower. Pollen release depends on anther vibration, and thus it should be affected by vibration transmission through flowers with distinct morphologies, as found among buzz-pollinated taxa. We compare vibration transmission between focal and non-focal anthers in four species with contrasting stamen architectures: Cyclamen persicum, Exacum affine, Solanum dulcamara and S. houstonii. We used a mechanical transducer to apply bee-like vibrations to focal anthers, measuring the vibration frequency and displacement amplitude at focal and non-focal anther tips simultaneously using high-speed video analysis (6000 frames per second). In flowers in which anthers are tightly arranged (C. persicum and S. dulcamara), vibrations in focal and non-focal anthers are indistinguishable in both frequency and displacement amplitude. In contrast, flowers with loosely arranged anthers (E. affine) including those with differentiated stamens (heterantherous S. houstonii), show the same frequency but higher displacement amplitude in non-focal anthers compared to focal anthers. We suggest that stamen architecture modulates vibration transmission, potentially affecting pollen release and bee behaviour.
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Mimicry is common in interspecies interactions, yet conditions maintaining Batesian mimicry have been primarily tested in predator-prey interactions. In pollination mutualisms, floral mimetic signals thought to dupe animals into pollinating unrewarding flowers are widespread (greater than 32 plant families). Yet whether animals learn to both correctly identify floral models and reject floral mimics and whether these responses are frequency-dependent is not well understood. We tested how learning affected the effectiveness and frequency-dependence of imperfect Batesian mimicry among flowers using the generalist bumblebee, Bombus impatiens, visiting Begonia odorata, a plant species exhibiting intersexual floral mimicry. Unrewarding female flowers are mimics of pollen-rewarding male flowers (models), though mimicry to the human eye is imperfect. Flower-naive bees exhibited a perceptual bias for mimics over models, but rapidly learned to avoid mimics. Surprisingly, altering the frequency of models and mimics only marginally shaped responses by naive bees and by bees experienced with the distribution and frequency of models and mimics. Our results provide evidence both of exploitation by the plant of signal detection trade-offs in bees and of resistance by the bees, via learning, to this exploitation. Critically, we provide experimental evidence that imperfect Batesian mimicry can be adaptive and, in contrast with expectations of signal detection theory, functions largely independently of the model and mimic frequency. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.
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Abejas/fisiología , Begoniaceae/anatomía & histología , Mimetismo Biológico , Flores/anatomía & histología , Polinización , Animales , AprendizajeRESUMEN
Pollen collection is necessary for bee survival and important for flowering plant reproduction, yet if and how pollen extraction motor routines are modified with experience is largely unknown. Here, we used an automated reward and monitoring system to evaluate modification in a common pollen-extraction routine, floral sonication. Through a series of laboratory experiments with the bumblebee, Bombus impatiens, we examined whether variation in sonication frequency and acceleration is due to instrumental learning based on rewards, a fixed behavioral response to rewards, and/or a mechanical constraint. We first investigated whether bees could learn to adjust their sonication frequency in response to pollen rewards given only for specified frequency ranges and found no evidence of instrumental learning. However, we found that absence versus receipt of a pollen reward did lead to a predictable behavioral response, which depended on bee size. Finally, we found some evidence of mechanical constraints, in that flower mass affected sonication acceleration (but not frequency) through an interaction with bee size. In general, larger bees showed more flexibility in sonication frequency and acceleration, potentially reflecting a size-based constraint on the range over which smaller bees can modify frequency and acceleration. Overall, our results show that although bees did not display instrumental learning of sonication frequency, their sonication motor routine is nevertheless flexible.
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Over 22,000 species of biotically pollinated flowering plants, including some major agricultural crops, depend primarily on bees capable of floral sonication for pollination services. The ability to sonicate ("buzz") flowers is widespread in bees but not ubiquitous. Despite the prevalence of this pollinator behavior and its importance to natural and agricultural systems, the evolutionary history of floral sonication in bees has not been previously studied. Here, we reconstruct the evolutionary history of floral sonication in bees by generating a time-calibrated phylogeny and reconstructing ancestral states for this pollen extraction behavior. We also test the hypothesis that the ability to sonicate flowers and thereby efficiently access pollen from a diverse assemblage of plant species, led to increased diversification among sonicating bee taxa. We find that floral sonication evolved on average 45 times within bees, possibly first during the Early Cretaceous (100-145 million years ago) in the common ancestor of bees. We find that sonicating lineages are significantly more species rich than nonsonicating sister lineages when comparing sister clades, but a probabilistic structured rate permutation on phylogenies approach failed to support the hypothesis that floral sonication is a key driver of bee diversification. This study provides the evolutionary framework needed to further study how floral sonication by bees may have facilitated the spread and common evolution of angiosperm species with poricidal floral morphology.
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Abejas/fisiología , Evolución Biológica , Polinización , Animales , Flores , SonicaciónRESUMEN
The ecological success of social insects is frequently ascribed to improvements in task performance due to division of labour amongst workers. While much research has focused on improvements associated with lifetime task specialization, members of colonies can specialize on a given task over shorter time periods. Eusocial bees in particular must collect pollen and nectar rewards to survive, but most workers appear to mix collection of both rewards over their lifetimes. We asked whether bumblebees specialize over timescales shorter than their lifetime. We also explored factors that govern such patterns, and asked whether reward specialists made more foraging bouts than generalists. In particular, we described antennal morphology and size of all foragers in a single colony and related these factors to each forager's complete foraging history, obtained using radio frequency identification (RFID). Only a small proportion of foragers were lifetime specialists; nevertheless, >50% of foragers specialized daily on a given reward. Contrary to expectations, daily and lifetime reward specialists were not better foragers (being neither larger nor making more bouts); larger bees with more antennal olfactory sensilla made more bouts, but were not more specialized. We discuss causes and functions of short and long-term patterns of specialization for bumblebee colonies.
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Abejas , Conducta Alimentaria , Néctar de las Plantas , Polen , Animales , Abejas/anatomía & histología , Abejas/fisiología , Abejas/ultraestructura , Dispositivo de Identificación por RadiofrecuenciaRESUMEN
The ability to forage and return home is essential to the success of bees as both foragers and pollinators. Pesticide exposure may cause behavioural changes that interfere with these processes, with consequences for colony persistence and delivery of pollination services.We investigated the impact of chronic exposure (5-43 days) to field-realistic levels of a neonicotinoid insecticide (2·4 ppb thiamethoxam) on foraging ability, homing success and colony size using radio frequency identification (RFID) technology in free-flying bumblebee colonies.Individual foragers from pesticide-exposed colonies carried out longer foraging bouts than untreated controls (68 vs. 55 min). Pesticide-exposed bees also brought back pollen less frequently than controls indicating reduced foraging performance.A higher proportion of bees from pesticide-exposed colonies returned when released 1 km from their nests; this is potentially related to increased orientation experience during longer foraging bouts. We measured no impact of pesticide exposure on homing ability for bees released from 2 km, or when data were analysed overall.Despite a trend for control colonies to produce more new workers earlier, we found no overall impacts of pesticide exposure on whole colony size. Synthesis and applications. This study shows that field-realistic neonicotinoid exposure can have impacts on both foraging ability and homing success of bumblebees, with implications for the success of bumblebee colonies in agricultural landscapes and their ability to deliver crucial pollination services. Pesticide risk assessments should include bee species other than honeybees and assess a range of behaviours to elucidate the impact of sublethal effects. This has relevance for reviews of neonicotinoid risk assessment and usage policy world-wide.