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Individual (a) and inflorescence (b) of Byrsonima variabilis containing flowers in different floral phases
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Pollinators search for multiple flora resources throughout their life cycle. Most studies, however, only assess how bees discriminate floral cues in the context of nectar foraging. In the present study, we sought to elucidate whether oil-collecting bees discriminate flowers of Byrsonima variabilis (Malpighiaceae) with petals of different colours wh...
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The large carpenter bees are the important pollinators and vital component of the mellitofauna. They are cosmopolitan, common in subtropical , tropical and thin in temperate and cold arid conditions. The large carpenter bees of Jammu & Kashmir and Ladakh region includes Xylocopa valga, X. dejeanii, X. fenestrata and X. pubesence. The species presid...
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... Close-range visual distinction directs bees to flowers with rewards guiding them away from empty flowers (Schaal and Leverich 1980;Lamont 1985;Gori 1989;Weiss 1991). Solitary oil-collecting Centris bees (Apidae), for instance, use the yellow standard-petal before its color changes to orange and red as a pollen guide when they search for pollen resources in oil-producing flowers of Byrsonima variabilis (Malpighiaceae) (Melo et al. 2018). The yellow pollen on dehisced anthers of C. elegans probably implies reward recognition, as bees have an innate preference for yellow pollen (Osche 1979;Lunau and Maier 1995;Lunau et al. 2024). ...
In specialized plant-pollinator associations, partners may exhibit adaptive traits, which favor the maintenance of the interaction. The association between Calibrachoa elegans (Solanaceae) and its oligolectic bee pollinator, Hexantheda missionica (Colletidae), is mutualistic and forms a narrowly specialized pollination system. Flowers of C. elegans are pollinated exclusively by this bee species, and the bees restrict their pollen resources to this plant species. The pollen presentation schedules of C. elegans were evaluated at the population level to test the hypothesis that H. missionica females adjust their foraging behavior to the resource offering regime of C. elegans plants. For this, the number of new flowers and anthers opened per hour (as a proxy for pollen offering) was determined, and pollen advertisement was correlated with the frequency of flower visits during the day. Preferences of female bees for flowers of different stages were also investigated, and their efficiency as pollinators was evaluated. Pollen offering by C. elegans was found to be partitioned throughout the day through scattered flower openings. Females of H. missionica indeed adjusted their foraging activity to the most profitable periods of pollen availability. The females preferred new, pollen-rich flowers over old ones and gathered pollen and nectar selectively according to flower age. Such behaviors must optimize female bee foraging efficiency on flowers. Female bees set 93% of fruit after a single visit. These findings guarantee their importance as pollinators and the persistence of the specialized plant-pollinator association.
... Individuals lacking oil glands or with a reduced number of them are thought to allocate more resources to pollen production (Teixeira and Machado 2000). However, oil-collecting bees can collect pollen from both glandular and eglandular flowers (Teixeira and Machado 2000;Schäffler et al. 2012;Melo et al. 2018), which may also be visited by non-oil-collecting bees for pollen. Thus, plants that offer only pollen as a reward (eglandular individuals) could face reproductive uncertainties as all visits to flowers would be concentrated on pollen collection, causing reductions in pollen delivery. ...
... Floral cues involved in floral oil-mediated plantpollinator interactions have been investigated only for a few species Steiner et al. 2011;Schäffler et al. 2012Schäffler et al. , 2015Melo et al. 2018;Castañeda-Zárate et al. 2021). These studies have demonstrated that both visual and olfactory signals are important in locating floral oil-producing flowers for both pollen and oil, and these signals are likely to be subjected to pollinator-mediated selection Schäffler et al. 2012). ...
... For instance, in Byrsonima variabilis A. Juss. (Malpighiaceae), visual cues may indicate the availability of pollen only and be interpreted as a foraging filter, leading bees to approach flowers (Melo et al. 2018). However, recognition of resources can also be signalled by floral scents (Milet-Pinheiro et al. 2015). ...
... No trabalho realizado por Mendes et al. (2011) [35], os autores sugerem que o comportamento de mudança nas cores das peças florais pode ser um indicativo de uma adaptação das espécies vegetais como meio de comunicação para os seus visitantes, permitindo que as visitas sejam redirecionadas a outras flores ricas em grãos de pólen, o que provavelmente contribui para as abelhas evitarem um gasto energético desnecessário, conforme também assinalam Melo et al. (2018) [36]. Conforme ressaltam Deprá e Gaglianone (2018) [37], em uma população, os indivíduos diferem entre si em vários aspectos que resultam na floração em momentos diferentes. ...
... No trabalho realizado por Mendes et al. (2011) [35], os autores sugerem que o comportamento de mudança nas cores das peças florais pode ser um indicativo de uma adaptação das espécies vegetais como meio de comunicação para os seus visitantes, permitindo que as visitas sejam redirecionadas a outras flores ricas em grãos de pólen, o que provavelmente contribui para as abelhas evitarem um gasto energético desnecessário, conforme também assinalam Melo et al. (2018) [36]. Conforme ressaltam Deprá e Gaglianone (2018) [37], em uma população, os indivíduos diferem entre si em vários aspectos que resultam na floração em momentos diferentes. ...
Estudos fenológicos e de biologia floral são importantes para o entendimento da dinâmica dos eventos biológicos que ocorrem entre as espécies vegetais ao longo do tempo. O presente estudo foi realizado visando identificar padrões fenológicos, florais e eficiência de polinizadores de espécies de Byrsonima Rich. ex Kunth em área remanescente de vegetação de caatinga na Bahia, Brasil. Vinte espécimes de três espécies de Byrsonima spp. foram marcados e acompanhados diariamente durante o período de floração, entre novembro de 2017 a abril de 2018. As populações das espécies estudadas apresentaram padrão de floração anual e duração intermediária com 40% das flores abertas por inflorescência/dia expressando a estratégia cornucópia. A sincronia foi interespecífica com distintos picos de floração com maior sincronia entre B. gardneriana e B. verbascifolia. Das variáveis climáticas, a umidade e a temperatura mostraram correlação forte com a atividade de floração. Na coleta de grãos de pólen, verificou-se uma redução significativa no quantitativo de grãos forrageado entre a primeira e a segunda visita. A biologia floral foi similar entre as espécies, além de produzirem quantidade satisfatória de pólen e alta viabilidade polínica, com destaque para B. verbascifolia. As espécies ofertam óleo e grãos de pólen como recompensa floral. As espécies de Byrsonima spp. estudadas nessa região de caatinga são potencialmente férteis e capacitadas a serem empregadas em programas de reflorestamento e melhoramento genético.
... A diverse array of floral colors can be found in oil systems. Color changes are common over the anthesis of many floral oil-producing species (see Bezerra 2008;Carneiro et al. 2015;de Melo et al. 2018). In some of them, the corolla displays colored guides used as an orientation cue like the translucent 'window' at the upper lip of Diascia flowers (Steiner 1990). ...
... In some Malpighiaceae, the "flag" petal exhibits a different color pattern-in addition to its divergent morphology-compared to the other petals of the same flower, and has been recognized as a structure that works in pollinator orientation (Vogel 1974). In Byrsonima variabilis (Malpighiaceae), for instance, the "flag" petal has been demonstrated to function as an honest signal for pollen collection only, and color change during anthesis is a visual cue for pollinators to avoid visiting pollen-depleted flowers (de Melo et al. 2018). There is still no evidence that visual cues like 'floral oil guides' can be used by the bees as an indication of floral oil quantity and quality. ...
Fifty years have passed since the first descriptions of the “floral oil syndrome” by Stefan Vogel. Over those past decades, substantial knowledge was obtained mainly on the taxonomic distribution, morphologies and phylogenetics involved in floral oil-mediated interactions. Many studies have also extended the understanding of several ecological and evolutionary aspects of these interactions over the last two decades, mainly in neotropical environments, where oil bee–oil flower interactions are more diverse and abundant. Although researchers worldwide have been inspired by Vogel’s work, the Brazilian research on oil-collecting bees and oil-secreting plants has particularly played a crucial role for this expansion. Here, we review the findings on floral oil systems and organize them in an illustrative timeline, containing a representative picture of important studies since Vogel’s first discoveries. We summarize not only the structural biology and taxonomic groups involved, but also the ecological, evolutionary and conservation aspects addressed to date. In addition, we indicate future directions for a broader understanding of these interactions.
... Many studies have been carried out on the species of the Malpighiaceae family, since it is arguably the oldest lineage to have acquired oil glands (Renner and Schaefer 2010), and most neotropical species have elaiophores. These studies focused on plant-pollinator interaction (Sazima and Sazima 1989;Simpson 1989;Aguiar 2003;de Melo et al. 2018; among many others) and reproductive biology (Barros 1992;Sigrist and Sazima 2004;Costa et al. 2006;Cappellari et al. 2011;Avalos et al. 2021), but only a few approached the floral morphology and anatomy of fertile cycles (Possobom et al. 2016;Aliscioni et al. 2018Aliscioni et al. , 2019Arévalos-Rodriguez et al. 2020;Avalos et al. 2020), the tritrophic interactions among plant-pollinator-ants (Assunção et al. 2014) and the quantitative and qualitative composition of floral resources and pollinator abundance throughout the flowering phenology (Barônio et al. 2017). ...
The species of the family Malpighiaceae are mainly diversified in the Neotropical Region as a consequence of a specialized pollination system. Due to the production of floral oils as a reward to pollinators, and their interaction with Centris, Epicharis (Centridini) and Monoeca (Tapinotaspidini) oil-collecting bee species in most neotropical species, many studies were focused on this interesting mutualistic interaction. However, a few have approached the reproductive biology of these species. The aim of this study was to gather all the existing information to date on the reproductive biology, megagametophyte development and apomixis of the Malpighiaceae species and analyze it together. We found 39 studies on the reproductive biology of 66 species, of which 47% are self-compatible, 33.3% self-incompatible, 18.2% have a mixed system, showing variable behavior among populations and 1.5% agamospermic species. We also found studies/reports on apomixis for eight species (three genera), polyembryony for six species (five genera) and on the development of megagametophyte for 14 species. We showed that our knowledge about the reproductive biology of Malpighiaceae species is scarce and fragmented, obtaining data for only 70-80 species (6-7% out of the total), most of which belonged to one population and/or few analyzed individuals. Further studies about the integral reproductive biology of these species that focus on the analysis of inter-population variations of the reproductive characters should be carried out to better understand how certain reproductive traits of Mal-pighiaceae species might have evolved and to provide valuable information on the mechanisms of population differentiation.
... This phenomenon has been found in over 70 families of plants (Weiss 1995). Byrsonima variabilis (Malpighiaceae), for instance, changes standard petal color during anthesis from yellow to orange and finally red, and bees preferentially visit flowers with yellow standard petals when foraging for pollen (de Melo et al. 2018). The retention of old flowers increases display size and, by doing so, increases attraction of pollinators (Ishii & Sakai 2001). ...
Diversity and distribution of flower coloration is a puzzling topic that has been extensively studied, with multiple hypotheses being proposed to account for the functions of coloration, such as pollinator attraction, protection against herbivory, and prevention of damage by ultraviolet light. Recent methodologies have allowed studies to consider the visual system of animals other than humans, helping to answer questions regarding the distribution of flower coloration. A survey of keywords in Web of Science shows floral color to be mainly studied in relation to macroevolutionary traits and biochemistry of pigments, focusing on pollination and anthocyanins, respectively. The present paper reviews mechanisms that determine the color of flowers. First, it is discussed how pigment, visual systems and signaling environments influence flower color; secondly, patterns of convergent evolution of flower color is debated, including evolutionary history, pollinator preference, flower color change, flowering season, and habitat. Third and last, patterns of flower coloration that have been found around the globe are addressed. In short, the aim is to contribute to ongoing research, by underlining mechanisms that lead to global patterns of coloration and indicating perspectives for future study on the topic.
Keywords:
floral color; flower coloration; color vision; pollination ecology; sensory drive; flower color change; pollinator preference; color preference; flowering season
... We observed that T. spinipes and A. mellifera preferred to visit orange and yellow flowers. Results for Byrsonima variabilis (Malpighiaceae) were similar to ours, in which large and small bees showed greater preference for orange and yellow flowers during the collection of floral resources (pollen and nectar) [24]. ...
... Bees do not have a red-light receptor in the 700 nm band because their vision is restricted to short wavelengths between UV (300 nm) and orange (690 nm), while red and infrared (IR) are in a spectral range above 700 nm [36], explaining the low bee visits in these flowers. Thus, the green fluorescence color emitted by red T. majus flowers resembles green foliage dispersed in the environment, as leaves also present a chlorophyll compound with green fluorescence emission [19,24,56]; therefore, red corolla flowers were not in evidence, explaining the low bee visit abundances in orange-red, yellow-red, and especially red flowers, which had higher emissions. It is noteworthy that the odor exhaled by T. majus stamens attracts pollinators, serving as a cue to find these unattractive flowers [25]. ...
... They also prove that bees visit fewer red flowers due to their higher emissions (above 700 nm) and high chlorophyll fluorescence index in this band. Furthermore, our outcomes suggest that flower fluorescence pattern is an important signal in flower recognition by visiting bees [15,16,24,61]; therefore, our findings raise new possibilities in the perception of floral visitors since fluorescence was not considered important in attracting bees to different T. majus flowers. ...
Tropaeolum majus L. species produce flowers with all sorts of colors, from yellow to red. This work aimed to apply optical fluorescence spectroscopy to study bee abundance in T. majus, answering the following questions: (1) do corolla temperature and weather conditions affect the abundance of visiting bee species? (2) do flower color and corolla fluorescence affect the abundance of visiting bee species? (3) do red flowers attract more visiting bees? (4) is there a relationship between bee visits and flower compounds? The bee species Apis mellifera, Paratrigona lineata, and Trigona spinipes were the most observed in T. majus flowers. The latter was more active in the morning and preferred orange and yellow flowers. These colors also had higher temperatures and fluorescence emissions than did the red ones and those with yellow-red and orange-red nectar guides. Orange flowers emitted a broadband UV spectrum (between 475 and 800 nm). This range might be due to compounds such as hydroxycinnamic acid, flavonols, isoflavonoids, flavones, phenolic acid, and chlorophyll. Extracts from different T. majus corolla colors showed that flowers emit specific fluorescent signals, mainly related to bee color vision and learning, thus acting as a means of communication between bees and flowers. In this way, this information evidences the interaction between bees and T. majus flowers, allowing conservation actions for pollinators.
... Additionally, this floral UV category could be related with resource signalling, since yellow and UVabsorbing pollen and anthers (or mimics) trigger behavioural responses in bees and flies (Lunau et al., 2017 and references therein). Interestingly, oil-collecting bees are sensitive to floral visual changes (Ferreira and Torezan-Silingardi, 2013;Melo et al., 2018) and half of the Malpighiaceae species (mainly having oil as resource) show UV-absorbing reproductive structures (CR), a pattern usually associated with pollen-flowers . ...
Despite the wide interest in flower colours, only after the end of the nineteenth-century studies started to comprise floral UV reflection, which is invisible to humans but visible to the major groups of pollinators. Many flowers and inflorescences display colour patterns, an important signal for pollinators, promoted by the presence of at least two different colours within flowers or inflorescences, including colours in the UV waveband. For Neotropical savanna plant species, we characterised floral UV features using UV-photography and reflectance measurements. We tested (i) whether floral UV features were constrained by their shared ancestry, (ii) whether floral UV features were associated with pollinators, and (iii) whether floral UV features were associated with floral traits mediating these interactions, including floral resource, type of attraction unit and presence/absence of non-UV colour patterns. Of 80 plant species, ca. 70% were UV-patternless, most of them UV-absorbing. Approximately 30% presented one of three types of UV-patterns: bullseye, contrasting corolla markings oriented toward floral resources or contrasting reproductive structures, which were all considered as floral guides. Floral UV features were phylogenetically constrained and were associated with pollinators, floral resources and attraction unit, but not with non-UV colour patterns. UV-patternless flowers were associated with most of the pollination systems, while UV-patterned flowers were mainly associated with bee-pollination. UV-absorbing flowers comprised the only category with hawkmoth- and butterfly-pollinated flowers, and a high percentage of hummingbird-pollinated species. Nocturnal pollinated species were also commonly UV-absorbing, except for one UV-reflecting bat-pollinated species and one beetle-pollinated species with UV-reflecting stigmas. All types of floral UV features were associated with nectar; however, flowers with contrasting reproductive structures were mainly associated with pollen. There was an association between UV-absorbing species and the presence of inflorescences and intermediate attraction units. Our results evince that phylogenetic relatedness can constraint floral UV features’ diversification, but combinations of evolutionary and ecological processes may be expected in this scenario.
... Females of Pseudagapostemon fluminensis avoid old pollen-empty flowers, given that only 3% of their flower visits were made to these flowers. This implies that they are able to discriminate old from recently opened flowers, probably by visual (Wittmann et al., 1990;de Melo et al., 2018) and/or olfactory (Milet-Pinheiro et al., 2012, 2013 cues. For visual cues these bees may rely on differences in reflectance intensity, as was found in the spectrophotometric analysis presented here, and/or the presence/absence of blue anthers in newly opened vs. old flowers of Petunia mantiqueirensis, respectively. ...
Details of the foraging patterns of solitary bees are much less well known than those of social species, and these patterns are often adjusted to exploit floral resources of one or only a few species. The specialized flower-visiting bees of Petunia are good models for investigating such foraging patterns. Here we analysed the floral biology and pollen presentation schedule of the endangered Petunia mantiqueirensis in mixed Araucaria forests of Serra da Mantiqueira, Brazil. Pollinators and their pollen foraging behaviour and food specialization were determined through analyses of scopa pollen loads. Flowers opened throughout the day and presented all their pollen resources within the first 30 min of anthesis, thus providing their pollen resources in an asynchronous fashion in one-flower packages throughout the day. Females of Pseudagapostemon fluminensis were the most frequent flower visitors, contacting stigmas in 96% of their visits, and were the unique effective pollinators of Petunia mantiqueirensis. These pollinators were responsible for the first three visits to 115 individually monitored flowers at any daylight hour, removing ~86% of a flower’s total pollen supply during the first visit. Although female bees harvest the majority of pollen resources of Petunia mantiqueirensis, analyses of scopa loads revealed that most of them also collect pollen from plants of other families while foraging for pollen in Petunia flowers.
... In our experiment we chose stimuli that would be relatively difficult for bees to discriminate, to both be ecologically realistic (in natural foraging scenarios bees often need to discriminate between stimuli this similar in colour e.g. 89 ), and to maximize the chances that we would detect an effect on learning if it existed in this context. We also replicated the experiment across two different scenarios where the motivational value of the US changed, as well as the opportunity to learn. ...
Neonicotinoids are widely-used pesticides implicated in the decline of bees, known to have sub-lethal effects on bees’ foraging and colony performance. One proposed mechanism for these negative effects is impairment to bees’ ability to learn floral associations. However, the effects of neonicotinoids on learning performance have largely been addressed using a single protocol, where immobilized bees learn an association based on a single sensory modality. We thus have an incomplete understanding of how these pesticides affect bee learning in more naturalistic foraging scenarios. We carried out the first free-foraging study into the effects of acute exposure of a neonicotinoid (imidacloprid) on bumblebees’ (Bombus impatiens) ability to learn associations with visual stimuli. We uncovered dose-dependent detrimental effects on motivation to initiate foraging, amount of nectar collected, and initiation of subsequent foraging bouts. However, we did not find any impairment to bees’ ability to learn visual associations. While not precluding the possibility that other forms of learning are impaired, our findings suggest that some of the major effects of acute neonicotinoid exposure on foraging performance may be due to motivational and/or sensory impairments. In light of these findings, we discuss more broadly how pesticide effects on pollinator cognition might be studied.
