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Bumble bees damage plant leaves and accelerate flower production when pollen is scarce

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Abstract

Bumble bee gardeners Bumble bees rely heavily on pollen resources for essential nutrients as they build their summer colonies. Therefore, we might expect that annual differences in the availability of these resources must simply be tolerated, but Pashalidou et al. made observations suggesting that bees may have strategies to cope with irregular seasonal flowering (see the Perspective by Chittka). When faced with a shortage of pollen, bumble bees actively damaged plant leaves in a characteristic way, and this behavior resulted in earlier flowering by as much as 30 days. Experimenters were not able to fully replicate the results with their own damage, suggesting that there is a distinct method that the bees use to stimulate earlier flowering. Science , this issue p. 881 ; see also p. 824
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... In addition, pollinators themselves may be able to induce the onset of flowering when faced with low availability of pollen resources and increase synchronisation of flowering time with pollinator presence (Pashalidou et al., 2020). Plant-pollinator temporal mismatches are of particular concern for highly specialized plant - (Takeno, 2016) . ...
... Although in that study the fumigation was performed when the plants were 4 weeks old, on average they were likely in an earlier stage in their life cycle than in the present study due to the observed conditions during their development. Earlier flowering onset is a common phenomenon when plants are under abiotic stresses, such as poor nutrition, drought, high salinity and high or low temperatures (Takeno, 2016) , but it can also be observed on plants exposed to biotic stresses, such as herbivory and damage caused by pollinators (Pashalidou et al., 2020;Pashalidou et al., 2013) . The plant-mediated effects of ozone on herbivory were less clear than those on flower visitation, but in the few situations where effects were observed, th ey were positive, meaning ozone increased herbivory in exposed plants. ...
Thesis
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Anthropogenic activities are causing air pollution. Amongst air pollutants, tropospheric ozone is a major threat to human health and ecosystem functioning. In this dissertation, I present three studies that aimed at increasing our knowledge on how plant exposure to ozone affects its reproduction and its interactions with insect herbivores and pollinators. For this purpose, a new fumigation system was built and placed in a greenhouse. The annual plant Sinapis arvensis (wild mustard) was used as the model plant. Plants were exposed to either 0 ppb (control) or 120 ppb of ozone, for variable amounts of time and at different points of their life cycle. After fumigation, plants were exposed to herbivores or pollinators in the greenhouse, or to both groups of insects in the field. My research shows that ozone affected reproductive performance differently, depending on the timing of exposure: plants exposed at earlier ages had their reproductive fitness increased, while plants exposed later in their life cycle showed a tendency for reduced reproductive fitness. Plant phenology was a key factor influencing reproductive fitness: ozone accelerated flowering and increased the number of flowers produced by plants exposed at early ages, while plants exposed to ozone at later ages tended to have fewer flowers. On the other hand, the ozone-mediated changes in plant-insect interactions had little impact on plant reproductive success. The strongest effect of ozone on plant-pollinator interactions was the change in the number of flower visits received per plant, which was strongly linked to the number of open flowers. This means that, as a rule, exposure of plants to ozone early in the life cycle resulted in a higher number of pollinator visits, while exposure later in the life cycle resulted in fewer flower visits by potential pollinators. An exception was observed: the higher number of visits performed by large syrphid flies to young ozone-exposed plants than to the respective control plants went beyond the increase in the number of open flowers in those plants. Also, honeybees spent more time per flower in plants exposed to ozone than on control plants, while other pollinators spent similar amounts of time in control and ozone-exposed plants. This guild-dependent preference for ozone-exposed plants may be due to species-specific preferences related to changes in the quality and quantity of floral rewards. In the field, ozone-exposed plants showed only a tendency for increased colonization by sucking herbivores and slightly more damage by chewing herbivores than control plants. On the other hand, in the greenhouse experiment, Pieris brassicae butterflies preferred control plants over ozone-exposed plants as oviposition sites. Eggs laid on ozone-exposed plants took longer to hatch, but the chances of survival were higher. Caterpillars performed better in control plants than in ozone-exposed plants, particularly when the temperature was high. Most of the described effects were dependent on the duration and timing of the ozone exposure and the observed temperature, with the strongest effects being observed for longer exposures and higher temperatures. Furthermore, the timing of exposure altered the direction of the effects. The expected climate change provides ideal conditions for further increases in tropospheric ozone concentrations, therefore for stronger effects on plants and plant-insect interactions. Acceleration of flowering caused by plant exposure to ozone may put plant-pollinator interactions at risk by promoting desynchronization between plant and pollinator activities. Reduced performance of caterpillars feeding on ozone-exposed plants may weaken herbivore populations. On the other hand, the increased plant reproduction that results from exposing young plants to ozone may be a source of good news in the field of horticulture, when similar results would be achieved in high-value crops. However, plant response to ozone is highly species-specific. In fact, Sinapis arvensis is considered a weed and the advantage conferred by ozone exposure may increase its competitiveness, with negative consequences for crops or plant communities in general. Overall, plant exposure to ozone might constitute a threat for the balance of natural and agro-ecosystems.
... Plants can recognize these HAMPs, inducing a defensive response different from that associated with simply mechanical damage [37,38]. In addition, a recent study showed that damage caused by bumble bees could promote the early flowering of plants, revealing a new interaction mode between pollinating insects and flowering plants and suggesting that bumble bees may secrete special signaling substances during the process of plant damage, to which plants respond by changing their flowering time to coordinate with bumble bees [39]. According to various evidence, therefore, we speculate that the reason for the decrease in operative strength of staminodes in response to nectar robbing was that nectar robbers might secrete a specific chemical signal during the process of stealing the nectar. ...
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Nectar-robbing insects, which are frequently described as cheaters in plant–pollinator mutualisms, may affect plant reproductive fitness by obtaining nectar rewards without providing pollination services. The negative effects of nectar robbing on plant reproductive success have been widely reported, but the reasons for possible positive effects demand further investigation. The goal of the study was to evaluate the effects of nectar robbing on the reproductive success of Delphinium caeruleum. Two staminodes cover the stamens and pistils in the flowers of D. caeruleum, forming a “double door” type of structure that compels pollinators to physically manipulate the staminodes to access the sex organs. In order to explore whether the operative strength required to open the staminodes is affected by actions associated with nectar robbing, we set up five different treatment groups: no nectar robbing, natural nectar robbing, artificial nectar robbing, hole making, and nectar removal. A biological tension sensor was used to measure the operative strength required to open the staminodes in the flowers. We also assessed the effect of nectar robbing on the flower-visiting behavior of pollinators and the effect of nectar robbing on reproductive fitness by the flower. The results showed that the operative strength needed to open staminodes was reduced by nectar robbers but not by artificial nectar robbing, hole making, or nectar removal. The flowers’ continuous visitation rate and visitation frequency by pollinators decreased significantly in robbed flowers. Both the pollen export and pollen deposition in naturally robbed flowers were significantly higher than those in nonrobbed flowers. Our results demonstrate that nectar robbers play an indirect positive role in the reproductive fitness of D. caeruleum flowers by reducing the operative strength of staminodes to promote pollen transfer. The reduction in operative strength of staminodes might be an adaptive mechanism that responds to nectar robbing.
... branching from same precursor, changing cellular environmental etc.), there must be a trade-off between pollinaton and defence against florivores [51][52][53] . This trade-off is further complicated by some pollinators turning against the plant on opportunity and some being florivores as larvae whereas pollinators as adults ( Fig.3) 54,55 . For instance, the caterpillar of Pieris brassicae feeds on Brassica nigra whereas the adults pollinates it. ...
Thesis
Angiosperms are the most widespread and diversified group of plants on Earth. They achieved such success during the Cretaceous radiation partly thanks to pollination of their flowers by insects. While attracting pollinating insects, the plant must repel predators and parasites. Some of these are florivore, flower eaters, that appear to be the former pollinators. Here I briefly present how this relationship might have led to the trade-off between pollination and defence against florivory. First, I introduce a brief history of how flowers and pollination evolved, with emphasis on its current consequences for interaction between flowers and insects. Secondly, I shortly illustrate how flower traits are used to attract pollinating insects. Thirdly, I summarise the plant defences against florivory. Finally, I discuss how angiosperms adapted to optimize the trade-offs between pollination and defence against florivory.
... Transcriptomic analyses can be used to detect differential gene expression associated with plant-arthropod interactions (e.g., plant-herbivore-pollinator interactions). For instance, treatments such as herbivory, pollination, herbivory + pollination, herbivory + predator/parasitoids + pollination treatments Schiestl, 2019, 2020;Pashalidou et al., 2020;Egan et al., 2021) may have illuminating effects. These may include differences in RNA expression between tissues and/or organs of interest (Koenig et al., 2013;Hekman et al., 2015), as well as during the tissues' and organs' development (Hradilová et al., 2017). ...
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Aboveground plant-arthropod interactions are typically complex, involving herbivores, predators, pollinators, and various other guilds that can strongly affect plant fitness, directly or indirectly, and individually, synergistically, or antagonistically. However, little is known about how ongoing natural selection by these interacting guilds shapes the evolution of plants, i.e., how they affect the differential survival and reproduction of genotypes due to differences in phenotypes in an environment. Recent technological advances, including next-generation sequencing, metabolomics, and gene-editing technologies along with traditional experimental approaches (e.g., quantitative genetics experiments), have enabled far more comprehensive exploration of the genes and traits involved in complex ecological interactions. Connecting different levels of biological organization (genes to communities) will enhance the understanding of evolutionary interactions in complex communities, but this requires a multidisciplinary approach. Here, we review traditional and modern methods and concepts, then highlight future avenues for studying the evolution of plant-arthropod interactions (e.g., plant-herbivore-pollinator interactions). Besides promoting a fundamental understanding of plant-associated arthropod communities' genetic background and evolution, such knowledge can also help address many current global environmental challenges.
... As with the E. huxleyi-P. inhibens metabolite/pathogen switch, which exhibits a symbiotic-to-pathogenic trigger under excess algal density and perhaps other environmental conditions, it has been shown that bumble bees damage plant leaves and accelerate flower production when pollen is scarce (Pashalidou et al., 2020). Many bees, including the western honey bee Apis mellifera, face harm by multiple pest and pathogen stressors, despite ineffective interventional strategies, which are short-term, expensive, or impractical. ...
Chapter
The olive fruit fly is considered a major threat for olive fruits and may cause damage to up to 100% of the harvested fruit. Olive fruit fly control falls under the generic topic of integrated pest management (IPM). Identifying the presence and the count of the olive fruit fly in time allows IPM to infer the best treatment strategy to be followed to prevent the pest from damaging the crop. This not only protects the crop yield but also increases the quality of the olive crop and, consequently, the quality of the resulting products, such as olive oil. In this chapter, we present a comprehensive survey of the literature of pest recognition technologies with emphasis on the detection and counting of the olive fruit fly using artificial intelligence techniques. We broadly classify existing pest recognition and counting techniques into manual, semiautomatic, and automatic detection and counting. We further categorize the automatic detection and counting based on the used technology into machine learning-based, deep learning-based, image processing-based, optoacoustic spectrum-based, and hyperspectral spectroscopy-based schemes.
... A recent study reveals that bumble bees bite flowering plants to induce rapid flowering, perhaps through chemical signals in their saliva. Remarkably, given their short life cycles these flowers will benefit only the next generation of bees (Pashalidou et al., 2020). Even more dramatic is Simard's (2021) research on transitive processes of resource circulation among and between tree species via the mediation of fungi in healthy forests. ...
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Sustainability is a wicked social problem, one difficult to solve because market capitalism inevitably produces ecological precarity. Consequently, marketing requires a paradigm shift. To address this problem, this research investigates a renewal of resource circulation theory and offers a glimpse of a sustainable neo-animist system. Neo-animist theory suggests new perspectives towards a more sustainable eco-economy of persons. Neo-animism foregrounds an alternative subjectivity to that inscribed in the modern social imaginary. Neo-animism is defined by the relationality of persons, the contingent extension of the principle of sociality to other living beings, and the recognition that all living beings are in communicative relations with significant others. Further, in a neo-animism framework resources circulate through transitive value co-creation processes, gifting, reciprocal exchange, and predation. Neo-animism provides an alternative to the dominant social exchange paradigm in marketing and addresses the challenges to sustainability identified in marketing and consumer research.
... Although in that study the fumigation was performed when the plants were 4 weeks old, on average they were likely in an earlier stage in their life cycle than in the present study due to the observed conditions during their development. Earlier flowering onset is a common phenomenon when plants are under abiotic stresses, such as poor nutrition, drought, high salinity and high or low temperatures 59 , but it can also be observed on plants exposed to biotic stresses, such as herbivory and damage caused by pollinators 60,61 . Together, our results suggest that compensatory stress responses of young wild mustard plants in the ozone treatment lead to higher investment in flower production, together with earlier flowering or extended flowering times. ...
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Exposure of plants to environmental stressors can modify their metabolism, interactions with other organisms and reproductive success. Tropospheric ozone is a source of plant stress. We investigated how an acute exposure to ozone at different times of plant development affects reproductive performance, as well as the flowering patterns and the interactions with pollinators and herbivores, of wild mustard plants. The number of open flowers was higher on plants exposed to ozone at earlier ages than on the respective controls, while plants exposed at later ages showed a tendency for decreased number of open flowers. The changes in the number of flowers provided a good explanation for the ozone-induced effects on reproductive performance and on pollinator visitation. Ozone exposure at earlier ages also led to either earlier or extended flowering periods. Moreover, ozone tended to increase herbivore abundance, with responses depending on herbivore taxa and the plant age at the time of ozone exposure. These results suggest that the effects of ozone exposure depend on the developmental stage of the plant, affecting the flowering patterns in different directions, with consequences for pollination and reproduction of annual crops and wild species.
... Nevertheless, according to a metaanalysis, on average, earlier flowering time is favored in most of the studied plant species (Munguía-Rosas et al., 2011). In turn, herbivore-induced changes in floral morphology and physiology can change the behavior of pollinators, as observed in Brassica nigra (Rusman et al., 2019), and even pollinators can force earlier flowering by chewing on leaves when there is a lack of pollen resources (Pashalidou et al., 2020). ...
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Insect pollinators such as bumblebees (Bombus spp.) are in global decline. A major cause of this decline is habitat loss due to agricultural intensification. A range of global and national initiatives aimed at restoring pollinator habitats and populations have been developed. However, the success of these initiatives depends critically upon understanding how landscape change affects key population-level parameters, such as survival between lifecycle stages, in target species. This knowledge is lacking for bumblebees, because of the difficulty of systematically finding and monitoring colonies in the wild. We used a combination of habitat manipulation, land-use and habitat surveys, molecular genetics and demographic and spatial modelling to analyse between-year survival of family lineages in field populations of three bumblebee species. Here we show that the survival of family lineages from the summer worker to the spring queen stage in the following year increases significantly with the proportion of high-value foraging habitat, including spring floral resources, within 250-1,000 m of the natal colony. This provides evidence for a positive impact of habitat quality on survival and persistence between successive colony cycle stages in bumblebee populations. These findings also support the idea that conservation interventions that increase floral resources at a landscape scale and throughout the season have positive effects on wild pollinators in agricultural landscapes.
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