Floral chemistry mediates plant interactions with pollinators, pathogens, and herbivores, with major consequences for fitness of both plants and flower visitors. The outcome of such interactions often depends on compound dose and chemical context. However, chemical diversity and intraspecific variation of nectar and pollen secondary chemistry are known for very few species, precluding general statements about their composition. We analyzed methanol extracts of flowers, nectar, and pollen from 31 cultivated and wild plant species, including multiple sites and cultivars, by liquid‐chromatography–mass‐spectrometry. To depict the chemical niche of each tissue type, we analyzed differences in nectar and pollen chemical richness, absolute and proportional concentrations, and intraspecific variability. We hypothesized that pollen would have higher concentrations and more compounds than nectar, consistent with Optimal Defense Theory and pollen's importance as a male gamete. To investigate chemical correlations across and within tissues, which could reflect physiological constraints, we quantified chemical overlap between conspecific nectar and pollen, and phenotypic integration of individual compounds within tissue types. Nectar and pollen were chemically differentiated both across and within species. Of 102 compounds identified, most occurred in only one species. Machine‐learning algorithms assigned samples to the correct species and tissue type with 98.6% accuracy. Consistent with our hypothesis, pollen had 23.8‐ to 235‐fold higher secondary chemical concentrations and 63% higher chemical richness than nectar. The most common secondary compound classes were flavonoids, alkaloids, terpenoids, and phenolics (primarily phenylpropanoids including chlorogenic acid). The most common specific compound types were quercetin and kaempferol glycosides, known to mediate biotic and abiotic effects. Pollens were distinguished from nectar by high concentrations of hydroxycinnamoyl‐spermidine conjugates, which affect plant development, abiotic stress tolerance, and herbivore resistance. Although chemistry was qualitatively consistent within species and tissue types, concentrations varied across cultivars and sites, which could influence pollination, herbivory, and disease in wild and agricultural plants. Analyses of multivariate trait space showed greater overlap across sites and cultivars in nectar than pollen chemistry; this overlap reflected greater within‐site and within‐cultivar variability of nectar. Our analyses suggest different ecological roles of nectar and pollen mediated by chemical concentration, composition, and variability.
Summary 1.Invasive species are considered a main driver of pollinator declines, yet the direct effects of invasive alien plants on pollinators are poorly understood. 2. Abundant, invasive plant species can provide a copious nectar resource for native pollinators. However, the nectar of some plants contains secondary compounds, usually associated with defence against herbivores. The impacts of these compounds on pollinators are often unknown. 3. We compared how consumption of grayanotoxin I and III, natural secondary compounds in the nectar of invasive Rhododendron ponticum L., affected three native bee species: a honeybee, (Apis mellifera L.), a solitary mining bee (Andrena carantonica, P erez) and a bumblebee, (Bombus terrestris, L.). 4. Survival of the solitary bee and the bumblebee species was not affected by either grayanotoxin, but honeybees were $ 209 more likely to die when fed solutions containing grayanotoxin I. Furthermore, solitary bees were deterred from feeding and exhibited malaise behaviours indicative of sublethal toxicity in response to consumption of grayanotoxin I. In contrast, grayanotoxins did not affect bumblebee survival or behaviour, even when bees were subjected to multiple stressors (parasite infection or food stress). 5. Our experiments suggest that while R. ponticum provides abundant floral nectar, it is only available as a food resource to pollinators that tolerate grayanotoxins. Pollinators whose health is negatively affected by grayanotoxins may experience negative impacts from R. ponticum invasion directly (if they consume R. ponticum nectar) or indirectly (if native floral resources are replaced by R. ponticum). 6. Our study makes a novel comparison of the effects of a natural nectar secondary compound on three pollinator species and clearly demonstrates drastic variation in the responses of different key pollinator taxa to a nectar toxin. Our findings are thus in congruence with literature demonstrating the varying effects of invasive plant chemistry on native foliar herbivores, and our work demonstrates that nectar chemistry should be taken into account when determining the impacts of plant invasion for native pollinators.
The need to reduce pollinator exposure to harmful pesticides has led to calls to expedite adoption of integrated pest management (IPM). We make the case that IPM is not explicitly 'pollinator-friendly', but rather must be adapted to reduce impacts on pollinators, and to facilitate synergies between crop pollination and pest control. To reconcile these diverse management needs, we introduce a systematic framework for 'integrated pest and pollinator management' (IPPM). We also highlight novel tools to unify monitoring and economic decision making processes for IPPM, and outline key policy actions and knowledge gaps. We propose that IPPM is needed to promote more coordinated ecosystem-based strategies for sustainable food production, against the backdrop of increasing pesticide regulation and pollinator dependency in agriculture.
Biological control, or biocontrol, is the exploitation of living agents (incl. viruses) to combat pestilential organisms (incl. pathogens, pests, and weeds) for diverse purposes to provide human benefits. Thus, during the last century the practices and concepts involved have evolved in separate streams associated with distinct scientific and taxonomic disciplines. In parallel developments, there have been increasing references to biological control in industrial contexts and legislation, resulting in conceptual and terminological disintegration. The aim of this paper is to provide a global conceptual and terminological platform that facilitates future development of the field. We review use of previously suggested terms in key fields (e.g., phytopathology, entomology, and weed science), eliminate redundant terminology, identify three principles that should underpin the concept, and then present a new framework for biological control, rooted in seminal publications. The three principles establish that (1) only living agents can mediate biological control, (2) biological control always targets a pest, directly or indirectly, and (3) all biocontrol methods can be classified in four main categories depending on whether resident agents are utilized, with or without targeted human intervention (conservation biological control and natural biological control, respectively) or agents are added for permanent or temporary establishment (classical biological control and augmentative biological control, respectively). Correct identification of what is, and is not, biological control can help efforts to understand and optimize biological pest control for human and environmental benefits. The new conceptual framework may contribute to more uniform and appropriate regulatory approaches to biological control, and more efficient authorization and application of biocontrol products.
Summary Secondary compounds in nectar can function as toxic chemical defences against floral antagonists, but may also mediate plant–pollinator interactions. Despite their ecological importance, few studies have investigated patterns of spatial variation in toxic nectar compounds in plant species, and none outside their native range. Grayanotoxin I (GTX I) occurs in nectar of invasive Rhododendron ponticum where it is toxic to honeybees and some solitary bee species. We examined (i) geographic variation in the composition of nectar GTX I, as well as GTX III (which is not toxic to these species), in the native and introduced range of R. ponticum, (ii) how their expression is structured at patch and landscape scales within ranges, and (iii) whether climatic and environmental factors underpin spatial patterns. While both GTXs varied within ranges, variation in GTX I, but not GTX III, was detected between ranges. GTX I expression was thus markedly lower or (in 18% of cases) absent from nectar in introduced plants. Spatial autocorrelation was apparent at both patch and landscape scales and in part related to heat load interception by plants (a function of latitude, aspect and slope). As expression of nectar GTXs was generally robust to environmental variation, and aggregated in space, this trait has the potential to be spatially discriminated by consumers. Given the specificity of change to GTX I, and its differential toxicity to some bee species, we conclude that its expression was likely to have been influenced during invasion by interaction with herbivores/consumers, either via pollinator‐mediated selection or enemy release from floral antagonists. Synthesis. As the first demonstration of large‐scale geographic variation and spatial structure in toxic nectar compounds, this work deepens our understanding of the chemical ecology of floral interactions in native and introduced species. Spatially explicit studies of nectar secondary compounds are thus required to show how the extent and structure of spatial variation may affect floral ecology. Future development of invasion theory should incorporate a holistic view of plant defence, beyond antagonistic interactions, which integrates the consequences of chemically defended mutualist rewards.
The global decline in pollinators has partly been blamed on pesticides, leading some to propose pesticide-free farming as an option to improve pollination. However, herbivores are likely to be more prevalent in pesticide-free environments, requiring knowledge of their effects on pollinators, and alternative crop protection strategies to mitigate any potential pollination reduction. Strawberry leaf beetles (SLB) Galerucella spp. are important strawberry pests in Northern Europe and Russia. Given that SLB attack both leaf and flower tissue, we hypothesized pollinators would discriminate against SLB-damaged strawberry plants (Fragaria vesca, cultivar ‘Rügen’), leading to lower pollination success and yield. In addition we screened the most common commercial cultivar ‘Rügen’ and wild Swedish F. vesca genotypes for SLB resistance to assess the potential for inverse breeding to restore high SLB resistance in cultivated strawberry. Behavioral observations in a controlled experiment revealed that the local pollinator fauna avoided strawberry flowers with SLB-damaged petals. Low pollination, in turn, resulted in smaller more deformed fruits. Furthermore, SLB-damaged flowers produced smaller fruits even when they were hand pollinated, showing herbivore damage also had direct effects on yield, independent of indirect effects on pollination. We found variable resistance in wild woodland strawberry to SLB and more resistant plant genotypes than the cultivar ‘Rügen’ were identified. Efficient integrated pest management strategies should be employed to mitigate both direct and indirect effects of herbivory for cultivated strawberry, including high intrinsic plant resistance.
Crop domestication can lead to weakened expression of plant defences, with repercussions for herbivore and pathogen susceptibility. However, little is known about how domestication alters traits that mediate other important ecological interactions in crops, such as pollination. Secondary metabolites, which underpin many defence responses in plants, also occur widely in nectar and pollen and influence plant-pollinator interactions. Thus, domestication may also affect secondary compounds in floral rewards, with potential consequences for pollinators. To test this hypothesis, we chemically analysed nectar and pollen from wild and cultivated plants of highbush blueberry (Vaccinium corymbosum L.), before conducting an artificial diet bioassay to examine pollinator-pathogen interactions. Our results indicated that domestication has significantly altered the chemical composition of V. corymbosum nectar and pollen, and reduced pollen chemical diversity in cultivated plants. Of 20 plant metabolites identified in floral rewards, 13 differed significantly between wild and cultivated plants, with a majority showing positive associations with wild compared to cultivated plants. These included the amino acid phenylalanine (4.5 times higher in wild nectar, 11 times higher in wild pollen), a known bee phagostimulant and essential nutrient; and the antimicrobial caffeic acid ester 4-O-caffeoylshikimic acid (two times higher in wild nectar). We assessed the possible biological relevance of variation in caffeic acid esters in bioassays, using the commercially available 3-O-caffeoylquinic acid. This compound reduced Bombus impatiens infection by a prominent gut pathogen (Crithidia) at concentrations that occurred in wild but not cultivated plants, suggesting that domestication may influence floral traits with consequences for bee health. Appreciable levels of genetic variation and heritability were found for most floral reward chemical traits, indicating good potential for selective breeding. Our study provides the first assessment of plant domestication effects on floral reward chemistry and its potential repercussions for pollinator health. Given the central importance of pollinators for agriculture, we discuss the need to extend such investigations to pollinator-dependent crops more generally and elaborate on future research directions to ascertain wider trends, consequences for pollinators, mechanisms, and breeding solutions.
Species of the carnivorous genus Drosera L. have long been a source of valuable natural products. The various phytochemicals characteristic of these species, particularly 1,4-naphthoquinones and flavonoids, have contributed to the diverse utilization of sundews in traditional medicine systems worldwide. A growing number of studies have sought to investigate the comparative phytochemistry of Drosera species for improved sources of pharmaceutically important compounds. The outcomes of these studies are here collated, with emergent trends discussed in detail. Important factors which affect production of secondary metabolites in plants are critically examined, such as environmental influences and in vitro culture, and recommendations subsequently presented based on this. Explicitly, the current review aims to i) present an updated, comprehensive listing of the phytochemical constituents of the genus (including quantitative data where available), ii) summarize important factors which may influence the production of phytopharmaceuticals in plants, and iii) recommend guidelines for future research based on the above, including improved standardization and quality control. We have also included a section discussing future perspectives of research on Drosera spp. based on three different research lines i) the potential to produce much needed lead compounds for treatment of tuberculosis, ii) the potential role of anthocyanins in nitrogen transport, and iii) research into 'Natural Deep Eutectic' solvents produced by Drosera spp. in the droplets or 'dew' employed to capture insect prey.
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