Effects of Non-Protein Amino Acids in Nectar on Bee Survival and Behavior

Bogo, Gherardo; Bortolotti, Laura; Sagona, Simona; Felicioli, Antonio; Galloni, Marta; Barberis, Marta; Nepi, Massimo

doi:10.1007/s10886-018-01044-2

Cited by 32 publications

(45 citation statements)

References 41 publications

(48 reference statements)

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“…We also demonstrated that bees did not exhibit innate feeding preference between a plain sucrose solution and an equal solution laced with NPAAs in a two-minute assay. In line with a previous study [36], our 10-day-long toxicological assays showed that nectar NPAAs affected neither food consumption nor bees' longevity. Taken together, these results strongly suggest that nectar NPAAs at concentrations within the natural range do not alter nectar palatability, at least for the pollinator Apis mellifera.…”

Section: Discussionsupporting

confidence: 92%

“…However, this possibility fits poorly with our results, given that both GABA and β -alanine improved rather than weakened the acquisition level of bees encountering these NPAAs in the reinforcement offered during training. Improved acquisition in appetitive learning also did not reflect a generalized enhancement of feeding because in this and other studies [36] caged bees did not consume more food enriched with NPAAs. Moreover, in one assay freely moving bees did not prefer NPAA-free sucrose solutions.…”

Section: Discussionmentioning

confidence: 43%

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Nectar non-protein amino acids (NPAAs) do not change nectar palatability but enhance learning and memory in honey bees

Carlesso¹,

Smargiassi²,

Pasquini³

et al. 2020

Preprint

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Floral nectar is a pivotal element of the intimate relationship between plants and pollinators and its chemical composition is likely to have been shaped by strong selective pressures. Nectars are composed of a plethora of nutritionally valuable compounds but also hundreds of secondary metabolites (SMs) whose ecological role is still not completely understood. Here we performed a set of behavioural experiments to study whether five ubiquitous nectar non-protein amino acids (NPAAs: β-alanine, GABA, citrulline, ornithine and taurine) interact with gustation, feeding preference, and learning and memory in the pollinator Apis mellifera. We showed that harnessed foragers were unable to discriminate NPAAs from water when only accessing antennal chemo-tactile information and that freely moving bees did not exhibit innate feeding preferences for NPAA-laced sucrose solutions. Also, dietary consumption of NPAAs did not alter food consumption or longevity in caged bees over 10 days. Taken together our data suggest that ecologically relevant concentrations of NPAAs did not alter nectar palatability to bees. Olfactory conditioning assays showed that honey bees were more likely to learn a scent when it signalled a sucrose reward containing either β-alanine or GABA, and that GABA also enhanced specific memory retention. Conversely, when ingested two hours prior to conditioning, GABA, β-alanine, and taurine weakened bees’ acquisition performances but not specific memory retention, which was enhanced in the case of β-alanine and taurine. Neither citrulline nor ornithine affected learning and memory. Our study suggests that NPAAs in nectars may represent a cooperative strategy adopted by plants to attract beneficial pollinators, while simultaneously enhancing pollen transfer among conspecific flowers. Future work should validate these results in more ecological scenarios and extend the study to as many nectar SMs as possible, alone and in combination, as well as to other species of pollinators.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionmentioning

confidence: 43%

Nectar non-protein amino acids (NPAAs) do not change nectar palatability but enhance learning and memory in honey bees

Carlesso¹,

Smargiassi²,

Pasquini³

et al. 2020

Preprint

View full text Add to dashboard Cite

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“…Therefore on the basis of environmental stimuli (presence of pollinators and/or herbivores), a plant can: (i) control the production of nectar, (ii) regulate the quantity of nectar among its flowers so as to induce pollinators to visit more than one flower and increase out‐crossing, and (iii) modulate the presence of nutrients and secondary metabolites in the nectar. Based on the above, an intriguing theory has developed about the ability of plants to ‘manipulate’ pollinator visits, mainly of insects (Nepi et al, 2018; Bogo et al, 2019). Indeed, to optimize the flow of pollen between individuals, plants exercise control over the nectar standing crop, generating very variable production of nectar.…”

Section: Flowers Nectar and Fertilizationmentioning

confidence: 99%

Plant behaviour: an evolutionary response to the environment?

2020

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Plants are not just passive living beings that exist in nature. They are complex and highly adaptable species that react sensitively to environmental forces/stimuli with movement, morphological changes and through the communication via volatile molecules. In a way, plants mimic some traits of animal and human behaviour; they compete for limited resources by gaining more area for more sunlight and spread their roots underground. Furthermore, in order to survive and thrive, they evolve and ‘learn’ to control various environmental stress factors in order to increase the yield of flowering, fertilization and germination processes. The concept of associating complex behaviour, such as intelligence, with plants is still a highly debatable topic among researchers worldwide. Recent studies have shown that plants are able to discriminate between positive and negative experiences and ‘learn’ from them. Some botanists have interpreted these behavioural data as a form of primitive cognitive processes. Others have evaluated these responses as biological automatisms of plants determined by adaptation to the environment and absence of intelligence. This review aims to explore adaptive behavioural aspects of various plant species distributed in different ecosystems by emphasizing their biological complexity and survival instincts.

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“…Based on the fact that phenylalanine and GABA are known to elicit a strong phagostimulatory response in bees, the presence of these floral nectar-specific amino acids may function to attract this pollinator (Hendriksma et al, 2014; Nepi, 2014; Petanidou et al, 2006). GABA may also confer health benefits for bees as GABA-enriched artificial nectar has been shown to increase the locomotion and survival time of bees (Bogo et al, 2019). Leucine and tryptophan may also provide a desirable flavor due to stimulation of sugar chemosensory cells (Shiraishi and Kuwabara, 1970).…”

Section: Discussionmentioning

confidence: 99%

Systems analyses of key metabolic modules of floral and extrafloral nectaries of cotton

Chatt

Mahalim

Mohd-Fadzil

et al. 2019

Preprint

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23United States 24 25 Author contributions 26 ECC, CJC, and BJN conceived and planned the study. Sample collection, microscopy, and 27 metabolomic analyses were conducted by ECC, SNM, and NAMF. Additional contributions 28 for microscopic analyses were provided by HTH. RNA preparation was completed by PMK, 29 RR, and CJC. MH processed all RNAseq data and conducted informatics analyses in 30 conjunction with ECC. ECC and BJN wrote the manuscript with feedback from all 31 coauthors. 33One sentence summary 34 The eccrine-based model of nectar synthesis and secretion is conserved in both trichomatic 35 and extrafloral nectaries determined by a system-based comparison of cotton (Gossypium 36 hirsutum) nectaries. 37 Abstract 47 Nectar is a primary reward mediating plant-animal mutualisms to improve plant fitness and 48 reproductive success. In Gossypium hirsutum (cotton), four distinct trichomatic nectaries 49 develop, one floral and three extrafloral. The secreted floral and extrafloral nectars serve 50 different purposes, with the floral nectar attracting bees to promote pollination and the 51 extrafloral nectar attracting predatory insects as a means of indirect resistance from herbivores. 52 Cotton therefore provides an ideal system to contrast mechanisms of nectar production and 53 nectar composition between floral and extrafloral nectaries. Here, we report the transcriptome, 54 ultrastructure, and metabolite spatial distribution using mass spectrometric imaging of the four 55 cotton nectary types throughout development. Additionally, the secreted nectar metabolomes 56 were defined and were jointly composed of 197 analytes, 60 of which were identified. 57 Integration of theses datasets support the coordination of merocrine-based and eccrine-based 58 models of nectar synthesis. The nectary ultrastructure supports the merocrine-based model due 59 to the abundance of rough endoplasmic reticulum positioned parallel to the cell walls and 60 profusion of vesicles fusing to the plasma membranes. The eccrine-based model which consist 61 of a progression from starch synthesis to starch degradation and to sucrose biosynthesis was 62 supported by gene expression data. This demonstrates conservation of the eccrine-based model 63 for the first time in both trichomatic and extrafloral nectaries. Lastly, nectary gene expression 64 data provided evidence to support de novo synthesis of amino acids detected in the secreted 65 nectars.66 67 68 69 130 synthesis to assess for the first time whether this model is conserved among trichomatic and 131 extrafloral nectaries. 132 Results 133 Domesticated Upland cotton, G. hirsutum (TM-1), develops four types of nectaries, 134 three are extrafloral and one is floral, and all consist of multicellular glandular trichomes, 135 specifically called papillae. The three extrafloral nectary types, foliar, bracteal, and 136 circumbracteal, are subcategorized as vegetative or reproductive. The vegetative foliar nectary 137is located on the abaxial surface of the leaf midrib ( Fig. 1A; Fig...

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Effects of Non-Protein Amino Acids in Nectar on Bee Survival and Behavior

Cited by 32 publications

References 41 publications

Nectar non-protein amino acids (NPAAs) do not change nectar palatability but enhance learning and memory in honey bees

Nectar non-protein amino acids (NPAAs) do not change nectar palatability but enhance learning and memory in honey bees

Plant behaviour: an evolutionary response to the environment?

Systems analyses of key metabolic modules of floral and extrafloral nectaries of cotton

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