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Nepi, M. Nectar-Mediated Tripartite Interactions. Encyclopedia. Available online: https://encyclopedia.pub/entry/8474 (accessed on 15 December 2025).
Nepi M. Nectar-Mediated Tripartite Interactions. Encyclopedia. Available at: https://encyclopedia.pub/entry/8474. Accessed December 15, 2025.
Nepi, Massimo. "Nectar-Mediated Tripartite Interactions" Encyclopedia, https://encyclopedia.pub/entry/8474 (accessed December 15, 2025).
Nepi, M. (2021, April 06). Nectar-Mediated Tripartite Interactions. In Encyclopedia. https://encyclopedia.pub/entry/8474
Nepi, Massimo. "Nectar-Mediated Tripartite Interactions." Encyclopedia. Web. 06 April, 2021.
Nectar-Mediated Tripartite Interactions
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This entry is adapted from the peer-reviewed paper 10.3390/plants10030507

The Mediterranean basin hosts a high diversity of plants and bees, and it is considered one of the world’s biodiversity hotspots. Insect pollination, i.e., pollen transfer from male reproductive structures to conspecific female ones, was classically thought to be a mutualistic relationship that links these two groups of organisms, giving rise to an admirable and complex network of interactions. Although nectar is often involved in mediating these interactions, relatively little is known about modifications in its chemical traits during the evolution of plants.

nectar Mediterranean plants

1. Introduction

The Mediterranean basin hosts 25,000 angiosperm species and accounts for 7.8% of world plant diversity, while it covers only 1.6% of emerged land [1]. It is also considered a centre of bee speciation, hosting 3000–4000 species of bees [2][3]. The richness of flowering plants and pollinating insects results in particularly diverse plant–pollinator communities [4] in which wild bees are common pollinators for a large fraction of Mediterranean plants and are active almost all year round [4][5][6]. The main floral resources exploited by pollinators in the Mediterranean are pollen and nectar [3]. Although studies suggest that a high percentage of species reward pollinators only with pollen [7][8], nectar is in any case relatively common and a precious resource for many pollinators in dry Mediterranean habitats [9]. Regarding other floral traits, there is evidence of pollinator-driven selection of nectar attributes. In particular, nectar chemistry has been linked to specific preferences, in terms of sugar and amino acid profile, of pollinator guilds [10][11][12][13][14][15][16][17][18][19][20][21]. On the other hand, phylogeny and climate may impose constraints on nectar traits [9][22][23][24][25][26]. Thus, a number of factors of varying relative weight may shape nectar chemistry in different ecological and taxonomic contexts.

Here, we discuss nectar traits in angiosperms in the light of recent advances in nectar biology, ecology, and evolution, taking the Mediterranean plants as a case study. As far as the evolution of nectar is concerned, there is recent evidence that the plant–arthropod relationships involved in pollination and mediated by nectar-like secretions were established well before the rise of angiosperms [27][28]. Nectar evolved and diversified in angiosperms, allowing them to develop more efficient interactions with insects, and to override interactions already established previously by gymnosperms [28]. New and complex chemical profiles of floral nectar may have played a fundamental role in shaping such interactions. An outstanding concept of nectar biology was the demonstration that secondary compounds in nectar, which have been known since the 1970s and initially thought to be toxic deterrents of nectar thieves, may directly affect certain traits of forager behavior and therefore mediate plant–animal interactions [29][30]. A further complexity of nectar-mediated plant–animal interactions is the evidence that nectar-inhabiting microorganisms may be a third party in mutualistic relationships linking plants and nectar foragers. The ecological and evolutionary significance of this emerging tripartite relationship is still far from well understood [31].

2. Nectar Sugars of Flowering Plants: An Evolutionary Hypothesis

Most plants of the Mediterranean basin flower in spring–summer and generally have nectar sugar profile high in sucrose [9][18][19][26][32][33]. It is said that high sucrose content in nectar can result from adaptation to Mediterranean spring–summer drought conditions, since high-hexose nectars consume more water than high-sucrose nectars per unit weight of sugar [9]. This consideration offers an opportunity to speculate about the evolution of this sugar profile that is shared by most of the angiosperms [34]. Sucrose-rich floral nectar was presumably not a plesiomorphic trait in early angiosperms, but it rather developed in response to climate changes in the Cretaceous period after the first appearance of angiosperms.

2.1. Rewards and Pollinators in the Mesozoic Era and in Early Angiosperms

Very early angiosperms were probably void of nectar. Fossil insect coprolites from the Early Cretaceous period, containing angiosperm pollen, suggest that the earliest (“ANITA” grade) angiosperms had dry stigmas and pollen was the only floral reward for pollinators [35][36][37]. Although controversies persist, a dry stigma is reported for Amborella trichopoda, the only extant species of Amborellales, which is considered to be the sister group to the rest of the flowering plants [36][38]. Some early diverging lineages (Annonaceae, Austrobaileyaceae, Chloranthaceae, Winteraceae) evolved stigma secretions independently [39]. In addition to providing an optimal medium for pollen germination, at least in some cases, these could function as rewards for pollinators, thus the name stigmatic nectar [37] or protonectar [39][40]. In the Early Cretaceous, flowers may also have produced “true” nectar, i.e., nectar produced by specialized complex secretory organs called nectaries [36]. In ANITA grade taxa, nectaries are relatively rare and scattered but diverse in structure (though relatively simple), pointing to the convergent evolution of nectaries in the basal angiosperm groups [35][36]. Nectaries became more common and their structure more defined and complex in clades that appeared soon after in the Early Cretaceous such as Magnoliales and Laurales [36]. In a 100 million-year-old flower assigned to Laurales, stamens or staminodes bear what are presumably paired nectariferous appendages [41]. Thus, the emerging picture of floral rewards in basal angiosperms highlights a variety of food that can be exploited by insects: pollen, stigma exudates (stigma nectar or protonectar), and nectar. The picture improves if we consider that insects fed on the pollination drop of gymnosperms, a sugary secretion produced by the ovule, well before the evolution of angiosperms. A certain consensus regarding a Mid Mesozoic (Early-Middle Jurassic) plant–insect pollination network was recently developed on the basis of new evidence from insect and plant fossils that highlights insects feeding on pollination drops of several extinct taxa of early seed plants [42][43][44][45][46]. This evidence suggests that insects fed on nectar-like secretions (pollination drops) about 40 million years before the rise of angiosperms.

In the Late Jurassic and Early Cretaceous periods, various beetles, early brachyceran flies, aglossatan mandibulate moths, sphecid wasps, and thrips consumed pollen grains and stigmatic or other sugary secretions, qualifying them as candidates for the earliest pollinators of angiosperms [35]. It is highly probable that beetle, moth, and fly pollination all evolved in angiosperms at much the same time [36]. The pollinator guilds that were active when the earliest angiosperms appeared, namely beetles, flies, thrips, and micropterigid moths, are still the main pollinators of living basal angiosperm families and of extant insect-pollinated gymnosperms [28][36]. Today, the hypothesis that the first flowering plants had a generalist pollination mode involving various insects as well as air currents is widely accepted [35][36][38]. Notably, all living and some extinct insect-pollinated gymnosperms are also, or are also thought to have been, pollinated by wind (ambophylous pollination) [28]. It is clear that the evolution of early rewards in angiosperms converged toward sugary secretions. The new condition of enveloped ovules that evolved in angiosperms led to the disappearance of sugary exudates (the pollination drop), and strong selective pressure may have promoted the provision of a new sugary exudate in flowers to cope with insects already adapted to feed on sugary surface fluids [27].

We do not know much about the chemistry of these early secretions. Direct evidence of the chemical profile of the pollination drop of insect-pollinated Mid Mesozoic gymnosperms is obviously impossible, but inference is possible. Mapping the compositions of ovular secretions of extant gymnosperms in a phylogenetic framework of seed plants led to the inference that early gymnosperms had ovular secretions that were a mosaic of those of modern species, with a high-fructose sugar profile [28].

Concerning stigma exudates, there is only one report on the sugar profile of a plant (Uvaria macrophylla) of an early divergent family (Annonaceae), revealing a hexose-rich (fructose-dominant, 72.2%) sugar profile with very little sucrose (8.4%) [47]. This sugar profile is in line with the beetle pollination that occurs in this plant, since the nectar of beetle-pollinated species is typically hexose-rich [48].

Interestingly, a hexose-rich sugar profile is common in the pollination drops of all extant ambophylous gymnosperms [28]. These taxa belong to the Cycadopsida and Gnetopsida, and the main pollinating insects are generally thrips, flies, and beetles [42][49][50]. In the Early and Middle Cretaceous period, Gnetopsida underwent a radiation that paralleled the diversifying angiosperms [42], and these taxa presumably competed to secure insect visits.

Therefore, gymnosperms (pollination drops) and early diverging angiosperms (stigma exudates) may have shared a hexose-dominant chemical profile of secretions that mirrored shared guilds of pollinators, such as Diptera, Mecoptera, Neuroptera, and Coleoptera [44].

Considering this scenario, it is also plausible that the secretions of the first “true” nectar-secreting angiosperms (i.e., angiosperm species in which the nectar is produced by a specialized organ, i.e., the nectary) had a hexose-rich sugar profile. In this regard, it is interesting to note that Diptera, which are the most common pollinators of today’s entomophilous Gnetophyta and also pollinate several angiosperm species due to their preference for hexose-rich nectar [22], experienced limited extinction in the interval when angiosperms became ecologically dominant [44]. Diptera probably shifted from earlier fluid-feeding on ovular secretions of gymnosperms to later nectar-feeding on angiosperms [50].

2.2. Evolution of Rewards along the Cretaceous

The further evolution of sugar-based secretions involved in rewarding pollinating insects was probably influenced by the nature of the secretion itself. The original functions of the ancient gymnosperm pollination drop were microgametophyte capture, delivery, germination, and ovule defense [51], all directly connected with plant reproduction. Subsequently, another function was acquired, i.e., insect rewarding, which can be considered a kind of exaptation for co-opting insects into feeding on these secretions [27]. However, chemical modifications to adapt to the new function were limited, since the maintenance of a suite of chemical and biochemical traits was necessary to accomplish the original functions (see also Section 3.1).

Something similar may be true for stigma exudates. The original function of the stigma was reception and interaction with the male microgametophyte. According to recent studies, the dry stigma is considered the basal condition in angiosperms [38]. Although involved in rewarding insects, stigma exudates still also needed to fulfill the original aim of receiving pollen and promoting its germination. Interestingly, stigma exudates of extant angiosperms are involved in a series of functions [47].

True nectar, i.e., a sugary secretion elaborated by a nectary, produced solely to interact with animals, without any direct connection to reproductive function, is a different question. It allows the nectar and nectary to readily adapt to new requirements for efficient interaction with the environment and animals. The nectary is independent of the ABC floral homeotic genes that are responsible for floral organ specification according to position [52]. During evolution, the “new” secreting organ is “free” to move about the flower in response to selection imposed by interactions with the environment and pollinators, and it was acquired and lost independently several times in the course of angiosperm phylogeny [39]. On the other hand, the nectar chemical profile can be adjusted to the requirements of specific pollinator guilds in different ways in phylogenetically related species, revealing high phenotypic plasticity [10][12][19][21]. Thus, nectar that became common in Late-Cretaceous flowers (see below) could be a more efficient tool to interact with pollinators than others employed by gymnosperms and early angiosperms in the Mid-Mesozoic and early Cretaceous, i.e., pollination drops and stigma exudates constrained physiologically by their direct involvement in the reproductive mechanism.

3. Nectar Secondary Compounds and Their Importance in Mediterranean-Type Ecosystems

Sugars are only one of the solutes in floral nectar: other known substances are amino acids, which are generally the most abundant after sugars, proteins, lipids, organic acids, and vitamins [53]. A major recent discovery in nectar biology has concerned a re-consideration of secondary metabolites (SMs) and their role in shaping plant–pollinator interactions [54]. Tannins, phenols, alkaloids, and terpenes have been detected in floral nectar in several angiosperm families since the 1970s and are considered to be toxic deterrents against predators, as well as a defense against microorganisms [31]. The concentrations of secondary metabolites in nectar are generally lower than in other plant parts, such as leaves, stems, or flowers, where they deter herbivores [55]. Plants that modulate concentrations of SMs in their tissues and secretions evolved strategies to deter herbivores (high concentrations of SMs) while attracting and manipulating mutualists (low concentrations of SMs) to maximize the benefits they obtained [29]. Two secondary metabolites are clear examples of such strategies, namely the alkaloids caffeine and nicotine. At high concentration, they are used by plants as deterrent molecules to keep away phytophagous insects [56]. The same alkaloids have been detected at low concentrations in the floral nectar of a few angiosperm species [57][58]. These concentrations in nectar have been found to have an important effect on insect neurobiology. In particular, they stimulate memory and associative learning of bees and bumblebees, thus potentially affecting their foraging behavior [57][58].

Non-protein amino acids γ-aminobutyric acid (GABA), β-alanine, and taurine were recently highlighted in floral nectar. These substances may directly affect insect nervous system activity and possibly insect behavior [30][59]. GABA is one of the main neurotransmitters in both vertebrates and insects [30]. GABA is a major neurotransmitter in vertebrates and insects [30]. Taurine and β-alanine are not neurotransmitters, but they may interact with receptor proteins on neurons [30].

GABA seems to have a special role in Mediterranean ecosystems. GABA is particularly common in the floral nectar of plants of the Mediterranean basin. Petanidou et al. [14] found GABA in the nectar of 63% of plant species of the phrygana community, which is a low dwarf shrubland plant association common in the eastern Mediterranean. GABA was detected in 82/82 species of the Lithospermeae tribe (Boraginaceae) having typical Mediterranean distribution at concentrations positively correlated with that of sucrose [60][61]. GABA seems to be related to specific pollinator guilds, such as long-tongued anthophorid, and andrenid bees, which are particularly diverse in the Mediterranean region, as well as anthomyiid and syrphid flies [14].

Several functions of GABA have been recognized in plants and animals. In plants, GABA is reported to be involved in response to pathogen attack and to accumulate after infection by fungi and bacteria [59][62]. Plants also use GABA to combat abiotic stress due to drought, salinity, low light, and low temperature [63]. Furthermore, GABA is an endogenous signaling molecule involved in the regulation of plant growth and development and in plant fertilization, where it drives pollen tube growth in pistil tissues [63][64].

In vertebrate and invertebrate animals, GABA is the most abundant inhibitory neurotransmitter [30]. Its inhibitory effect is at least partly due to binding of the molecule to ionotropic receptors, i.e., ion channels that change their permeability to ions after binding with the ligand. The flow of K+ or Cl− along the channel hyperpolarizes the neuron, decreasing its probability of firing [30]. Interestingly, K+ is generally the most abundant nectar ion [20][65]. A diet containing GABA affects the survival and behavior of pollinating insects. Caged bumble bees, fed with artificial nectar containing GABA at concentrations similar to those occurring naturally in nectar, have a higher survival rate than control bumble bees [66]. In insects, GABA also limits excessive, potentially disruptive excitation states under conditions of stress [59][66].

As a result of its role in stress protection, GABA could have originated in plant tissues as an adaptation to increasing aridity in the Cretaceous period, similar to how sucrose dominates in floral nectar. As postulated for other secondary compounds in nectar, low concentrations of GABA may leak into nectar from the surrounding tissues as a pleiotropic effect, as postulated for other secondary compounds in nectar [59]. Pollinators, specifically bees, may impose a selection of specific concentrations of GABA if it has positive effects on their physiology, as suggested by Bogo et al. [66] and as observed for other nectar secondary compounds [57][58].

Nectars with appropriate concentrations and profiles of SMs presumably evolved and diversified in angiosperms and allowed them more efficient interactions with insects, overriding interactions already established in gymnosperms [28]. In this regard, it is interesting that ambophylous gymnosperms, which co-diversified with angiosperms, contain a non-protein amino acid (β-alanine) in their pollination drop, unlike wind-pollinated gymnosperms, the pollen drops of which are almost devoid of non-protein amino acids [28]. Testing the pollination drops of ambophylous gymnosperms for other secondary metabolites could shed light on the evolution of a “blend” of secondary metabolites in this group of plants, which competed with radiating angiosperms to secure pollinator visits. Although we know few nectar secondary compounds [30][54], discovering how they were shaped and how they influenced the evolution of plant–pollinator relationships could be an interesting topic for future research. A further development in this topic will be to assess the effect on insects of a mixture of secondary compounds, since the current studie

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Subjects: Plant Sciences
Contributor MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register : Massimo Nepi
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