More recent research, however, is starting to unravel the mechanisms by which plants produce nectar — identifying some of the pathways sugars are transported within the plant and concentrated in their nectar [8]. There is still lots to learn. Nectaries and Nectar. Springer: The Netherlands. ISBN: Antimicrobial nectar inhibits a florally transmitted pathogen of a wild Cucurbita pepo Cucurbitaceae. American Journal of Botany 97 6 : Honeybees prefer warmer nectar and less viscous nectar, regardless of sugar concentration link.
The protective function of ants visiting the extrafloral nectaries of Bixa orellana Bixaceae. What does it cost a plant to produce floral nectar? Nature Ancestral deceit and labile evolution of nectar production in the African orchid genus Disa. Are nectar robbers cheaters or mutualists? Ecology 81 10 : The strawberry timebomb: how basic plant biology can help you store your produce. Leave a Reply Cancel reply Your email address will not be published.
Once older, plants can be colonized by other ant species that do not sterilize them allowing their reproduction Palmer et al. The overall effect may be an increase in plant fitness. The few examples reported above show that nectar-foraging behavior of animals may be unpredictable and highly variable, exposing nectar producing plants to the risk of not receiving any real benefit as a counterpart for the expense of nectar production.
Selection can therefore be expected to favor strategies to counteract this risk. Plants have several ways of affecting the behavior of nectar foragers and study of these effects led to the first hypotheses about nectar-based manipulation of insects by plants Biernaskie and Cartar, ; Pyke, The studies were almost exclusively focused on relationships between FN and pollinators, but the manipulation hypothesis was recently extended to EFN and ants Grasso et al.
The reproductive success of plant species that rely on pollination by insects is determined by insect foraging activity. The behavior of foraging insects determines which flowers set seed and the pattern of pollen transfer and thus male gametes between plants, and ultimately plant population genetic structure Goulson, The behavior of foraging insects involves decisions when encountering a food resource according to variability of nectar traits such as volume and concentration and their spatial distribution Goulson, ; Leiss and Klinkhamer, ; Cnaani et al.
The abundance and spatial distribution of nectar available to a foraging insect at a given time is called the nectar standing crop Galetto and Bernardello, Nectar standing crop varies widely between flowers of a plant Keasar et al. This variability is the combined result of the nectar production rate of flowers and insect foraging activity. Plants may be under selection to produce variable nectar resources so as to economize investment in nectar production while increasing the possibility of cross-pollination.
At population level, the nectar standing crop generally has a patchy distribution: one or more highly productive plants are neighbors to others that produce less Leiss and Klinkhamer, The same happens at the smaller scale of individuals of nectar producing species that may bear a certain number of nectarless flowers Gilbert et al. Empty flowers borne by nectar-producing individuals are an energy-saving strategy that enables the plant to save resources normally allocated to nectar production while maintaining its attraction for pollinators Bell, Nectar standing crop variability is also revealed by the generally positive skewed distribution of nectar production by individuals, which means that there are few flowers producing a large quantity of nectar and many flowers producing a smaller amount Gilbert et al.
Standing crop structure i. Short visits and fast moves between flower patches reduces the probability of geitonogamy self-pollination between flowers on the same plant and the risk of inbreeding. Highly variable standing crops are therefore considered a strategy to increase the out-crossing rate and offspring fitness Smithson and Gigord, ; Bailey et al. Moreover, plants offering high rewards may have an emanating effect on neighbors offering small rewards Leiss and Klinkhamer, In this way plants with low nectar production may benefit from pollinator services enhanced by the presence of high nectar producing neighbors, while saving on the cost of nectar production.
Plants may exert control over nectar standing crop by providing highly variable nectar production that in turn affects the foraging behavior of pollinators. In this framework a manipulation hypothesis was first elaborated by Biernaskie and Cartar who reported a positive correlation between variability in nectar production rate and floral display number of open flowers in individual plants of nine angiosperm species. According to these authors, the increased attractiveness of a plant caused by an abundance of flowers is coupled with greater variability in nectar production rates of its flowers so as to obtain an optimal trade-off between number of visits and the length of the pollinator visitation sequence.
Nonetheless, nectar standing crop is affected by two orders of variability: variability in nectar production controlled by plants, on which further variability generated by the foraging activity of pollinators is superimposed Goulson, ; Keasar et al.
Pollinator-generated variation seems to have major effects on pollinator foraging, possibly overriding the effects of plant-generated variation. Pollinator-generated variability in nectar resources may thus reduce the selective benefit of plant-generated variability as a strategy to decrease geitonogamy Keasar et al.
It is also worth noting that environmental parameters at macro- and micro-environment level may influence nectar production, standing crop and insect activity Pacini and Nepi, , further decreasing the strength of the control exerted by plants. It follows that plant control of pollinator behavior through modulation of variable nectar production is possible but seems quite weak. Plants may, however, use other tools to influence the feeding behavior of pollinators.
A nectar trait quite recently considered when studying the effect of nectar on insect feeding behavior is its chemical composition. Floral and EFN is largely composed of sugars, usually together with other primary metabolites, such as amino acids, lipids, and proteins Nicolson and Thornburg, Secondary metabolites alkaloids, terpenoids, and phenols are reported more rarely than primary metabolites, but their presence is presumed to be quite common Nicolson and Thornburg, ; Roy et al.
Sugars and amino acids are the most abundant primary metabolites and are an important source of energy and nitrogen, respectively Roy et al.
They are therefore the main determinant of the food value of nectar, but they can also affect the attractiveness of nectar since they are responsible for its taste Gardener and Gillman, Both sugars and amino acids affect insect feeding behavior through post-ingestive signaling, involved in associative learning and memory Simcock et al.
Associative learning is a mechanism that allows animals to identify cues associated with nutrients so that they can be located quickly when required Simcock et al. Sucrose is the most common and abundant nectar sugar Baker and Baker, b and is preferred by honeybees to other naturally occurring sugars Barker and Lehner, Its concentration is an important determinant for many foraging-related decisions Scheiner et al.
Interestingly, this disaccharide is recognized as the most phagostimulatory sugar for honeybees, and bees rewarded with sucrose are more likely to learn to associate an odor with a food source Simcock et al. All twenty amino acids commonly found in proteins have been identified in various plant nectars.
Proline seems to be of special importance for insects. It not only contributes a taste preferred by insects Alm et al. In an experiment using free-flying foragers, Hendriksma et al. Phenylalanine, one of the most abundant amino acids in nectar Petanidou, , has strong phagostimulatory activity, while glycine is a phagodeterrent, both at concentrations similar to that occurring naturally in nectar Hendriksma et al.
The same authors also demonstrated a trade-off between sucrose concentration and amino acid preferences: nectar with low sucrose concentration that is normally unattractive to bees can become attractive if it contains minute concentrations of the phagostimulant phenylalanine, whereas the phagodeterrence of glycine can be masked by high concentrations of sucrose Hendriksma et al.
It follows that plants can replace expensive carbohydrates in their nectar with minute concentrations of phagostimulating amino acids, or modulate pollinator visits by adding phagodeterrent amino acids. The link between sucrose and amino acids in affecting feeding behavior was also revealed by experiments testing how nutritional state affected the taste of specific amino acids isoleucine, proline, phenylalanine, and methionine and associative learning of honeybees Simcock et al. Results showed that bees pre-fed sucrose solution consumed less of solutions containing amino acids and were less likely to associate amino acid solutions with odors.
Surprisingly, bees pre-fed solutions containing an amino acid were also less likely to associate odors with sucrose the next day. Bees consumed more food and were more likely to learn when rewarded with an amino acid solution if they were pre-fed isoleucine and proline Simcock et al.
The authors concluded that single amino acids at relatively high concentrations decrease feeding on sucrose solutions containing them, and they can act as appetite reinforcers during learning. Plants produce a plethora of SMs with a variety of functions. They are mainly involved in defense against herbivores and other enemies such as fungi and bacteria but may also have other additional functions Schoonhoven et al.
Secondary metabolites, including tannins, phenols, alkaloids, and terpenes, have been found in FN in more than 21 angiosperm families Adler, These compounds have been known since the s and were initially considered to be toxic deterrents of nectar thieves while encouraging specialist pollinators Baker and Baker, a ; Adler, ; Barlow et al.
More recently, researchers have discovered that these compounds, and particularly alkaloids, may play an important role in managing visitor behavior. Nicotine a pyridine alkaloid is a typical insect-repelling alkaloid and is found in the FN of Nicotiana attenuata , where it increases the number of flowers visited and reduces the volume of nectar consumed by hummingbirds and moth pollinators Kessler and Baldwin, The unpleasant taste of nectar containing nicotine reduces nectar consumption and the length of flower visits, leading to a higher rate of outcrossing Kessler et al.
Shorter visits also reduce the risks associated with excessive visitation of individual flowers, such as increased reception of incompatible pollen or removal of compatible pollen grains from the stigma surface Pyke, Plants with FN containing nicotine are able to minimize nectar volumes, while maximizing pollination efficiency, seed production and plant fitness. In this perspective the function of nectar is not to increase flower attractiveness but rather to optimize pollen flow between individuals by altering the feeding behavior of insects.
Other nectar SMs may have phagostimulatory activity, although this function seems restricted to species adapted to feed on plants with a high content of SMs Stevenson et al. Note that SM effects on insects are dose dependent Manson et al. The feeding deterrent function of nectar SMs is due to the unpalatable taste of alkaloids, especially nicotine, that is perceived by insects as soon as their proboscis contacts the nectar.
The mouth parts of insects have contact chemoreceptors with neurons responding to sugars, salts, acid, water and non-nutrient compounds Stevenson et al.
Nectar SMs may have post-ingestive effects on other targets in the insect body, such as the brain, affecting their neurobiology Table 1.
It was recently reported that honeybees rewarded with solutions containing caffeine a purine alkaloid at concentrations similar to that occurring naturally in the FN of Coffea and Citrus species, remembered the learned floral scent better than honeybees rewarded with sucrose alone Wright et al. At higher concentrations, caffeinated solutions exerted a deterrent effect and bees were more likely to reject caffeinated solutions.
Pollinators therefore drive selection for nectar that is not repellent but still has neurobiological activity. From the plant perspective, pollinator constancy is clearly beneficial since it minimizes pollen wastage and unfruitful heterospecific pollination.
TABLE 1. Secondary compounds and their hypothesized or tested post-ingestive effects on neurobiological or physiological traits of insects. A similar behavioral effect was reported in bumblebees fed with solutions containing nicotine at concentrations within or above the natural range Table 1.
Bumblebees were only deterred by unnaturally high nicotine concentrations 50 ppm and this deterrence disappeared or became attraction at lower nectar-like concentrations 1 and 2. The same concentrations affected bumblebee flower preference through enhanced memory of floral traits. Increasing numbers of bumblebees remained faithful to flowers containing nicotine at any tested concentration, even if they become a suboptimal choice in terms of caloric value Baracchi et al.
Although the neurobiological mechanism was not studied, it is postulated that nicotine, being an agonist of nicotinic acetylcholine receptors, may act as a psychoactive drug, modulating cholinergic neuron activity in the insect brain and positively reinforcing the flower-reward association Baracchi et al.
Those more common in nectar, i. They may affect insect behavior in several ways: by affecting insect nervous system physiology, regulating nectar intake through phagostimulation and promoting muscle function Felicioli et al. However, no clear confirmation of this hypothesis has yet been found.
Thus it appears that indirect plant protection involving ants is elicited by plant-mediated dietary imbalances. Actually, the aggressiveness of tending ants increases with increasing EFN carbohydrate content Grover et al. Carbohydrates are a major fuel for metabolically expensive behaviors, such as ant aggressiveness and hyperactivity. There is little literature on secondary metabolites in EFN.
This alkaloid was retained in the extra-floral nectary at high concentrations as well as excreted into EFN at low concentrations. The plant modulated secondary metabolite concentrations to relate differently to herbivores and mutualistic consumers: high concentrations in EFNs protected the gland from herbivores while low trace concentrations in EFN had no apparent effect on ants Cardoso-Gustavson et al.
Though not reported in EFN, four alkaloids caffeine, theophylline, cocaine, and atropine can have significant effects on many aspects of ant physiology and behavior Cammaerts et al. In particular, when ingested, the alkaloids altered locomotion, memory, olfactory perception and reactions to stimuli in the Myrmica sabuleti ant model Table 1. Whether any of these or other neuroactive compounds could be components of EFN, and their effects on attending ants at concentrations plausible for EFN, are not known.
In this context, it is worth noting that ants are subject to manipulation by other organisms Hughes, ; Grasso et al.
A recent case regards blue butterflies Lepidoptera: Lycaenidae whose caterpillars produce a sugary secretion that attracts ants which then defend the larvae from predators. Hojo et al. A striking case of partner manipulation involving the myrmecophyte Acacia cornigera and the mutualist ant Pseudomyrmex ferrugineus is therefore not surprising Heil et al. These ants only feed on the sucrose-free nectar produced by their host plant; the nectar is not attractive to other generalist exploiter ants.
Until a few years ago, Pseudomyrmex ferrugineus ants were believed to lack invertase a sucrose hydrolysing enzyme in their digestive tract, a physiological trait compensated by the plant through secretion of sucrose-free EFN Heil et al.
Once eclosed, young workers ingest EFN as the first food available. Since this inhibits their invertase, they are forced to continue feeding on host-derived EFN, being unable to digest any other food Heil et al.
The plant manipulates the digestive physiology of the symbiotic ants to enhance their dependence on host-derived food rewards, thus stabilizing in the partnership and avoiding possible interference by exploiters. Recent research on nectar-mediated plant—animal interactions highlights that FN and EFN is much more than a sugary reward for animal services.
As suggested by Pyke , nectar can now be viewed as a pollinator manipulant rather than simply an attractant or reward Figure 2. Clear effects of nectar-mediated manipulation are known for pollinating insects and are mainly based on secondary metabolites in FN Figure 2.
Although detailed studies are only available for caffeine and nicotine Kessler et al. Diagram of nectar-mediated manipulation of pollinators and tending ants. Picture of nectar-dwelling microorganism Metschnikowia gruessii reproduced with permission from Carlos M. The real outcomes of these manipulative strategies are not yet well-understood. Plants enhance recall of a food resource by presenting appropriate concentrations of psychoactive drugs in FN Wright et al.
On the animal side, although improved recall can be positive for efficient foraging activity, it also has a negative counterpart since bees tend to return to the source of caffeinated nectar when it is no longer available Couvillon et al.
The presence of nectar-dwelling microorganisms adds a further level of complexity to these manipulative interactions Figure 2. Microorganisms such as yeasts and bacteria are very common in FN where they are inoculated by pollinators and can be considered a third partnership in nectar-mediated plant—pollinator interactions Herrera et al.
They are responsible for drastic changes in nectar chemical profile that potentially affect pollinator behavior and foraging choices: they alter the concentrations of specific sugars and amino acids Canto and Herrera, ; de Vega and Herrera, ; Pozo et al.
Interestingly, microorganisms are also able to alter the profile of nectar SMs. For example, they can significantly lower the concentration of nicotine and thus interactions with pollinators, since the effects of secondary compounds are concentration-dependent Vannette and Fukami, Ants are known to transport microorganisms de Vega and Herrera, although the presence of the latter in EFN has never been reported.
Another aspect that needs to be considered in reporting complex outcomes of manipulative exploitation in mutualistic relationships is that nectar is a complex mixture of solutes, while experiments on the effects of nectar-specific compounds are often conducted on single molecules, ignoring any synergic or antagonistic effects.
Secondary metabolites in EFN and their possible interactions with tending ants and other insects have not been the subject of much research Figure 2. Complexity similar to that of FN-mediated interactions is also likely for EFN but has not yet been investigated Grasso et al. Since the targets of indirect defense by mutualism with ants are plant enemies such as herbivores, aggression is an obvious ant behavioral trait that could be manipulated by plants, although other less conspicuous behaviors could also be affected and have significant positive effects Grasso et al.
Plants modulating the concentration of SMs in their tissues and secretions evolved strategies to deter herbivores high concentrations , while attracting and manipulating mutualists low concentrations to maximize the benefits they obtained.
When such strategies evolved is hard to say. The oldest plant—insect relationship is predation of plants by herbivores and plants underwent natural selection on the basis of chemical defenses secondary metabolites evolved against herbivores. When mutualistic insects evolved defenders and pollinators they presumably drove plant selection toward optimal low concentrations of SMs and other substances in secretions they fed on, while plants probably started to manipulate insect behavior pharmacologically, improving their own fitness.
Nectars with SM profiles presumably evolved and diversified in angiosperms and allowed them more efficient interactions with insects, overriding interactions already established by gymnosperms Nepi et al. Concluding, since conflicts also arise in cooperative partnerships, nectar-mediated partner manipulations may be more frequent than previously thought in plant—insect interactions conventionally regarded as mutualistic.
MN designed the outline and wrote the draft of the paper. DG and SM commented on the draft. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Ackerman, J.
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Back to News Update. Nectar and Migration Article Journal. For example, in a study of dandelions in Alberta, researchers discovered: Larger flowers produced more nectar. The quantity and concentration of nectar were significantly higher in flowers 2 days old than in those 1 day old.
Most flowers opened in the morning and closed in the afternoon, so nectar was not available for the full day. Nectar-sugar concentration and sugar value increased with increasing temperature.
High nectar-foraging activity by honeybees coincided with peak nectar-sugar production. Where is nectar produced? Image: Harlen Aschen.
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