Water, Secondary (& Minor) Metabolites, and the Gastronomical Benefits of Monoculture Honeys for Thee, Not for Bee
Part One covered the micronutrients. Part two deals with the secondary metabolites, those compounds with deterring (or attracting) functions: alkaloids, flavonoids, phenolics, the inorganic ions, the caffeine, the nicotine, and other products that manipulate pollinator behaviour for the plant’s own benefit. Water deserves a mention, as some (avian) pollinators cannot tolerate it, while bees have developed several methods of removing it from their nectar. (How Apis mellifera manages water has been covered here).
Secondary Metabolites in Nectar: Therapeutic Effects, Deterring Effects & (at the Colony Level) Toxin-Buffering Effects
Plants produce secondary metabolites (“phytochemicals”) as a defence against herbivory. Nectar-feeding animals ingesting such compounds may end up manipulated into favouring plants with a lower nutritional value, so long as it contains those “desirable” substances. The reader will not be surprised to know that caffeine and nicotine are two such examples. This benefits plant twofold: it improves reproductive success (pollinators are more likely to visit you) and provides protection against plant pests & pathogens ([some] bugs and bacteria will not be able to harm you).
In honey bees, ingestion of sugar syrups containing caffeine (as well as other syrups containing kaempferol [found in heaths] or coumaric acid [found in sweet clovers]) lowered the number of Nosema ceranae spores in the worker’s hindgut, reducing the Nosemosis severity & improving their lifespan (Bernklau et al., 2019). The caffeine concentrations administered were within the naturally-occurring range of 25 ppm (“parts-per-million”, as in, for every one million parts of a solution [here, sugar syrup], 25 of those parts will be caffeine molecules). Both low & medium caffeine doses (25 & 250 ppm respectively) had a positive effect on infected worker bee longevity, whereas the highest dose of 2,500 ppm had negative outcomes – think twice before spiking your next syrup feed with instant coffee.
Compare that to the experiment which fed honey bees field-relevant concentrations of nicotine (1 ppm) and found no reductions in the severity of Nosema infections (Hendriksma et al., 2020). That said, when Bombus impatiens were fed a 5 ppm concentration of anabasine (a structurally-similar nicotine alkaloid from tree tobacco Nicotiana glauca) they had reduced levels of the intestinal parasite Crithidia bombi1 (Richardson et al., 2015).
Secondary Metabolites Deters Non-Pollinators, Select for Mutually Beneficial Visitations
No two pollinators will share the same secondary metabolites preferences. The South African succulent shrub Aloe vryheidensis produces a dark red-brown nectar with “a distinctive bitter taste” (the authors tried it) due to a high concentration of phenols (Johnson, Hargreaves & Brown, 2006). Observations of A. vryheidensis visitors showed them to be generalist (and adorable) nectarivores birds (e.g. Bulbuls & White-eyes), who accumlated pollen on their faces as they fed on nectar. Of the bees, the native Apis mellifera species (probably A.m. capensis or A.m. scutellata) and the local sweat bees (Halictidae) visited the plant exclusively for its pollen2. When the authors setup feeding trials with A. vryheidensis nectar, the bees rejected it, opting for the control sugar syrups.
Another plant, the African Milkweed (Pachycarpus asperifolius), produces nectar that is favoured by the large spider-hunting wasps genus Hemipepsis (Shuttleworth & Johnson, 2006). A variety of insect species visited the milkweeds, with the wasp being the only one capable setting fruit (i.e. pollination). Again, the authors found P. asperifolius nectar to be distasteful, as feeding experiment in honey bees showed them preferring plain sugar syrups over the floral nectar, even when adjusted for sweetness (70% sucrose!). Analysis of the nectar showed a high phenol content, and as with the Aloe example above, suggests that this secondary metabolite selects for specialist insects who can pollinate the plant rather than a generalist hungry-hungry-hippo.
Bumble Bees’ Syrup Consumption is Impacted by the Prescence of Secondary Metabolites
Secondary metabolites can also be referred to as “plant toxins” if you’re a herbivorous insect. It also makes for clickbaity titles in the literature since botanically speaking, a compound like nicotine is a “plant toxin”. Pharmacologically, the dose makes the poison, and a low dose of a poison can have a therapeutic effect, as in tobacco smoking, despite your mother’s disapproval.
Research by Tiedeken and colleagues found that the Buff-tailed bumblebee B. terrestris would consume less sucrose solution if it held certain secondary metabolites at field-relevant doses (caffeine, nicotine and grayanotoxin [found in Rhodendrons]; Tiedeken et al., 2014). The authors suggest that it may be due to “post-ingestive detection of the toxins, which is modulating appetite”, and this author reckons that the same effect is evident in mankind when we consume a combination of caffeine and nicotine (recall that the Breakfast of Champions™ consists of coffee and cigarettes).
A caveat: these are sugar syrups containing one compound, and nectar has many other compounds that may interact to either enhance or reduce the effect(s) of the secondary metabolite being tested. Still, it is a useful model. After all, when such feeding experiments showed that A. mellifera preferred sugar solutions that contain low doses of neonicotinoids (Kessler et al., 2015), we learnt that one: pesticides are bad, and two: generalist bees either cannot detect pesticides or do not object to their taste.
Do Eusocial Bees Have Less Taste Receptors Because of Colony-Level “Social Buffering” Towards Toxins?
Honey bees have very few taste receptors (around 10 gustatory receptor genes, discussed more broadly in de Brito Sanchez, 2011), and bumble bees are in a similar boat. Could this lack of taste contribute to generalists foraging, as more taste receptors would lead to greater discrimination of foods? Maybe, given that fruit flies have 68 receptors genes and they specialise on decomposing plant material, or perhaps this number random luck and only a third of those 68 receptor genes encode for functional proteins (Dunipace et al., 2001).
“Social buffering” of toxins occurs at the colony level: An individual (may) suffer from a toxin, but the collective survives. Consider that should Bee One ingests harmful secondary metabolites, the concentrations of those compounds decreases as the nectar is transferred to Bee Two, Three, and so on… The colony then processes this no-longer-toxic nectar into a useable form, surviving at the cost of (potentially) long-term harm to the bees who forage and handle it in its “raw” form. Even if the forager dies, the colony is unharmed, as other hive members will not visit that deadly flower patch as dead bees cannot waggle dance. Yet another example of “superorganism resilience” at work.
Nectar’s Inorganic Ions are an Insignificant Fraction; Perhaps Contributing to Plant-Pollinator Specialisations
The inorganic ions of nectar are insubstantial features since pollinators supplement their mineral intake through pollen, “dirty” water (e.g. urine) or arthropod consumption (as with birds, bats or wasps). The primary ions are cations (sodium, potassium, calcium, magnesium) and anions (chloride, phosphate, sulfate, and iodide); in some nectars they contribute to salt balance (I wonder if this is more relevant for purely nectarivorous animals like hummingbirds?).
Part One discussed how nectar contains trace amino acids, and this scarcity also applies to inorganic ions. One study of 20 Nicotiana species showed that the inorganic ion content (specifically anions) was greater in night-time pollinated species versus the daytime ones (Teideg & Lohaus, 2017). Potassium is the dominant cation and chloride the dominant anion, suggesting that nighttime pollinators are more active, or have relatively higher ion needs.
High levels of potassium were shown to deter honey bees from collecting onion nectar (concentrations vary from 3,600 to 13,000 ppm; Waller Carpenter & Ziehl 1972 [I wonder if our modern farming & fertiliser methods have led to reduced levels of potassium in onion nectar over time?]).
The same high potassium (and phosphate) content reduced honey bee visitation to avocado flowers, but not their native stingless bee & wasp pollinators (Afik et al., 2014). While the authors’ results do not suggest that a high inorganic content is attractive for native avocado pollinators, it could show that as with the secondary metabolites, inorganic ions contribute to specialisations in plant-pollinator relationships. The native pollinators of onions are mostly flies and some solitary bees in central Asia (however the giant honey bees A. dorsata in South Asia are also efficient pollinators, as reviewed by Devi et al., 2015).
Bird-Pollinated Plants Produce High-Water Low-Sugar Nectars; Insect-Pollinated Ones Are More Concentrated
Nectar’s water content varies with the environment: a hotter-than-usual day will produce nectar containing less-than-usual water and vice versa, as the plant aims to conserve/offload excess water3. Insect-pollinated flowers produce low volumes of nectar to begin with, so from the researcher’s point of view, it’s hard to derive a flower’s exact volume or water content (you don’t need much nectar to feed a bee). How often nectar is removed (whether by plant or pollinator) also influences the total water content, and there are other factors that lead to variations at the individual plant level. We start with water management in insects:
Dilute Nectar is Easier to Collect; Concentrated Nectar is More Energy Efficient
A more-dilute nectar is (generally) easier to consume than a sugary one due to a lower viscosity. There are three primary feeding styles:
- A suction feeder like butterflies and moths (Lepidopterans) use their proboscis to suck up the nectar and will struggle when it gets too viscous (frozen smoothie appreciators can relate).
- Nectar-feeding birds use a subset of the suction method, relying on capillary action with their tongues acting as a porous surface that directs liquid from the nectaries and onto their tongue. They are adept at consuming nectar at both high-and low-sugar concentrations (covered below).
- Bees in general will dip their proboscis into the nectar and “lap it up”, a technique that favours the more energy-dense concentrated nectars.
- However, an individual bee can swap to the “suction” method for dilute nectars to maximise ingestion gains (Wei et al., 2020).
- In A. mellifera this swap is reflexive. When the aforementioned researchers offered bees solutions of different sucrose concentrations, the individual bee readily swapped between feeding styles. This adaptability is useful considering that they are generalist foragers and will visit a variety of flowers. Great for honey bee, not so much for the specialist solitary bee.
- However, an individual bee can swap to the “suction” method for dilute nectars to maximise ingestion gains (Wei et al., 2020).
In any case, the individual bee removes the excess water prior to storing it as honey (Apis spp.) or using it as brood food (every other bee [yes, I’m lumping the stingless bees here]):
- Solitary bees can control water levels via “blowing bubbles”,
- Bumble bees may hold droplets on their probiscis and repeated stick their tongues out,
- Honey bees bring it back to their hive for processing.
- A middle-aged bee received the forager’s payload and shares it with other nectar processors via trophallaxis (mouth to mouth feeding), and/or later placing into open cells where fanning bees will circulate air to evaporate the excess water.
No matter the bee, once the nectar is concentrated enough, it is ready for provisioning her brood or storage.
Now you may think it’s more energy efficient for the bees to gather concentrated nectar as there is less water processing required, and this is generally correct. It is when the weather warms that excess water becomes useful, either for cooling the brood or the forager. For example, the dilute nectar of A. castanea, Cat’s Tail Aloe, in South Africa is a popular source of water for birds in the dry season, despite it containing less than 10% nectar by weight (Nicolson & Nepi, 2005). However, in this instance, the honey bee foragers visiting the Aloe were collecting its pollen rather than the nectar, as the less-than-10% sugar concentration makes foraging inefficient.
Blowing Bubbles: Nectar Dehydration in Solitary Bees
This is more of a visual section. Bubble blowing behaviour is an adaptation of solitary bees to concentrating nectar. They do not have large hives or multiple “helpers” with the dehydration process, so the mother bee makes do by sitting on a surface and exposes the nectar (from her crop, the storage stomach, not the digestive one) to the outside air and repeating. The bubble formation controls how much liquid is released and is perhaps an effective way for a solitary bee to manage excess nectar water.
Sidenote: Bumble Bees Choose Flowers That Provide the “Fastest”, Not “Efficient-est” Energy to Their Colony
A tangent: Bombus spp. store little honey in their colonies, so their solution to nectar concentration is by loading the droplet onto their glossa, choosing a nice sunny spot (“nice” is optional), and continually exposing their tongue it to the outside world to evaporate excess water. The study by Pattrick & colleagues showed bumble bees foragers prefer large short-term sugar (“energy”) gains over a lower, sustained, source for their colony (Pattrick et al., 2023).
The authors found that B. terrestris opted for maximising the rate of energy return (carbohydrate flow to the nest) over worker longevity. Foragers will choose flowers that have a higher sucrose concentration even if it means more energy is expended in collecting them (which will impact its total lifespan – foraging is costly work). There is a need to raise a strong colony so that when the season ends and the reproductive males and females (gynes) emerge, they will be of a higher quality, thus increasing the subsequent generation’s chance of survival.
Nectarivorous Birds Adapted to High Water, Low Sucrose Nectar by Modulating Intestinal Absorption or Producing (Very) Dilute Urine
The three avian lineages that feed on nectar are the hummingbirds, sunbirds and honeyeaters (surprise!). Bird-pollinated plants tend to produce relatively-less-nectar than insect-pollinated ones (Pyke & Waser, 1981). As a result, they manage high-water, low-solute volumes (not to mention absorption, metabolism, warming the water to body temperature…) and simultaneously maintain the energy-intensive state of flying. These birds adapted to rapidly metabolise the dilute sucrose into glucose & fructose, and the former is readily utilised for flight (Hummingbirds use both glucose & fructose; reviewed in Nicolson & Fleming, 2014).
Sunbirds and honeyeaters control this excess water by stopping its absorption – it travels through their gut and out the other end. This is a challenge for their intestines, as they need to selectively absorb the sparse nectar nutrients (sugars, amino acids etc..), so that by the end of its journey, the expelled liquid is “mostly water” rather than “undigested nectar”. Hummingbirds absorb all of their ingested water, and depend on their kidneys to filter the excess while maintaining adequate salt levels (drinking too much water dehydrates as you dilute your electrolytes; reviewed in Nicolson & Fleming, 2014).
If you’re wondering why these bird-pollinated plants should have any water in them at all, consider that holding more water is advantageous for when the birds enter a fasting state (i.e. before bedtime). Sunbirds and honeyeaters increase their water retention in the last few hours of feeding of the day and throughout the night they lose water via dehydration rather than diuresis (this is the technical term for “passing it through the kidney and ending up as peepee”). Hummingbirds do not have this luxury, and will enter torpor, that state of lethargy and reduced metabolism/body temperature for the purposes of conserving energy, until their next meal the next day.
On Pollinator Health: Nectar Diversity Vs. Monocultures
A monoculture (“single-crop”) diet is insufficient for bee growth, even if that plant produced forage that met all the bees’ needs (and such plants do exist – clover pollen [Trifolium spp.] was proposed by Filipiak et al., 2017). Fields of ideal forage (clovers) are rare in commercial agriculture, as it is more likely to be soybeans, rapeseeds, almonds or citrus (amongst others); their nectar and pollen components vary in nutritional content.
Of course, what we take for “common sense” will not fly with the regulatory (or sciencey) types, so studies have come out showing that “why yes, mixed fruit and vegetable farms have better health outcomes over monocultures for both honey and non-honey bee species” (Doleazal et al 2019, St. Clair et al., 2020 & Noel et al., 2021). As you know by now, nectar is more than carbohydrates, and this nutritional diversity means that bees foraging on mixed crops will be better able to manage physiological stressors since the hive will have both the required nutrients for managing the stressors and the ability to favour one plant type over the other if its nectar (and/or pollen) provides the pharmacologically-favourable active compounds.
A monoculture-fed hive is more susceptible to stress from pesticides, pathogens (Varroa and migratory beekeeping are. to put it lightly, not a great combination) or perhaps from the higher temperatures that come during the spring and summer. These already nutritionally-deficient colonies are pushed over the edge, to the point where the boy cries “colony collapse disorder”, and all the villagers believe him.
Monocultures Are Good for One Thing: “Pure” Honey
I’ve put the “pure” in parenthesis as the legal definition for “pure honey” differs from the scientific one: you cannot predict that a forager’s ~10 km radius will purely contain the advertised crop. Perhaps they’ll gather nectar from a weed or native flowers and that will go into the honey supers. So long as the honey is sufficiently dominated by nectar from one floral source and expresses the characteristic properties of said source, it can be termed “Pure XYZ honey”. Citrus honey, lavender honey, various Eucalyptus honeys… the list goes on, and they taste spectacular.
Of course, the consumer (including myself) does not stop and think “oh those poor bees were fed on a single plant source in order to produce this hunny”, we eat it and quote great Ursine connoisseurs like Winne: “The only reason for being a bee is to make honey. And the only reason for making honey is so I can eat it.”.
This Nectar Chemistry Part Two was longer than I expected. Thank you for reading.
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Footnotes
- Consider the biological differences of the two intestinal parasites: Nosema reproduces intracellularly within the cells of the gut, whereas Crithidia does so in the gut lumen (i.e. extracellularly [the “lumen” is the empty, open space inside a hollow organ like the gut or blood vessel, where wastes and nutrients pass through]). As such, Nosema is exposed to less nicotine than Crithidia since there is more of the compound outside than inside the cells.
There are structural differences too: Nosema is a prokaryote and Crithidia an eukaryote- there may be more “weak points” in a eukaryotic cell than a “simpler” prokaryote, or it could be that Nosema has a rigid spore wall for protection, whereas Crithidia does not; the spore wall is a useful protector from abiotic stressors, and it is one of the reasons why American foulbrood is so difficult to manage. ↩︎ - Just because a bee visits a flower it does not mean they pollinate it. In A. vryheidensis, the bees were removing the pollen, rather than “pollinating”, scraping it from the anthers of each flower without making contact with the stigma (where pollen is deposited). Now compare that to the birds who stick their whole head into the flower in order to reach the nectaries: this method ensures the animal makes contact with both the stigmas & anthers, and as they visit multiple plants, lead to pollination. A caveat is that the “sheer abundance” of bees (there are many more honey bees than there birds) can lead to pollination of A. vryheidensis, but this is more by chance rather than intent (whether bees have intent is a question for Aristotle). ↩︎
- The small volume of nectar means it will be readily lost the environment when “unprotected”: protection comes in the form of flower structure (always-open vs selectively-closed, as in roses vs tulips), the microclimate around a flower (vegetation levels, shaded vs exposed blossoms) and the sugar profile: hexose-rich nectars are slower to evaporate than sucrose-rich ones, as sucrose is one molecule, whereas its component hexoses (glucose & fructose) are two molecules; chemists call this a “higher osmolarity”. ↩︎