And How Nectar Assisted the Relationships Between Plants and Pollinators
With the first plants came the first plant-feeding insects, some 300 million years ago in the Carboniferous period. Later emergents were the flowering plants of the late Cretaceous, which had increased angiosperm diversity (“flowering plants”), displacing the then-dominant conifers, ferns, cycads and the long-extinct bennettiales.
A caveat here is the fossil record itself, as there few samples if early fossilised flowers relative to how fast the flowering plant families emerged in this (relatively-short) geologically timeframe. With this in mind, the first pollinators were likely to be beetles, as their fossil evidence predate angiosperms. Beetles have diverse feeding habits (from fungi and spores to non-flowering-pollen-producing plants), all of which predated the angiosperms. Insect flight is what made crosspollination possible, as the aquatic and landlubber species lost much of their pollen grains in transit between flowers.
Flies, wasps, bees, moths and butterflies are the most significant pollinators of present day, and they enter the fossil record en masse in the late Cretaceous alongside the flowering plants. So what did bees do to continue developing this relationship with flowering plants? It’s in the pollen and nectar, read on.
Coevolution, the Reciprocal Interactions Over Evolutionary Time
There are several types of coevolution. The specific (or “pair-wise”) coevolution is when an insect trait is developed in response to that of a plant. Consider an insect’s ability to detoxify a plant poison, which itself is a response to the development of said poison in the tissues of the insect’s target plant. An example: citrus trees become more acidic and unpalatable to stink bugs, the same stink bugs develop the ability to tolerate high acidity and continue feeding on citrus until the plant comes up with something new. This gives the “evolutionary arms race” between eater and eaten, predator and prey.
Another mode is diffuse (or “guild”) coevolution, which describes reciprocal evolutionary changes among groups rather than pairs of species. A bee-related example would be the buzz pollination requirement of plants like tomatoes – the anthers do not release pollen unless the flower is “vibrated” at a specific frequency. Bumble bees (Bombus spp.) and blue-banded bees (Amegllia spp.) started doing just that, and over time had exclusive access to plants with poricidal anthers like tomatoes today1.
The issue with diffuse coevolution is that it can only be assigned retrospectively following very (very, very ) careful observations due to many overlapping variables. Consider flowers with deep tubules whose nectaries are located deep within. They would require a fly or moth (or hummingbird) with a probiscis of appropriate length to reach inside and collect the sugary reward. It’s not easy to isolate this trait as having coevolved in response to repeated interactions with one of the pollinators listed above as these “community level” interactions are complex – was it the fly or the moth or the hummingbird that led to this coevolution?
Internal & External Pollen Transport
External pollen transport is done either through the finely branched hairs on a bee’s body (“scopae”, most abundant on the abdominal region, hence “hairy abdominal scopae”) or flattened plates on their hind legs, termed “pollen baskets”, most common in the social bees (honey bees, bumble bees). The most specialised apparatus for pollen carrying is via the internal crop, in the same organ they use for transporting nectar (their “honey stomach”), and this has been the traditional hypothesis first mentioned in 1883 (Muller’s book “the Fertilisation of Flowers”).
Molecular studies shifted the origins of pollen transport so that external transport came first- the first “protobee” would have carried pollen on her unspecialised body hairs, and only later did they converge into abdominal or hind leg scopae we see today. External pollen transport can be further broken down into three modes: transported completely dry, completely moist, or glazed, where moist pollen is packed on top of dry pollen.
Recent work from Portman disagrees with external transport as having come first, and it is to this that we turn to next.
Steps Involved in the Origins of & Evolution of Pollen Transport
Extracted from Portman, 2021
- Crop transport represents the original form of pollen transport and evolved from pollen feeding behaviour. Bees consumed pollen by nibbling with the mouthparts and by drawing a pollen-covered foreleg through the mouthparts.
- The next stage of pollen transport evolution was the accumulation of pollen on the venter [the abdomen]. The accumulated pollen was then picked up by the foreleg and brought forward to the mouthparts and consumed by drawing the foreleg through the mouthparts.
- Next, external moist pollen transport evolved from internal transport, likely due to leftover pollen becoming stuck to the hind leg rather than completely groomed off.
- External dry and glazed transport evolved from external moist transport in parallel with a development of the scopal hairs, following an earlier hypothesis by Portman and Tepedino
- This hypothesis states that moist pollen transport came first, followed by glazed (part dry part moist) or purely dried pollen transport, based on studies on two distantly-related bee genera: Perdita (Andrenidae, mining bees) and Hesperapis (family Melittidae), suggesting that they switched from “moist to dry or glazed pollen transport due to the adhesive properties of pollen grains” (Portman and Tepedino, 2017).
- Finally, in various lineages that transport dry pollen, the scopal hairs expanded and migrated from the hind legs towards the midline of the body. In other lineages, crop transport secondarily evolved.
Under Discussion: Did Branched Hairs for External Pollen Transport Come First?
Previously, it was thought that internal crop carrying was the ancestral pollen transportation method based on observations from Colletidae family (plasterer bees; e.g. Jander 1976). As molecular biology advanced, there came support for Mellitdae rather than Colletidae as the first bee family, and none of the species in this family transported pollen internally (Reviewed [or “suggested”?] in Danforth et al., 2013). Now further advances are declaring that the original hypothesis was correct, and it is internal, not external transport that comes first (Portman, 2021).
Portman argues that only a couple of minor changes are required to transition from pollen feeding to external transport. As the bee foragers, it accumulates pollen on its body (“specialised patch of apically hooked hairs on the venter of the thorax” in the mining bee Perdita tortifoliae). This pollen is then transferred from the body to the mouthparts and moistened, then transferred back to the hind legs for collection.
The first three steps (foraging, accumulation and taking to the mouthparts) are shared between the internal & external pollen transport methods. Where they deviate is that in internal transport, pollen is consumed and excess amounts are brushed off, whereas in external transport it is moistened and sent to the hind legs for packing.
“The steps between pollen-feeding and external pollen transport require few to no transition steps. One could imagine a gradual change where internal pollen transport in the crop slowly changes over to external moist transport.” – Portman, 2021. From this perspective, successive generations of bees could end up with specialised, hairier bodies as it gives them a fitness advantage in capturing pollen. As the now-hairier bee is able to capture more pollen per flower, her foraging efficiency increased and thus her chances of survival & reproduction.
The Development of Pollen Baskets Allowed for Increased Foraging
The pollen-basket bees are termed “corbiculates” and this group consist of honey bees (Apis spp..), bumble bees (Bombus spp..) stingless bees (tribe Meliponini) and orchid bees (tribe Euglossini), all located on their hindlegs. Martins and colleagues suggest that pollen baskets emerged from a shared common ancestor with the oil collecting bees of the Centris genus Martins et al., 2014). These bees already had the pre-existing conditions for pollen baskets, those of a broad, flat plate on the bottom of their hindlegs (“basitarsi”), which likely aided the transition to pollen baskets.
Rather than having pollen transported on their abdominal scopae or diffused around their bodies, the corbiculae enabled bees to gather much (much, much) more pollen per foraging trip. This became advantageous for colony living, as the pollen can be compacted in the hind legs (either dry, moist or glazed as in above) and then transferred back to the hive.
The compaction reduced pollen loss during flight (moreso when it was “sticky”, i.e. glazed or moist) and did not interfere with the bee’s aerodynamics- confining your cargo to two symmetrical locations made for smoother flight as opposed to scattered pollen clumps all over the body. Further, pollen baskets worked best with floral consistency – if the pollen type is from the same flower, then their packing and transport behaviours will be predictable – this benefits both bee and plant, as it ensures the foraging bee will be “faithful” in the pollen transfer, as opposed to foraging from every plant in sight.
Pollen Wasps Only Carry Pollen Internally
There are two primary groups of pollen wasps: the masarid pollen wasps (family Vespoidea), and the genus Krombeinalictus (family Crabronidae). More is known about the former than the latter, and their lifestyle is similar to that of our protobee, making them a viable study model; if it works for thee, it works for bee. Pollen wasps (and wasps in general) lack body hairs so all transport is done internally, stemming from an ancestral pollen-feeding behaviour; not all pollen is digested, and some is regurgitated or passed through the digestive tract.
As the wasps feed on pollen, it accumulates on its body and some grains stick to the various hair patches on their body or antennae, whilst others stick to their legs. Both sexes consume pollen for their own nutritional needs (with females taking it back to the nest for broodrearing), and some wasp species gather pollen in a similar manner to bees (in this case, Perdita tortifoliae).
You may be thinking “so what, it’s all pollen transport” and you are correct. What Portman suggests is that these are viable ancestral forms of pollen transport and that over evolutionary time, bees went from internally transporting the pollen that stuck to their abdomen to external transport, whilst others (the masarid pollen wasps) continued performing internal transports (Portman, 2021).
Plants Produced Pollen Long Before They Did Nectar
Plants produce pollen for the purpose of reproduction; it predated the first animals and early pollen transport was either passive or by wind (“anemophily”). Nectar appeared later and was produced by plant as a “sugary reward” (as in, “incentive”) to attract pollinators. While it is economically costly to produce, it is “cheaper” for the plant to invest in part nectar-part pollen production if it means that the nectar will lead to more effective pollination by a visiting pollinator.
Pollen production is expensive as it contains proteins, lipids & micronutrients. If a plant where to offer say, “sweetened pollen”, it would be unsuccessful on three fronts:
- Pollen grains are more difficult to digest by the pollinator, relative to nectar (loss for the pollinator).
- The need for pollen in adult pollinators is smaller than the need for nectar, and excessive pollen collection, whether deliberate or incidental, is discarded by your average bee (not so much in social species who will store it in their hives).
- To reframe: You can stop for a sugary drink anytime during your flight (nectar), however it takes preparation and genuine need to stop for a full-course, cruelty-free, plant-based meal complete with all the essential vitamins, minerals, lipids, proteins, antioxidants, phytochemicals, shymtochemcials, fibre… you get the point (pollen).
- Every grain consumed by a pollinator is a gamete lost (for the plant).
Nectar as a Reward Mechanism in Exchange for Flower Pollination
Nectar can be altered by the plant in terms of sugar concentration, volume, chemical additives (amino acids, secondary metabolites etc.), all with the purposes of maximising pollinator stay while minimising the energetic costs to the plant. Doing this consistently enough builds habits and these habits will benefit both thee and bee2.
Even though the plant-pollinator relationship is a net positive, the evolutionary arms race means that as pollinators develop more sophisticated pollen-handling structures, the chances of “unfair players” increased – those animals that gather pollen without spreading it to the stamens of plants. Beneficial for bee, not for thee. Nectar addressed this issue by “paying” bees to prolong flower visitations to maximise the time spent at each blossom (and subsequent pollination chances).
Nectar & Pollen Thieves, and Plant Adaptations Against Them
Plants invest energy in ensuring their reproduction. So what do you make of those bees that can “rob” their efforts without pollination in return? A nectar thief is one that access the nectaries by piercing the floral tissue. Carpenter bees are the usual suspects, their strong jaws makes it possible for them to bore a hole straight to the nectaries. That same hole can be used by another pollinator who is not normally a thief, however they will not let an opportunity go to waste – ants and flies are such examples.
A pollen thief doesn’t “break in” as nectar ones do, instead they excessively groom themselves, pack the majority of pollen for transport, or are able to harvest pollen without contacting the stigma (the female part of the plant).
Plant adaptations against nectar thieves include:
- Morphological barriers, like long, narrow corolla tubes, deep nectar spurs or narrow entrances matching pollinator morphology. Examples:
- Aquilegia spp. (columbines): long nectar spurs restrict access to hawkmoths or long-tongued bees
- Lonicera spp. (honeysuckles): deep tubular corollas select for long-tongued pollinators
- Digitalis purpurea (foxglove): deep bell-shaped corolla limits nectar access
- Reward placement, where the nectaries are nectar positioned behind reproductive organs, forcing contact with anthers/stigma during access. Examples:
- Beardtongues; Penstemon spp.: nectar chamber behind stamensDelphinium spp.: nectar concealed behind spurred sepals and reproductive organs
- Borage family (Echium spp.): nectar access requires brushing past anthers
- Thickened corollas & fibrous tissue resistant to piercing, as in rhododendrons, Japanese camillas, and the hardy fuchsias
- Nectar secretion timed to legitimate pollinator activity, or with nocturnal/crepuscular nectar partitioning.
- An example are the Agave species, who provide nocturnal nectar for bats, or evening primrose, which blooms at night to attract hawkmoths
- Chemical deterrents: alkaloids, phenolics, terpenoids in nectar with dose-dependent effects that tolerated by specialists but detested by generalists and thieves… note that honey bees are generally well-tolerant of these things.
- Some examples include nicotine from plants (yum!) or limonoids and alkaloids in citrus species (in response to our stink bug pest from the introduction).
With pollen, it is similar, concealing pollens, gradual release, pollen traps, as well as chemical defences. The examples here will be brief:
- Pisum spp. and Lupinius spp. keel (“capsize”) flowers to conceal anthers, hiding pollen inside structures inaccessible to casual foragers.
- Tomatoes and blueberries preferably release pollen when buzz pollinated by bees with the ability to vibrate their muscles (e.g. bumble bees) in lieu of “scrabbling” like honey bees.
- Hibiscus flowers gradually expose pollen along the staminal column, as an adaptation to prevent complete robbery in a single trip.
- Milkweeds have sticky pollen that attaches to the legs of a pollinator, this is an area that’s difficult to groom, and as the insect visits multiple flowers, their legs are more likely to make contact with the stamens and facilitate pollination.
Vulture Bees: a Re-Reversal into Carnivory
I end with a description of the “vulture bees”, those bees who use animal flesh rather than pollen for their protein needs. Initially it was though that they only foraged on carrion for their (Camargo & Roubik, 1991), and later work from Maetus & Noll observed them hunting for live social wasp larvae (Mateus & Noll, 2004). The gathered meat is mixed with honey-like substances (fruit juices and extrafloral nectaries [sugars secreted from leaves or stems rather than the flower bud]), and stored for ~14 days in wax pots where microbial decomposition of the flesh takes place. Once complete, this non-vegetarian bee bread is a viscous substance that is likened to royal jelly.
These stingless bees are found in South America and belong to the Trigona hypogea group: T. hypogea, T. necrophaga, and T. crassipes. Their scouting and hunting of abandoned wasp nests (see image below) gives them a clean, & easily digestible protein source that sits undefended (they compete with vertebrates and other larger animals for carrion). Further, their flight makes them faster at locating a nest than ants do.
How could this have come about? I leave you with Mateus & Noll: “Basal hymenopterans are vegetarians. This life-history trait gave way to carnivory in the form of parasitoidism. In the bees, we observe a return to exclusive vegetarianism, a reversal to the primitive state. In this context, T. hypogea represents a remarkable re-reversal to carnivory.” (Mateus & Noll, 2004).
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Footnotes
- I’m hesitant to include this example because of its complexity. Buzz-pollinating bees can still access flowers that do not require buzz pollination, however if the development of this trait is viewed in response to “intense pollinator competition” by a group of bees and a response to “how do I stop pollen theft by insects?” by a group of plants, then labelling buzz pollination as “diffuse coevolution” in response is reasonable. ↩︎
- Some plants have an advantage of being favoured by pollinators over others depending on the pollinator’s condition: secondary plant metabolites in black locust and sunflower nectar have antimicrobial properties, and pollinators will preferably forage on such plants when they are diseased (in this case it was honey bee colonies infected with American & European Foulbrood diseases; Erler et al., 2014). ↩︎