Benign delinquents

By Athayde Tonhasca

Christian Konrad Sprengel (1750-1816) is not widely known nowadays, but the German teacher, naturalist and theologian was a pioneer in recognising flowers as lures to insects. Sprengel made significant contributions to our understanding of the role played by insects in plant fertilization, although his writings, published in German, were mostly ignored outside Germany (which is a common fate in the Anglo-centric scientific world). Even still, Sprengel’s discoveries were acknowledged by Darwin in his own work with plants.

A page of Sprengel’s Das entdeckte Geheimniss der Natur im Bau und in der Befruchtung der Blumen (‘The secret of nature discovered in the structure and pollination of flowers’), 1793 © Uwe Thobae, Wikimedia Commons.

Among many novel contributions, Sprengel recorded the ‘outrage against a flower’ played by some bumble bees; they perforate the base of a flower to get access to its nectar, bypassing its opening. From the plant’s perspective, this is cheating. A bee that avoids the flower’s reproductive parts may not pollinate it: the metabolically expensive nectar could be for nothing. This behaviour is known as nectar robbery, a term that reflects a sympathetic bias towards plants; after all, bees – and other insects and some birds as well – are just getting a resource that would be inaccessible otherwise. Most robbed flowers have tubular corollas or nectar spurs (hollow extensions that contains nectar-producing organs) which are out of reach for many visitors, especially bees with short tongues. You can watch them in the act here.

Nectar spurs on Aquilegia formosa; not reachable by traditional means © Daniel Schwen, Wikimedia Commons.

It has been long assumed, reasonably, that primary nectar robbers (those that perforate the flower to access nectar) and secondary nectar robbers (species that take advantage of existing perforations), are bad: ‘all plants must suffer in some degree when bees obtain their nectar in a felonious manner by biting holes through the corolla’ (Darwin, 1872). Indeed, robbers may reduce the availability of nectar to conventional flower visitors, therefore affecting plants’ reproductive success. Robbers may also destroy floral structures while in the act of breaking in.

A buff-tailed bumble bee (Bombus terrestris) pilfering nectar © Alvesgaspar, Wikimedia Commons.

In Brazil’s Atlantic Forest, the understory shrub Besleria longimucronata is pollinated by the reddish hermit (Phaethornis ruber) and violet-capped woodnymph (Thalurania glaucopis) hummingbirds – that is, if the stingless bee Trigona spinipes is not around. Despite lacking a sting, this bee is quite aggressive, pursuing and biting intruders with its sharp teeth, so that it can perforate the flowers and take their nectar at leisure. Those hummingbirds that are not driven away avoid the nectar-depleted flowers; even worse for the plant, some hummingbird individuals slip into a criminal life themselves and become secondary robbers, taking advantage of the holes created by the bees. As a consequence of the robber’s direct and indirect actions, the shrub suffers a reduction in seed production (Bergamo & Sazima, 2018). Trigona spp. are notorious nectar rustlers throughout the Neotropical region, damaging many wild plants and crops in varying degrees. 

A Besleria sp. shrub (art by Louis van Houtte), its violet-capped woodnymph pollinator (©
Dario Sanches), and the nectar robber T. spinipes (© José Reynaldo da Fonseca), Wikimedia Commons.

But as is invariably the case in biology, things are more nuanced. Bees tend to stick around patches of rewarding flowers to save energy and forage more efficiently. But if flowers are low in nectar because of robbing, bees are forced to fly longer distances to get what they need. Also, they often spend less time in a given flower and visit more flowers per unit of time to compensate for lower nectar volume. All this shuffling about has a positive outcome for plants: more flowers are visited, more pollen is deposited on stigmas, and outcrossing (mating of unrelated individuals) is more frequent: the end result is increased reproduction and fitness. 

Some of these effects were elegantly demonstrated by Mayer et al. (2014) in experiments with potted aconite or monkshood (Aconitum napellus lusitanicum). This endangered herb is pollinated by the common carder bee (Bombus pascuorum), and often robbed by the European honey bee (Apis mellifera). The researchers simulated nectar robbing by removing nectaries from some flowers and estimated pollen dispersal by dabbing anthers with fluorescent dye, a pollen surrogate, which was subsequently detected in stigmas collected from plants placed at some distance from the source. The results: bumble bees visited fewer flowers per plant and spent less time per flower. Also, fluorescent dye from patches with robbed flowers was dispersed over larger distances when compared to dye from control plants that had not been artificially robbed. 

A bumble bee making way among the petals of an aconite to get access to its nectar © Franz van Duns, Wikimedia Commons.

And robbers often do more than rob. In northwest Spain, the hairy-footed flower bee (Anthophora plumipes) is the main pollinator of kidney vetch (Anthyllis vulneraria vulgaris), but muggers interfere in this relationship: the buff-tailed (B. terrestris) and the heath (B. jonellus) bumble bees may purloin over 3/4 of all kidney vetch flowers. Despite this rampage, robbed flowers have a higher probability of setting fruit than intact flowers. It turns out that robbers are forced to trample all over the plant’s capitulum (an inflorescence of closely packed flowers), touching anthers and stigmas during the act of thievery, pollinating the flowers (Navarro, 2000).  

The heath bumble bee, a nectar robber, stomps around a kidney vetch capitulum, pollinating the flowers © Arnstein Staverløkk and Ivar Leidus, respectively. Wikimedia Commons.

Other studies have confirmed the pollination role of nectar robbers, such as the case of the fuzzy-horned (B. mixtus) and frigid (B. frigidus) bumble bees when visiting tall bluebells (Mertensia paniculata) in Alaska. These two bees pollinate flowers during their early stages of development, when pollen is plentiful, but shift to nectar robbing when nectar becomes abundant later on. But this is not only about a change of diet preferences: older flowers to be robbed of their nectar attract pollinators to young flowers nearby, which means that nectar pilfering aids the pollination of tall bluebells (Morris, 1996).

Tall bluebell flowers are pollinated then robbed, with a positive outcome for the plant © Walter Siegmund, Wikimedia Commons.

Sprengel labelled nectar robbing an ‘outrage against a flower’ and Darwin considered it ‘a felony’, but there’s more to it than meets the eye. Thorough investigations have shown that in some cases flower larceny reduces plant reproduction and fitness, but there are many instances of no ill effects on plants, or even beneficial outcomes. It all depends on flower and robber morphologies, insect behaviour, flower density, how much nectar is available, how much of it is taken away, and so on. 

‘Robbery’ sounds like a wrench thrown in the mutualistic relationship between plants and pollinators, but the phenomenon is way too common and widespread to be considered an anomaly. And like many other natural events, first impressions can be deceiving: the sight of a flower damaged by a rough visitor is not necessarily a harbinger of harm. 

Flowers with punctured corollas, indicating nectar robbing. This could be bad, neutral or good for the plant © Raju Kasambe, Wikimedia Commons.

A rattling good tale

When it comes to creating a meadow you need allies, and they don’t come much more reliable than yellow rattle.  Rhinanthus minor, to roll out the scientific name, is one of those plants, like kidney vetch, red clover and common knapweed, which is a staple of meadows and an absolute boon for pollinators. And in the case of yellow rattle’s its value extends beyond nectar and pollen.

Now if I told you yellow rattle is a parasite you might recoil, but you should resist; not all parasites are bad news.  Yellow rattle is a point in case.

Yellow rattle is what botanists refer to as a hemiparasitic plant. The ‘charge’ laid at its door is that it steals nutrients from surrounding grass roots. How does it do this?  It can send out roots of its own which in turn invade the roots of neighbouring grasses, hence the occasional reference to ‘vampire’ behaviour. As you can imagine this isn’t great for those unsuspecting grasses which will, as a result, experience a loss in height and vigour. 

With the advantage switched from grasses to yellow rattle, other less dominant wildflowers seize the moment and move in to exploit the emerging opportunity. It’s this ability to help encourage floral diversity which earns yellow rattle the charming nickname of the ‘meadow maker’.  

Greater Yellow-rattle (Rhinanthus angustifolius) growing on the Battleby meadow

That’s a name they would approve of in the environment team at East Dunbartonshire Council.  They have increasingly sown yellow rattle in early autumn on areas they have carefully scarified.  This is followed up with both the seeds of other species and the direct planting of tiny plants of different species.  The yellow ‘meadow magician’ is however is the star ingredient within the floral recipe. A key point in the years thereafter is making sure that mowing is planned for late summer, carefully timed to take place after the yellow rattle and wildflower plants have shed their seeds.

Relaxed mowing regimes and delayed cuts fit neatly with another East Dunbartonshire Council tactic. They’ve identified a reduction in the rotations for grass-cutting as an intervention which they can easily follow, whilst simultaneously gaining biodiversity benefits. Ever adaptable, when the council found they simply couldn’t resource creating any new perennial meadows in 2022 they compensated by sowing annual pictorial flower meadows on roundabouts and along transport corridors whilst protecting ongoing perennial meadow management. This entailed adopting a welcome cut-and-bale strategy for all of their meadow sites. The introduction of soft-track machinery on the wettest areas was another welcome advance, both for the soil structure and aesthetically.

That’s our mechanical cue to return to ‘nature’s lawnmower’, yellow rattle.

Yellow rattle (Rhinanthus minor) seedhead

Yellow rattle is an intriguing name. Why ‘rattle’ you might ask? The answer is remarkably logical, for when it sets seed it makes the sound of a rattle when your brush against the seed pods. Indeed few plants have such a range of fascinating descriptive names. Penny rattle, rattle basket, hay rattle and rattle grass are all ancient local names that capture the essence of the sound those dry seed pods make. In some areas the pods themselves were known as dog’s pennies as they resembled rough coins and formed part of childhood games. 

In Gaelic the common name for yellow rattle is bodach nan claigeann, literally ‘old man of the skulls’. It is also referred to as gleadhran ‘rattling one’ and modhalan buidhe ‘yellow humble one’.

There are many delights with yellow rattle and they aren’t confined to the list of charming names. It holds its nectar quite deep and is thus popular amongst long-tongued bumblebees. Fascinating studies have revealed that yellow rattle is also susceptible to nectar robbing where shorter-tongued bumblebees simply gnaw through the flower to cleverly reach the otherwise unobtainable nectar supply.

What more could you want when it comes to plant gazing? What with ‘vampires’, ‘magicians’ and ‘nectar robbing’ that’s surely more intrigue than most plants offer.  

The best time to see yellow rattle in Scotland is between May and July.