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.
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.
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.
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.
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.
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).
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).
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.