Plant Cuttings

This image with the caption “Trigona bees chew through unopened flowers to access pollen” by Katja Schulz is made available under the Creative Commons Attribution 2.0 Generic license.

Flowers and insects have a very long evolutionary history, so much so that there’s a lot of research into the coevolution (John Rafferty & John Thompson) of both groups, much of which examines the role played by insects as pollinators of flowers (Joe Arnett; Shusheng Hu et al. (PNAS 105(1): 240-245, 2008; https://doi.org/10.1073/pnas.0707989105); Steven Johnson & Bruce Anderson (Evo Edu Outreach 3: 32–39, 2010; https://doi.org/10.1007/s12052-009-0192-6); Akira Shimizu et al. (Sci Rep 4, 3988 (2014); https://doi.org/10.1038/srep03988). In performing this pollination service – the transfer of pollen from one flower to another – the insects are – usually* – rewarded by the plant with calory-rich foods such as nectar and pollen (Felix Wäckers, Suitability of (extra-)floral nectar, pollen, and honeydew as insect food sources, In: Plant-Provided Food for Carnivorous Insects: A Protective Mutualism and its Applications (Eds: FL Wäckers et al.), pp. 17 – 74. Cambridge University Press, 2005; https://doi.org/10.1017/CBO9780511542220.003); Susan Nicolson, African Zoology 46(2): 197-204, 2011; doi: 10.1080/15627020.2011.11407495) (but not all of the latter or there’ll be no pollination and no next generation of plants to help fuel the insects of the future…). Indeed, it seems likely that it’s the food reward that’s sought and the pollination is a bonus from the plant’s perspective.

In most cases of flower-insect interaction it’s a mutually beneficial one (Rebecca Reynandez), both organisms benefit from the arrangement. But, as with many human relationships, the possibility exists that one partner will take advantage of the other. Where such possibilities exist, they will be taken, by one ‘chancer’ or another. One such one-sided arrangement is the phenomenon known as nectar robbery [“a foraging behavior used by some organisms that feed on floral nectar, carried out by feeding from holes bitten in flowers, rather than by entering through the flowers’ natural openings”].

Although it wasn’t, the phrase ‘daylight robbery’ could have been invented to describe the activity of bees that steal nectar from flowers [I’m assuming they only engage in this thievery during the hours of daylight]**. In this act, the insects chew a hole into/through the ‘wall’ of a flower to target the nectary-containing region directly, rather than having to thread their proboscis (Rachel Mallinger) down towards the bottom of the flower through a tube that’s lined with pollen-bearing structures.

In nectar-robbing they get the reward without doing the necessary work of pollination/pollen-translocation that would benefit the flower/from one flower to another. Such an arrangement looks like it’s moved from being a mutually-beneficial symbiotic (Emily Osterloff) pollinator-plant relationship, to a non-symbiotic, feeding relationship where only one, the animal, benefits***. Indeed, the punctures in the plant’s tissues could act as entry points for microbes or other pests that could actually harm the plant that may subsequently die, or for other nectar-consuming opportunists to thieve some nectar (‘secondary robbery’ (Joe Boggs)), which is not a fair exchange at all. So, whilst we may consider that behaviour to be imaginative and creative, that crafty bit of pollen-pilfering is not a good example of best beehaviour.

But, some bees have got even lazier than those – comparatively – harder-working, but still nectar-nicking ne’er-do-wells, that steal nectar. In this case, instead of putting in the effort to poke through plant tissues and hope to get at a nectar food reward, they’ve gone straight to another – but freely-accessible – nutritious source of plant-derived food, pollen taken from the bodies of bumblebees that have already done the hard work to collect pollen. This revelation was revealed to me in a science news item by Darren Incorvaia, which reports on the work of Tiziano Londei & Giuliana Marzi (Apidologie 55, 4 (2024); https://doi.org/10.1007/s13592-023-01049-1)****.

Working in the northern Italian region of Liguria (Darren Incorvaia), Londei & Marzi report that the honey bee (Apis mellifera L.) preferred to collect pollen from the red-tailed bumble bee (Bombus lapidarius L.) [for some guidance on how to distinguish honey from bumble bees, see here] rather than directly from flowers. Refining this observation the pair found that this behaviour appeared to be the case in a very specific set of circumstances; when the bumble bees were sufficiently numerous, and when only one species – woolly thistle (Cirsium eriophorum L.) – was in bloom to forage from. At another site where both woolly thistle and Tyrol thistle (Centaurea nigrescens Willd.) were present and flowering, the honey bees foraged on the latter, and the bumble bees kept to the woolly thistle [bees appear to have a particular affinity for thistles (Lorraine). Where there were fewer of the bumble bees present and only woolly thistle as a pollen source, both bee species foraged on the flowers.

It would therefore appear that pollen-robbery is not an ‘obligate’ behaviour or condition for the honey bees, but, rather, is a ‘facul tative’ one, exploited under circumstances when normal pollen-collection – direct from flowers – is avoidable or somehow ‘inappropriate’. In this regard, the honey bees can be considered ‘opportunists’; they’re not obliged to steal pollen from bumble bees, but they have the faculty to do so when opportunity permits.

Additionally, the observation that “the thieves tended to target male bumblebees slightly more than females, as the males appeared less bothered by the pilfering (though even females didn’t react aggressively)” (Darren Incorvaia) gives support to an alternative name for bumble bees as humble bees (here, here, Richard Jones, Katy Malone, and Maria Wheeler-Dubas).

As Londei & Marzi point out, this phenomenon had previously been observed and documented in the USA, by Sebastiāo Laroca & Mark Winston (Journal of the Kansas Entomological Society 51(2): 274-275, 1978; https://www.jstor.org/stable/25083029), Robbin Thorp & Dennis Briggs (Journal of the Kansas Entomological Society 53(1): 166-170, 1980; https://www.jstor.org/stable/25084015), and Robert Jean (Journal of the Kansas Entomological Society 78(2): 172-175, 2005; https://doi.org/10.2317/0406.15.1). Which begs the question of how – and when and where – the Italian bees began this activity. Did they discover it for themselves – independently of the American population? Or did an American bee get blown across the Atlantic Ocean and the Mediterranean Sea and ‘teach’ the Italian insects..?*****

This ‘pollen-theft’ appears to be but one of a whole suite/range of pollen-gathering behaviours, many of which have been examined and categorised by Zachary Portman et al. (Journal of Hymenoptera Research 71: 171-208, 2019; https://doi.org/10.3897/jhr.71.32671). Interestingly, pollen theft doesn’t appear to be mentioned as a pollen-collecting behaviour in Portman et al’s otherwise – seemingly – quite comprehensive review. [For completeness, and to help you increase your word power, this “exploitation interaction” has been termed ‘cleptolecty’ (clepto- meaning thief; -lecty meaning pollen collection) (Thorp & Briggs, 1980).]

Finally, but relatedly, researching the Italian cleptolectic honey bee story, I came across another phenomenon – new to me, but which appears well-known, at least amongst the bee-keeping community – the notion of ‘robber bees’. In this behaviour, honey bees ‘steal’ nectar and/or honey from hives that are not their own (David Cushman; Rusty; Ryan Willingham et al.). Although this theft may be associated with periods when nectar is in short supply, it is still an issue for beekeepers – and the members of the colony that’s affected******. But, in support of the saying that “cheats never prosper”, Karolina Kuszewska & Michal Woyciechowski (Apidologie 45: 537–544, 2014; https://doi.org/10.1007/s13592-014-0267-4) present evidence that individual honey bees engaged in this activity “live shorter lives than foragers under the same cage conditions, and that they are more often and more heavily infected with the intestinal parasite Nosema than foragers are”.

Theft from colonies also happens between colonies of commercial bumble bees (Bombus terrestris), where such activity is classified under the rather inoccuous term ‘drifting’ [“entering a foreign colony”] (Ellen MacKenzie et al., J Insect Behav 34: 334–345, 2021; https://doi.org/10.1007/s10905-021-09790-0) [for a newspaper article on this work, see Sarah Knapton].

All of which is truly a case of [bad pun alert!] bees behiving badly…

* Arguably, the most infamous case of insects not being suitable rewarded for their pollinating services is the phenomenon of pseudocopulation (Hayley Dunning), which superbly subtle sexual subterfuge is practised by several orchids.

** For more on the phenomenon of nectar robbery, see Joe Boggs; Laurie Jackson; Laura Preston; Joan Maloof & David Inouye (Ecology 81: 2651-2661, 2000; https://doi.org/10.1890/0012-9658(2000)081); Rebecca Irwin (Ecology 84: 485-495, 2003; https://doi.org/10.1890/0012-9658(2003)084); Sarah Richardson (Oecologia 139: 246–254, 2004; https://doi.org/10.1007/s00442-004-1504-8); Sandra Rojas-Nossa et al. (Oikos 125: 1044-1055, 2016; https://doi.org/10.1111/oik.02685); Judith Bronstein et al. (Current Opinion in Insect Science 21: 14–18, 2017; https://doi.org/10.1016/j.cois.2017.05.013); Sarah Richman et al. (2021) Front. Ecol. Evol. 9:698137; doi: 10.3389/fevo.2021.698137); and Sailee Sakhalkar et al. (Ecosphere 14 November 2023 e4696; https://doi.org/10.1002/ecs2.4696).

*** I’m no expert on the terminology of these inter-species relationships, but do wonder if nectar-robbery is purely a feeding relationship, a sort of herbivory (Kim Rutledge et al.) with insects solely using the plant’s nectar as a food source (technically known as nectarivory). Or, if this behaviour – by a group of animals that includes true pollinators – is viewed as an extension of that symbiotic relationship spectrum, but, since it’s one where the insect benefits and one assumes that the plant doesn’t suffer harm [apparently, that’s the case for bluebells that get ‘robbed’ (William Morris, Ecology 77(5): 1451-1462, 1996; https://www.jstor.org/stable/2265542)], maybe it should be categorized as commensalism (Emily Osterloff).

However, extending that notion further, maybe the interaction could be classified as a form of parasitism if the plant suffer some harm should other organisms – such as fungi, bacteria or viruses (PA Nazarov et al., Acta Naturae 12(3): 46-59, 2020; doi: 10.32607/actanaturae.11026) – enter the plant through the wound created by the nectar robber and cause disease, etc., or has insufficient energy or resources for its own growth requirements because of the nectar it’s produced that has been stolen.

If one was being hyper-critical, and in light of de Bary’s original definition that defined symbiosis broadly as “the living together [Zusammenlebens] of dissimilar organisms” (WB McDougall, The Plant World 21(10): 250-256, 1918; https://www.jstor.org/stable/43477691) (or “namely, the living together of differently named organisms” (Nathalie Oulhen et al., Symbiosis 69: 131–139, 2016; https://doi.org/10.1007/s13199-016-0409-8)), since the insects don’t live with the plants (they merely visit for a short period of time), it’s not a symbiosis of any kind at all. Countering that overly-strict interpretation is a more modern-day definition of symbiosis “any kind of relationship or interaction between two dissimilar organisms, each of which may receive benefits from their partners that they did not have while living alone (Angelard & Bever, 2013)” avoids the notion of living together. [And, if one was to be ultra-hyper-critical, one should point out that the term symbiosis was apparently coined by Albert Bernhard Frank in 1877, and originally defined as “where two species live on or in one another” (Nat Rev Microbiol 6, 709 (2008); https://doi.org/10.1038/nrmicro2010)] Which all sounds like a discussion topic for a future time, and place (or post..?).

**** For more scicomm items on this phenomenon, see ‘Grand theft pollen’ [this story has been a bit of a boon to headline writers…] here, here, and Darren Incorvaia.

***** Whether this behaviour will take us eventually into territory similar to that of blue tits and their discovery of how to access cream in milk bottles in the 20^th century, and notions of Carl Jung’s collective unconscious or Rupert Sheldrake and morphic resonance, I know not [for more on this, see here, Jane Piirto (Synchronicity and Creativity, In: Encyclopedia of Creativity (Second Edition) (Eds Mark Runco & Steven Pritzker), pp. 409-413, Academic Press, 2011), and Rupert Sheldrake).

****** Honey robbery is not only carried out by honey bees; wasps (Vespula vulgaris, ‘yellow jackets’) may also engage in this activity (Roger Patterson), and there are at least two categories of honey-robbery by honey bees (Roger Patterson).