& shades of green in-between
Last spring, I was leaning over the garden pond, my rubber-gloved hands fumbling around in the water trying to pull up an out-of-action pump. Suddenly, something small and furry began flying at my face, over and over. I flapped it away, only for a second tiny winged body to arrive on the scene, darting back and forth in front of me in loops as though frantically signalling. The utter fury of the first creature, and the sheer desperation of the second, seemed palpable. These were common drone-flies, an important hoverfly pollinator whose appearance mimics the honeybee. Swimming about in the pond, I quickly realised, were drone-fly larvae (the unfortunately named rat-tailed maggots). I was disturbing the drone-flies’ nursery, threatening the welfare of their larval babies. Their emotion seemed tangible. But these were just flies, with microscopic invertebrate brains: was I merely projecting human feelings and motivations onto crudely reflexive insect behaviour?
It seems a deeply ingrained human trait to anthropomorphise the insect world. We sense pleasure and contentment oozing from bumble bees as they buzz drowsily from bloom to bloom. Wasps seem angry and vindictive. Crickets and grasshoppers are rather rude and superior fellows who vanish in a split second just as you bend down to introduce yourself. Except when they are munching on your favourite flowers: then they will hang around to stare back defiantly. Smug box-tree moths love to taunt and flaunt their presence near buxus topiary, positioning themselves where they are just out of reach. Marmalade hoverflies seem full of youthful curiosity, hanging around plants like miniature helicopters, carefully absorbing what other insects are getting up to.
One of the earliest scientists to investigate insect emotions, Charles Henry Turner (1867-1823) was a pioneering American zoologist of African descent.1 Turner, who was committed to overcoming racial barriers in academia, conducted ground-breaking research into invertebrate learning and behaviour, making important contributions to the development of research methods, the investigation of colour and pattern in honey bee vision, and providing what is believed to be the first demonstration of Pavlovian conditioning in an insect. With a total of 71 publications to his name, Turner carried out much of this research whilst working as a high school science teacher with no access to higher institutional laboratory resources. Turner's research provides some of the first evidence that Hymenoptera, which includes bees, wasps, ants and sawflies, are not lower-order machines with behaviour solely governed by reflexes, but have problem-solving abilities, memory and learning skills, and experience feelings, such as excitement.
More recently, there has been a resurgence of interest in insect emotion, with scientists seeking to establish whether invertebrates are sentient. Research suggests that buff-tailed bumblebees exhibit a positive emotion–like state when receiving an unexpected sugary reward.2 On the other hand, it has been reported that honey bees exposed to a simulated predatory attack seem to develop an anxiety-like state and subsequently show biases in decision-making akin to pessimistic thinking.3
Thomas Ings and Lars Chittka studied the effects of a simulated crab spider attack on bumblebee behaviour.4 Crab spiders are a type of non web-building spider that ambush prey, and can change colour to camouflage themselves in flowers. For this experiment, a robotic padded trap installed beneath a life-sized spider model was designed to harmlessly grab a feeding bee and hold it for two seconds before release. Bees quickly learned to avoid flowers with crab spider models, although this took longer if models matched the colour of petals. However, Chittka was struck by long-lasting psychological changes that occurred after the simulated predator attack.5 Bees showed a newly anxious demeanour for 24 hours afterwards, resulting in longer times spent cautiously inspecting flowers before landing. They experienced ‘false alarms’, causing them to reject entirely predator-free flowers. It was, according to Chittka, as if they were ‘seeing ghosts’, bringing to mind the psychiatric research on human patients that suggests many ghost experiences result from traumatic life events: ‘everything outside the person may begin to look spooky’.6
Chittka argues that bees not only have emotion-like states but show profoundly advanced cognitive abilities, enabling them to count, recognise flowers and human faces, use simple tools, solve problems, learn by observing others, and feel pain. They show distinct individual personalities, some being more curious and confident than others, and evidence of metacognition, that is to say, they are aware of what they know. As science provides a new level of understanding about bee sentience, Chittka draws attention to the moral obligation of humankind to further investigate, respect, and guard the welfare of bees and other insects through animal welfare legislation.
Having halted my activities in our pond, responding to the apparently emotionally-charged actions of the drone-flies, I left their larvae to develop undisturbed. Perhaps this was not just the right thing to do on an ecological level but from an insect welfare perspective too. One thing is for sure, the hoverflies had achieved the outcome they wanted: those were two smart little flies.
All images copyright of APPLE PEA FERN SEA unless otherwise indicated below.
Once our pond pump went out of action, drone-flies (Eristalis tenax) must have considered the stagnant pool of water a very promising nursery for their larvae, known as rat-tailed maggots. Perhaps surprisingly, we have never seen frogs or toads eating the larvae.
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It is surely impossible for the gardener not to anthropomorphise the insect world. We sense pleasure and contentment oozing from bumble bees, defiance from plant-munching crickets, and the youthful curiosity of marmalade hoverflies (Episyrphus balteatus). Despite the genial bumblebees of our garden borders, in Beatrix Potter’s The Tale of Mrs Tittlemouse, Babbity Bumble and his friends are portrayed as slightly sinister invaders.
Pioneering zoologist Charles Henry Turner, conducted ground-breaking research into invertebrate learning and behaviour, providing some of the first evidence that Hymenoptera, which includes bees, wasps, ants and sawflies, are not mindlessly governed by reflexes, but have problem-solving abilities, memory and learning skills, and experience feelings, such as excitement.
Lars Chittka argues that bees not only have emotion-like states but show profoundly advanced cognitive abilities, drawing attention to the moral obligation of humankind to further investigate, respect, and guard the welfare of bees and other forms of insect life.
References
1 Charles I Abramson (2009). A Study in Inspiration : Charles Henry Turner (1867-1923) and the investigation of insect behavior. Annual Review of Entomology, 54(1), 343–359.
2 Cwyn Solvi, Luigi Baciadonna, & Lars Chittka (2016). Unexpected rewards induce dopamine-dependent positive emotion-like state changes in bumblebees. Science (American Association for the Advancement of Science), 353(6307), 1529–1531.
3 Melissa Bateson, Suzanne Desire, Sarah E Gartside, & Geraldine A Wright (2011). Agitated honeybees exhibit pessimistic cognitive biases. Current Biology 21(12)1070-3.
4 Thomas Ings & Lars Chittka (2008). Speed-Accuracy tradeoffs and false alarms in bee responses to cryptic predators. Current Biology, 18(19), 1520–1524.
5 Lars Chittka (2022). The Mind of a Bee. Princeton University Press.
6 Sally Squires (1985, October 30). Why people see ghosts. Washington Post. https://www.washingtonpost.com/archive/lifestyle/wellness/1985/10/30/why-people-see-ghosts/98f0442a-0f8f-4d2c-8665-cd4ed00cf44f/
Image Attributions
A URL: https://commons.wikimedia.org/wiki/File:Eristalis_2007-1.jpg
Attribution: Alvesgaspar, CC BY-SA 3.0 <https://creativecommons.org/licenses/by-sa/3.0>, via Wikimedia Commons
B URL: https://commons.wikimedia.org/wiki/File:Hoverfly_(Eristalis_tenax)_female.jpg
Attribution: Charles J. Sharp, CC BY-SA 4.0 <https://creativecommons.org/licenses/by-sa/4.0>, via Wikimedia Commons
C URL: https://commons.wikimedia.org/wiki/File:Eristalis_tenax_auf_Tragopogon_pratensis_01.JPG
Attribution: Uoaei1, CC BY-SA 4.0 <https://creativecommons.org/licenses/by-sa/4.0>, via Wikimedia Commons
D URL: https://en.wikipedia.org/wiki/File:Hoverfly_December_2007-8.jpg
Attribution: Alvesgaspar, CC BY-SA 3.0 <https://creativecommons.org/licenses/by-sa/3.0>, via Wikimedia Commons
E URL: https://commons.wikimedia.org/wiki/File:Mrs_tittlemouse.jpg
Attribution: Beatrix Potter (1866–1943), Public domain, via Wikimedia Commons
F URL: https://commons.wikimedia.org/wiki/File:Charles_Henry_Turner.jpg
Attribution: Unknown photographer, Public domain, via Wikimedia Commons
G URL: https://commons.wikimedia.org/wiki/File:Hymenoptera.jpg
Attribution: These belongs to his respective owners., Public domain, via Wikimedia Commons
H URL: https://commons.wikimedia.org/wiki/File:Sharing_Information.jpg
Attribution: DianitaKartika, CC BY-SA 4.0 <https://creativecommons.org/licenses/by-sa/4.0>, via Wikimedia Commons
I URL: https://commons.wikimedia.org/wiki/File:Nest_of_the_Common_Humble-Bee_Plate_15_Jardine.jpg
Attribution: Sir William Jardine, Public domain, via Wikimedia Commons
Video Links
Lars Chittka, a world authority on the behaviour, cognition, and ecology of bumblebees and honeybees gives a detailed lecture on the Linnean Society YouTube channel https://youtu.be/Iut33k3MHyI
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