By Vidya Rajan, Columnist, The Times
Expose a young mouse mother to a stressful stimulus – say a sudden loud noise – and she may eat her own pups. Rough for the young. But what turns a mother from nurture to cannibalism in an instant? Bees will also eat their young – younger larvae first – under some circumstances ([1]). And humans too. Why do they do it?
Cannibalism, which is the consumption of one species by another member of the same species, has been observed in over 3,000 types of organisms ([2]). A number of benefits accrue through this practice: elimination of competition, enhanced nutrition, and “lifeboat mechanism” – the enhanced survival of reproductive-aged adults when resources are limiting. But drawbacks also exist, primarily the acquisition of parasites through consumption of infected flesh. A freshwater shrimp species, Gammarus duebeni celticus, native to Ireland, shows different behaviors in the presence or absence of a spore-forming parasite called Pleistophora mulleri. When juvenile shrimp were placed in a container with uninfected and infected adult shrimp, the infected adults tucked in with gusto, cannibalizing the juvenile shrimp. The simple explanation is that parasitic infection draws more resources from the host, and the host needs to eat more to compensate. But there was an added twist. Uninfected adult shrimp, when given the choice, cannibalized uninfected juveniles over infected juveniles. But infected adults were indiscriminate in their consumption of infected vs. uninfected juveniles. This second observation may reflect an avoidance strategy by uninfected adults to prevent infection, the authors of the study surmise ([3]). How the adults identify which shrimp is infected or not is not clear, but it may be that infected shrimp are physically smaller or have odor or behavioral differences.
Many animals do not shrink from eating members of their own biological class. Insects eat other insects; fish predate other fish; birds other birds; mammals, others of their class of milk-producing, fur-bearing compatriots – when was the last time you ate a hamburger? – but there is a boundary. Class is one thing; species is another. Curiously enough, the reason may be more practical and less empathetic than once thought. Cannibalism of one’s specific compatriots does make a modicum of sense in an ecosystem where food has existential value. The most memorable example of human cannibalism occurred when a plane carrying the Uruguayan rugby team crashed on the border of Argentina and Chile in 1972 ([4]). Of the 45 passengers, 27 survived the initial crash. The survivors, trapped in the high Andes, survived initially on what they found on the plane. But then the food ran out. Faced with starvation on day 9, they faced the previously unimaginable. They tore open the shirt of a team mate and sliced strips of flesh. They laid the strips out. Then they steeled themselves and did the unthinkable: they ate the strips. After 72 days, the 16 passengers who remained alive were rescued. Their story was described in the book and movie titled Alive. But the struggle to eat the bodies of their friends was their biggest trauma.
The problem is that disease can be transmitted by eating the same species. Disease avoidance is probably the reason that humans do not consume other humans, because there is an example of human cannibalism in the absence of food deprivation. Before the 1950s, when an elder in the tribe of the Fore people from Papua New Guinea died, the women and children ate the brains and the men the bodies as homage ([5]). The practice no longer exists, however, it spread a prion disease called kuru, which is similar to a degenerative brain disease called Creutzfeldt-Jakob. Prions are also the causative agent of bovine spongiform encephalitis (BSE, mad cow disease), scrapie in sheep, (and Creutzfeldt-Jakob disease in humans). In fact, it was the action of feeding ground-up meal from scrapie-diseased sheep to cows, or from cows to other cows ([6]). Yes, you read that right, and it’s a long and part of a nasty story of what goes on in some livestock operations that caused the prion to cross the species barrier from sheep into cows to cause mad cow disease. Diseased sheep scraped their fleece off, presumably trying to relieve an itch. Cows simply seemed crazy. Eating diseased cow parts eventually caused the disease to cross the species barrier into humans. Anyone who lived in England during the “mad cow years” of the 1990s-early 2000s is prohibited from giving blood in the United States due to the danger of having eaten infected beef and incubating the long-term disease inside themselves. There is no test yet for incubators of mad cow disease in cows or humans.
On to bees. Sometimes dismembered larval corpses are seen on hive entrance boards – what’s going on? Housekeeping, apparently. Posada-Flores et. al (2021) say that “cannibalism is an essential part of social organization and colony-level hygiene” ([7]). Experimental evidence for larval cannibalism was seen, 1. When worker-laid larvae, particularly those laid in drone cells were being cleared out by other workers; 2. When pollen stores were inadequate to feed the brood; and 3. When hygienic behaviors are stimulated by the presence of deformed wing virus (DFW). Let me just step back and slow down a little and review the three conditions.
For condition number 1: When a hive is out of whack, such as if a queen dies or the colony gets so large that queen pheromone is diluted, some worker ovaries can mature, and they can start laying eggs. Being unmated, they are capable of only laying haploid (drone) eggs. But there is also – ahem – a matter of svelteness. The queen has a long and slender abdomen, but laying workers’ abdomens are stouter and shorter, and so they have less trouble laying in the wider drone cells. Workers can presumably sense queen eggs (or diploid eggs) from worker eggs (haploid eggs). In any case, there is less damage to the colony if the workers cannibalized an occasional legitimate drone egg laid by the queen than if legitimate queen-laid diploid eggs destined to become workers was destroyed.
Condition number 2: Imagine a fabulous spring flow. The weather is lovely, and the foragers are hauling it in by the bucketful, and doing their enthusiastic GPS dances. The queen is laying gangbusters. All of a sudden, the weather turns vicious. Rain, snow, sleet. The pollen stores inside the hive were dwindling anyway because everyone was so focused on bringing in nectar, but now the nurse bees have cleaned out the bee bread. What to do. It’s all about economics: minimize losses and consolidate investment. Eggs do not need to be fed. They are left alone. The capped larvae do not need feeding and additionally, they will be needed when the weather lifts. They are spared. That leaves uncapped brood. The oldest uncapped brood (6-9 days) have already consumed substantial nutrition and all that investment would be lost by killing them. So the younger brood (3-5 days old), which have not yet received much food are targeted for providing the protein that will keep the older larvae alive until conditions improve.
Condition number 3: Hygienic behavior, which is when workers seek out infected or unwell larvae and remove them from the hive (presumably as a way to limit the spread of disease) is typically lauded. But wouldn’t you know, it comes back to bite them hard on the butt. Posada-Flores et al. (2021) conducted an experiment with honeybee larvae injected with deformed wing virus (DWV) that was tagged with green fluorescent protein (GFP) as a way to distinguish it from wild DFW. They put varroa mites on these GFP–DWV infected larvae and then infected new larvae with the varroa which had acquired the virus by feeding on the injected larvae. Then they set hygienic workers loose and the workers cleaned out the DWV infected larvae. The team then found (as expected) that varroa spread DWV to other larvae, but (unexpectedly) that the workers spread it among themselves by trophallaxis! Figure 1 from the paper summarizes the dissemination of GFP–DWV in the experiment.
Figure 1: Model of DWV circulation in Varroa mite-infested Varroa Sensitive Hygienic (VSH) colonies. Varroa transmission – blue arrows, cannibalism-trophallaxis transmission – red arrows. Block arrows show possible evolutionary pressures which on Varroa and cannibalism-trophallaxis transmission routes impose on DWV virulence. Figure and legend reproduced from Posada-Flores et al. (2021) under Fair Use copyright law.
After reading all the research, my biggest question was: How do bees cannibalize? After all, they have sucking mouthparts, not teeth to tear and chew. The sucking part is easy to understand. Like a cowboy who sings cowboy songs, under their hard exterior, insects have a sappy interior. Their organs float in a liquid called hemolymph which takes the place of circulation. To tear the body open then suck up the liquid inside is not unlike sucking nectar from a flower. Then again, the first paper to discuss cannibalism ([8]) refers to bees “eating” larvae so perhaps they are also able to? James E. Tew explores further this in an article in Bee Culture ([9]). It seems bees can regurgitate digestive enzymes into the cell and then suck up the digestate. And then there is another way: Back in 1916, N.E. McIndoo, Ph.D., of the Bureau of Entomology, equipped himself with a pair of binoculars and set to watching bees eat. On page 40, McIndoo writes “While watching a bee eat, it is easily observed by using a pair of binoculars that the mentum (fig. 10, Mt) may be moved in three directions.” This manipulation allows small pieces to be ingested and swallowed.” He follows it up with a beautiful diagram of the mouthparts of a honeybee (reproduced below.) Hurrah for McIndoo, his binoculars, his immense patience and his extraordinary drawing skills! Bees can suck up liquids but also eat very small bits.
Figure 2: Diagram of the mouth-parts of a worker honey bee. Figure reproduced from reference [10] under Fair Use copyright law.
Check your 23 and Me genome readout. If you have valine in the prion gene, you are protected from degenerative brain diseases.
But don’t check too deeply into your ancestors’ food pantry.
[1]. Honey Bee Obscura Podcast. (2023). What’s This About Bees Eating Their Young? (120) | Honey B…. [online] Available at: https://www.honeybeeobscura.com/whats-this-about-bees-eating-their-young-120/ [Accessed 17 Dec. 2023].
[2]. Bunke, M., Alexander, M.E., Dick, J.T.A., Hatcher, M.J., Paterson, R. and Dunn, A.M. (2015). Eaten alive: cannibalism is enhanced by parasites. Royal Society Open Science, 2(3), p.140369. doi: https://doi.org/10.1098/rsos.140369
[3]. Magazine, S. and Blakemore, E. (n.d.). Parasites Linked to Cannibalism. [online] Smithsonian Magazine. Available at: https://www.smithsonianmag.com/smart-news/parasites-linked-cannibalism-180954615/ [Accessed 17 Dec. 2023].
[4]. Bever, L. (2016). Cannibalism: Survivor of the 1972 Andes plane crash describes the ‘terrible’ decision he had to make to stay alive. The Independent. [online] 25 Feb. Available at: https://www.independent.co.uk/news/world/americas/cannibalism-andes-plane-crash-1972-survivors-terrible-decision-stay-alive-a6895781.html
[5]. Kaplan, S. (2016). How a tribe who ate their dead relative’s brains can help us understand Alzheimer’s. The Independent. [online] 12 Apr. Available at: https://www.independent.co.uk/life-style/health-and-families/how-eating-human-brains-protected-a-papua-new-guinea-tribe-from-brain-disease-a6980176.html
[6]. Wikipedia Contributors (2019). Bovine spongiform encephalopathy. [online] Wikipedia. Available at: https://en.wikipedia.org/wiki/Bovine_spongiform_encephalopathy
[7]. Posada-Florez, F., Lamas, Z.S., Hawthorne, D.J. et al. Pupal cannibalism by worker honey bees contributes to the spread of deformed wing virus. Sci Rep 11, 8989 (2021). https://doi.org/10.1038/s41598-021-88649-y
[8]. Schmickl, T. and Crailsheim, K., 2001. Cannibalism and early capping: strategy of honeybee colonies in times of experimental pollen shortages. Journal of Comparative Physiology A, 187, pp.541-547. PDF available at: https://www.academia.edu/download/47449732/Cannibalism_and_early_capping_strategy_o20160723-17606-4h5k73.pdf
[9]. Tew, J.E. (2023). Honey Bee Cannibalism and some other quirks of our beloved bees. Bee Culture. [online] Available at: https://www.beeculture.com/honey-bee-cannibalism/ [Accessed 17 Dec. 2023].
[10]. McIndoo, N.E., 1916. The sense organs on the mouth-parts of the honey bee (Vol. 65, No. 14). Smithsonian Institution. PDF available at: https://repository.si.edu/bitstream/handle/10088/23540/SMC_65_McIndoo_1916_14_1-55.pdf?sequence=1&isAllowed=y
[11]. Mead, S., Stumpf, M.P.H., Whitfield, J., Beck, J.A., Poulter, M., Campbell, T., Uphill, J.B., Goldstein, D., Alpers, M., Fisher, E.M.C. and Collinge, J. (2003). Balancing selection at the prion protein gene consistent with prehistoric kurulike epidemics. Science (New York, N.Y.), [online] 300(5619), pp.640–3. https://doi.org/10.1126/science.1083320
