A male Xylocopa virginica (Eastern Carpenter bee) on Redbud (Cercis canadensis).

Bees can suffer serious effects from toxic chemicals in their environments. These include various synthetic chemicals,[1] particularly insecticides, as well as a variety of naturally occurring chemicals from plants, such as ethanol resulting from the fermentation of organic materials. Bee intoxication can result from exposure to ethanol from fermented nectar, ripe fruits, and manmade and natural chemicals in the environment.[2][3]

The effects of alcohol on bees are sufficiently similar to the effects of alcohol on humans that honey bees have been used as models of human ethanol intoxication.[4] The metabolism of bees and humans is sufficiently different that bees can safely collect nectars from plants that contain compounds toxic to humans. The honey produced by bees from these toxic nectars can be poisonous if consumed by humans.

Natural processes can also introduce toxic substances into nontoxic honey produced from nontoxic nectar. Microorganisms in honey can convert some of the sugars in honey to ethanol. This process of ethanol fermentation is intentionally harnessed to produce the alcoholic beverage called mead from fermented honey.

Ethanol

Effects of intoxication

Bee showing its proboscis, or tongue.

The introduction of certain chemical substances—such as ethanol or pesticides or defensive toxic biochemicals produced by plants—to a bee's environment can cause the bee to display abnormal or unusual behavior and disorientation. In sufficient quantities, such chemicals can poison and even kill the bee. The effects of alcohol on bees have long been recognized. For example, John Cumming described the effect in an 1864 publication on beekeeping.[5]

When bees become intoxicated from ethanol consumption or poisoned with other chemicals, their balance is affected, and they are wobbly when they walk. Charles Abramson's group at Oklahoma State University has put inebriated bees on running wheels, where they exhibit locomotion difficulties. They also put honey bees in shuttle-boxes that used a stimulus to encourage the bees to move, and found that they were less mobile as they became more intoxicated.[6]

A temulent bee is more likely to stick out its tongue, or proboscis. Inebriated bees spend more time flying. If a bee is sufficiently intoxicated, it will just lie on its back and wiggle its legs. Inebriated bees typically have many more flying accidents as well. Some bees that consume ethanol become too inebriated to find their way back to the hive, and will die as a result.[6] Bozic et al. (2006) found that alcohol consumption by honeybees disrupts foraging and social behaviors, and has some similar effects to poisoning with insecticides.[7] Some bees become more aggressive after consuming alcohol.[8]

Exposure to alcohol can have a prolonged effect on bees, lasting as long as 48 hours.[9] This phenomenon is also observed in fruit flies[10] and is connected to the neurotransmitter octopamine in fruit flies, which is also present in bees.[11]

Bees as ethanol inebriation models

In 1999, research by David Sandeman led to the realization that bee inebriation models are potentially valuable for understanding vertebrate and even human ethanol intoxication:

"Advances over the past three decades in our understanding of nervous systems are impressive and come from a multifaceted approach to the study of both vertebrate and invertebrate animals. An almost unexpected by-product of the parallel investigation of vertebrate and invertebrate nervous systems that is explored in this article is the emergent view of an intricate web of evolutionary homology and convergence exhibited in the structure and function of the nervous systems of these two large, paraphyletic groups of animals."[12]

The behavior of honey bees intoxicated by ethanol is being studied by scientists at Ohio State University, Oklahoma State University, University of Ljubljana in Slovenia, and other sites as a potential model of the effects of alcohol on humans. At the Oklahoma State University, for example, Abramson's research found significant correlations between the reactions of bees and other vertebrates to ethanol exposure:

"The purpose of this experiment was to test the feasibility of creating an animal model of ethanol consumption using social insects.... The experiments on consumption, locomotion, and learning suggest that exposure to ethanol influences behavior of honey bees similarly to that observed in experiments with analogous vertebrates."[6]

It has thus been found that "the honey bee nervous system is similar to that of vertebrates".[13][14] These similarities are pronounced enough to even make it possible to derive information on the functioning of human brains from how bees react to certain chemicals. Julie Mustard, a researcher at Ohio State, explained that:

"On the molecular level, the brains of honey bees and humans work the same. Knowing how chronic alcohol use affects genes and proteins in the honey bee brain may help us eventually understand how alcoholism affects memory and behavior in humans, as well as the molecular basis of addiction."[13][15]

The evaluation of a bee model for ethanol inebriation of vertebrates has just begun, but appears to be promising. The bees are fed ethanol solutions and their behavior observed.[6] Researchers place the bees in tiny harnesses, and feed them varying concentrations of alcohol introduced into sugar solutions.[6][13] Tests of locomotion, foraging, social interaction and aggressiveness are performed. Mustard has noted that "Alcohol affects bees and humans in similar ways—it impairs motor functioning along with learning and memory processing."[13][15] The interaction of bees with antabuse (disulfiram, a common medication administered as a treatment for alcoholism) has been tested as well.[16]

Bee exposure to other toxic and inebriating chemicals

Synthetic chemicals

Bees[17][18] can be severely and even fatally affected by pesticides,[19][20] fertilizers,[21][22][23] copper sulfate (more lethal than spinosad),[24][22] and other chemicals that man has introduced into the environment.[1] They can appear inebriated and dizzy, and even die. This is serious because it has substantial economic consequences for agriculture.

Bumblebee

This problem has been the object of growing concern. For example, researchers at the University of Hohenheim are studying how bees can be poisoned by exposure to seed disinfectants.[25] In France, the Ministry of Agriculture commissioned an expert group, the Scientific and Technical Committee for the Multifactorial Study on Bees (CST), to study the intoxicating and sometimes fatal effects of chemicals used in agriculture on bees.[26] Researchers at the Bee Research Institute and the Department of Food Chemistry and Analysis in the Czech Republic have pondered the intoxicating effects of various chemicals used to treat winter rapeseed crops.[27] Romania suffered a severe case of widespread bee intoxication and extensive bee mortality from deltamethrin in 2002.[28] The United States Environmental Protection Agency (EPA) even has published standards for testing chemicals for bee intoxication.[29]

Natural compounds

Bees and other Hymenoptera can also be substantially affected by natural compounds in the environment besides ethanol. For example, Dariusz L. Szlachetko of the Department of Plant Taxonomy and Nature Conservation, Gdańsk University observed wasps in Poland acting in a very sleepy (possibly inebriated) manner after eating nectar derived from the North American orchid Neottia.[30]

Detzel and Wink (1993) published an extensive review of 63 types of plant allelochemicals (alkaloids, terpenes, glycosides, etc.) and their effects on bees when consumed. It was found that 39 chemical compounds repelled bees (primarily alkaloids, coumarins, and saponins) and three terpene compounds attracted bees. They report that 17 out of 29 allelochemicals are toxic at some levels (especially alkaloids, saponins, cardiac glycosides and cyanogenic glycosides).[31]

Various plants are known to have pollen which is toxic to honey bees, in some cases killing the adults (e.g., Toxicoscordion), in other cases creating a problem only when passed to the brood (e.g., Heliconia). Other plants which have toxic pollen are Spathodea campanulata and Ochroma lagopus. Both the pollen and nectar of the California Buckeye (Aesculus californica) are toxic to honeybees,[32] and it is thought that other members of the Buckeye family are also.

Bee inebriation in pollination

Bucket orchid

Some plants reportedly rely on using intoxicating chemicals to produce inebriated bees, and use this inebriation as part of their reproductive strategy. One plant that some claim uses this mechanism is the South American bucket orchid (Coryanthes sp.), an epiphyte. The bucket orchid attracts male euglossine bees with its scent, derived from a variety of aromatic compounds. The bees store these compounds in specialized spongy pouches inside their swollen hind legs, as they appear to use the scent (or derivatives thereof) in order to attract females.

The flower is constructed in such a way as to make the surface almost impossible to cling to, with smooth, downward-pointing hairs; the bees commonly slip and fall into the fluid in the bucket, and the only navigable route out is a narrow, constricting passage that either glues a "pollinium" (a pollen sack) on their body (if the flower has not yet been visited) or removes any pollinium that is there (if the flower has already been visited). The passageway constricts after a bee has entered, and holds it there for a few minutes, allowing the glue to dry and securing the pollinium. It has been suggested that this process involves "inebriation" of the bees,[33][34][35][36] but this effect has never been confirmed.

In this way, the bucket orchid passes its pollen from flower to flower. This mechanism is almost but not quite species specific, as it is possible for a few closely related bees to pollinate any given species of orchid, as long as the bees are similar in size and are attracted by the same compounds.[37]

Van der Pijl and Dodson (1966) observed that bees of the genera Eulaema and Xylocopa exhibit symptoms of inebriation after consuming nectar from the orchids Sobralia violacea and Sobralia rosea.[38][39] The Gongora horichiana orchid was suspected by Lanau (1992) of producing pheromones like a female euglossine bee[40] and even somewhat resembles a female euglossine bee shape, using these characteristics to spread its pollen:

"A hapless male bee, blind drunk with the flower's overpowering pheromones, might well mistake a toadstool for a suitable mate, but the flower has made at least a modest attempt at recreating a beelike gestalt."[41]

This seems unlikely, given that no one has ever documented that female euglossines produce pheromones; male euglossines produce pheromones using the chemicals they collect from orchids, and these pheromones attract females, rather than the converse, as Cullina (2004) suggests.[41]

Toxic plant honey

A number of plants produce alkaloids which can taint honey made from their flowers.

Grayanotoxin

Some substances which are toxic to humans have no effect on bees. If bees obtain their nectar from certain flowers, the resulting honey can be psychoactive, or even toxic to humans, but innocuous to bees and their larvae.[42][43] Poisoning from this honey is called mad honey disease.

Accidental intoxication of humans by mad honey has been well documented by several Classical authors, notably Xenophon, while the deliberate use of such honey as a medicine and intoxicant (even hallucinogen) is still practiced by the Gurung tribe of Nepal, who have a long tradition of hazardous cliff-climbing to wrest the precious commodity from the nests of Apis laboriosa, the giant Himalayan honeybee. The honey thus collected by the Gurung owes its inebriating properties to the nectar which the giant bees gather from a deep red-flowered species of Rhododendron, which, in turn, owes its toxicity to the compound grayanotoxin, widespread in the plant family Ericaceae, to which the genus Rhododendron belongs.[44]

Tutu

The New Zealand native plant Tutu produces poisonous honey, due to the toxin tutin.

Opium

Morphine-containing honey has been reported in areas where opium poppy cultivation is widespread.[45]

Ethanol

Honey, can ferment, and produce ethanol. Animals, such as birds, that have consumed honey fermented in the sun can be found incapable of flight or other normal movement.[46] Sometimes honey is fermented intentionally to produce mead, an alcoholic beverage made of honey, water, and yeast. The word for "drunk" in classical Greek is sometimes translated as "honey-intoxicated"[47] and indeed the shared Indo-European antiquity of such a conception is enshrined in the names of at least two (euhemerised) goddesses of personified intoxication : the Irish Medb (see also Maeve (Irish name) ) and the Indian Madhavi of the Mahabharata (- see page Yayati), cognate with the English word mead and the Russian word for bear медведь ( – medved – literally 'honey-eater').[48]

See also

Notes and references

  1. 1 2 Tosi, Simone; Costa, Cecilia; Vesco, Umberto; Quaglia, Giancarlo; Guido, Giovanni (2018). "A survey of honey bee-collected pollen reveals widespread contamination by agricultural pesticides". Science of the Total Environment. 615: 208–218. doi:10.1016/j.scitotenv.2017.09.226. PMID 28968582. S2CID 19956612.
  2. ↑ Of course, other creatures are not immune to the effects of alcohol:
    Many of us have noticed that bees or yellow jackets cannot fly well after having drunk the juice of overripe fruits or berries; bears have been seen to stagger and fall down after eating fermented honey; and birds often crash or fly haphazardly while intoxicated on ethanol that occurs naturally as free-floating microorganisms convert vegetable carbohydrates to [alcohol] (Warren K. Bickel; Richard J. DeGrandpre (1996). Drug Policy and Human Nature: Psychological Perspectives On The Prevention, Management, and Treatment of Illicit Drug Abuse. Springer. ISBN 978-0-306-45241-3.)
  3. ↑ Fruit flies and other insects also exhibit symptoms of ethanol intoxication (Heberlein, Ulrike; Wolf, Fred W.; Rothenfluh, Adrian; Guarnieri, Douglas J. (2004). "Molecular Genetic Analysis of Ethanol Intoxication in Drosophila melanogaster". Integrative and Comparative Biology. 44 (4): 269–274. CiteSeerX 10.1.1.536.262. doi:10.1093/icb/44.4.269. PMID 21676709. S2CID 14762870.)
  4. ↑ Latest Buzz in Research: Intoxicated Honey bees may clue Scientists into Drunken Human Behavior, The Ohio State Research News, Research Communications, Columbus OH, October 23, 2004. Archived September 1, 2006, at the Wayback Machine
  5. ↑ John Cumming (1864). Bee-keeping, by 'The Times' bee-master. p. 144. bee intoxication.
  6. 1 2 3 4 5 Charles I. Abramson; Sherril M. Stone; Richard A. Ortez; Alessandra Luccardi; Kyla L. Vann; Kate D. Hanig; Justin Rice (August 2000). "The Development of an Ethanol Model Using Social Insects I: Behavior Studies of the Honey Bee (Apis mellifera L.): Neurobiological, Psychosocial, and Developmental Correlates of Drinking". Alcoholism: Clinical & Experimental Research. 24 (8): 1153–66. doi:10.1111/j.1530-0277.2000.tb02078.x. PMID 10968652. Archived from the original on 2013-01-01.
  7. ↑ Bozic J.; Abramson C.I.; Bedencic M. (2006). "Reduced ability of ethanol drinkers for social communication in honeybees (Apis mellifera carnica Poll.)". Alcohol. 38 (3): 179–183. doi:10.1016/j.alcohol.2006.01.005. PMID 16905444.
  8. ↑ Abramson CI, Place AJ, Aquino IS, Fernandez A (June 2004). "Development of an ethanol model using social insects: IV. Influence of ethanol on the aggression of Africanized honey bees (Apis mellifera L.)". Psychol Rep. 94 (3 Pt 2): 1107–15. doi:10.2466/pr0.94.3c.1107-1115. PMID 15362379. S2CID 24341827.
  9. ↑ Happy Hour Bees , Mythology and Mead, Carolyn Smagalski, BellaOnline, The Voice of Women, 2007 describes a prolonged effect from ethanol consumption by honey bees as similar to a "hangover".
  10. ↑ Ulrike Heberlein's group at University of California, San Francisco has used fruit flies as models of human inebriation and even identified genes that seem to be responsible for alcohol tolerance accumulation (believed to be associated with veisalgia, or hangover), and produced genetically engineered strains that do not develop alcohol tolerance
    Moore MS, DeZazzo J, Luk AY, Tully T, Singh CM, Heberlein U (June 1998). "Ethanol intoxication in Drosophila: Genetic and pharmacological evidence for regulation by the cAMP signaling pathway". Cell. 93 (6): 997–1007. doi:10.1016/S0092-8674(00)81205-2. PMID 9635429.
    Tecott LH, Heberlein U (December 1998). "Y do we drink?". Cell. 95 (6): 733–5. doi:10.1016/S0092-8674(00)81695-5. PMID 9865690.
    Bar Flies: What our insect relatives can teach us about alcohol tolerance. Archived 2006-12-30 at the Wayback Machine, Ruth Williams, Naked Scientist; "'Hangover gene' is key to alcohol tolerance", Gaia Vince, NewScientist.com news service, 22 August 2005. Accessed July 17, 2009.
  11. ↑ Degen J, Gewecke M, Roeder T (June 2000). "Octopamine receptors in the honey bee and locust nervous system: pharmacological similarities between homologous receptors of distantly related species". Br. J. Pharmacol. 130 (3): 587–94. doi:10.1038/sj.bjp.0703338. PMC 1572099. PMID 10821787.
  12. ↑ Sandeman D (August 1999). "Homology and convergence in vertebrate and invertebrate nervous systems". Naturwissenschaften. 86 (8): 378–87. Bibcode:1999NW.....86..378S. doi:10.1007/s001140050637. PMID 10481825. S2CID 83847612. Archived from the original on 2012-07-10.
  13. 1 2 3 4 Intoxicated Honey Bees May Clue Scientists Into Drunken Human Behavior, Science Daily, October 25, 2004
  14. ↑ Entomology Postdoctoral researcher Dr. Geraldine Wright, Ohio State University
  15. 1 2 Entomology Postdoctoral researcher Dr. Julie Mustard, Ohio State University
  16. ↑ Abramson CI, Fellows GW, Browne BL, Lawson A, Ortiz RA (April 2003). "Development of an ethanol model using social insects: II. Effect of Antabuse on consumatory responses and learned behavior of the honey bee (Apis mellifera L.)". Psychol Rep. 92 (2): 365–78. doi:10.2466/PR0.92.2.365-378. PMID 12785614.
  17. ↑ "Bees can sense a flower's electric field—unless fertilizer messes with the buzz". Popular Science. 9 November 2022. Retrieved 16 November 2022.
  18. ↑ "Bees Can Sense the Electric Fields of Flowers". nationalgeographic.com. 21 February 2013. Archived from the original on February 28, 2021. Retrieved 16 November 2022.
  19. ↑ Kakumanu, Madhavi L.; Reeves, Alison M.; Anderson, Troy D.; Rodrigues, Richard R.; Williams, Mark A. (16 August 2016). "Honey Bee Gut Microbiome Is Altered by In-Hive Pesticide Exposures". Frontiers in Microbiology. 7: 1255. doi:10.3389/fmicb.2016.01255. PMC 4985556. PMID 27579024.
  20. ↑ Graham, Flora (31 January 2020). "Daily briefing: Genetically engineered gut microbes can protect honey bees". Nature. doi:10.1038/d41586-020-00282-3. S2CID 242243957. Retrieved 16 November 2022.
  21. ↑ Chorbinski, P.; Tomaszewska, B. (1995). "Toxicity of mineral fertilizers to honey bees under laboratory conditions. Pt. 1. Toxicity of urea and ammonium sulphate". Pszczelnicze Zeszyty Naukowe (Poland) (in Polish). ISSN 0552-4563. Retrieved 16 November 2022 – via Food and Agriculture Organization.
  22. 1 2 Rodrigues, Cleiton G.; Krüger, Alexandra P.; Barbosa, Wagner F.; Guedes, Raul Narciso C. (June 2016). "Leaf Fertilizers Affect Survival and Behavior of the Neotropical Stingless Bee Friesella schrottkyi (Meliponini: Apidae: Hymenoptera)". Journal of Economic Entomology. 109 (3): 1001–1008. doi:10.1093/jee/tow044. PMID 27069099. Retrieved 16 November 2022.
  23. ↑ Hunting, Ellard R; England, Sam J; Koh, Kuang; Lawson, Dave A; Brun, Nadja R; Robert, Daniel (9 November 2022). "Synthetic fertilizers alter floral biophysical cues and bumblebee foraging behavior". PNAS Nexus. 1 (5): pgac230. doi:10.1093/pnasnexus/pgac230. PMC 9802097. PMID 36712354. Retrieved 16 November 2022.
  24. ↑ Kava, Ruth (21 April 2016). "Organic Fertilizer Is Great at Killing Bees". American Council on Science and Health. Retrieved 16 November 2022.
  25. ↑ "Honey bee intoxication caused by seed disinfectants", Dr.sc.agr. Klaus Wallner, University of Hohenheim. Accessed on July 17, 2009.
  26. ↑ Recent Issues Related to Bee Troubles in France Archived 2007-10-04 at the Wayback Machine, J.N. Tasei, report to International Apis Health Assessment Committee (IAHAC), Bologna, Italy, May 6, 2004. This report included the results of a study of the toxic effects on bees of the seed dressings imidacloprid and fipronil.
  27. ↑ František Kamler; Dalibor Titěra; Jiřina Piškulová; Jana Hajšlová; Kateřina Maštovská (2003). "Intoxication of honeybees on chemical treated winter rape: problem of its verification" (PDF). Bulletin of Insectology. 56 (1): 125–7. ISSN 1721-8861. Archived from the original (PDF) on 2007-09-23.
  28. ↑ Daniela Nica; Elisabeta Bianu; Gabriela Chioveanu (2004). "A case of acute intoxication with deltamethrin in bee colonies in Romania" (PDF). Apiacta. 39: 71–7. Archived from the original (PDF) on 2007-09-27.
  29. ↑ Ecological Effects Test Guidelines OPPTS 850.3030: Honey Bee Toxicity of Residues on Foliage, EPA 712–C–96–148 April 1996.
  30. ↑ Nelis A. Cingel (2001). An atlas of orchid pollination: America, Africa, Asia and Australia. CRC Press. p. 44. ISBN 978-90-5410-486-5.
  31. ↑ Detzel, Andreas; Wink, Michael (March 1993). "Attraction, deterrence or intoxication of bees (Apis mellifera) by plant allelochemicals". Chemoecology. 4 (1): 8–18. doi:10.1007/BF01245891. ISSN 0937-7409. S2CID 27701294.
  32. ↑ "School Native Plant Gardens and Nature Areas". California Native Plant Society. Archived from the original on August 17, 2007. Retrieved 2007-04-26.
  33. ↑ Dodson C.H.; Frymire G.P. (1961). "Natural pollination of orchids". Mo. Bot. Gard. Bull. 49 (9): 133–152.
  34. ↑ Pierre Jolivet (1998). Interrelationship Between Insects and Plants. CRC Press. p. 192. ISBN 978-1-57444-052-2. The first hymenopteran to visit has difficulties coping with the rostrellum but the later ones to arrive easily escape, soaked, drunk, and often having completed their pollinating function.
  35. ↑ bumblebee.org article on Hymenoptera
  36. ↑ William C. Agosta (2001). Thieves, Deceivers, and Killers: tales of chemistry in nature. Princeton University Press. ISBN 978-0-691-00488-4.
  37. ↑ Dressler Robert L (1968). "Pollination by Euglossine Bees". Evolution. 22 (1): 202–210. doi:10.2307/2406664. JSTOR 2406664. PMID 28564982.
  38. ↑ Nelis A. Cingel (2001). An atlas of orchid pollination: America, Africa, Asia and Australia. CRC Press. ISBN 978-90-5410-486-5.
  39. ↑ Leendert Van der Pijl; Calaway H. Dodson (1966). Orchid Flowers Their Pollination and Evolution. University of Miami Press. ISBN 978-0-87024-069-0.
  40. ↑ Lunau, Klaus (June 1992). "Evolutionary aspects of perfume collection in male euglossine bees (Hymenoptera) and of nest deception in bee-pollinated flowers". Chemoecology. 3 (2): 65–73. doi:10.1007/BF01245884. ISSN 0937-7409. S2CID 26259242. speculated that the chemicals produced by the bucket orchid mimic bee pheromones.
  41. 1 2 William Cullina (2004). Understanding Orchids : An Uncomplicated Guide to Growing the World's Most Exotic Plants. Boston: Houghton Mifflin. p. 180. ISBN 978-0-618-26326-4.
  42. ↑ Jansen; et al. (2012). "Grayanotoxin Poisoning: 'Mad Honey Disease' and Beyond". Cardiovascular Toxicology. 12 (3): 208–13. doi:10.1007/s12012-012-9162-2. PMC 3404272. PMID 22528814.
  43. ↑ "Grayanotoxins". Foodborne Pathogenic Microorganisms and Natural Toxins Handbook. US FDA. 2012. Retrieved August 7, 2015.
  44. ↑ Treza, Raphael (2011). "Hallucinogen honey hunters". topdocumentaryfilms.com. Retrieved 20 October 2015.
  45. ↑ Alistair McAlpine (2002). Adventures of a Collector. Allen & Unwin. ISBN 978-1-86508-786-3.
  46. ↑ Kettlewellh, B.D. (February 1945). "A Story of Nature's Debauch". The Entomologist. 88 (1101): 45–7.
  47. ↑ Karl Kerenyi (1976). Dionysus: Archetypal Image of Indestructible Life. Princeton University Press. ISBN 978-0-691-09863-0.
  48. ↑ Dumézil,Georges, Mythe et Epopée I. II. III. Quarto Gallimard, pub. Éditions Gallimard 1995 ISBN 2-07-073656-3. pps. 995–998

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