The Sting of the Wild

by Justin O. Schmidt

  In discussions of symbiosis, I outlined in 2014 one important symbiotic relationship involving our species that has been overlooked.14 It is one of our most important symbioses: the symbiosis between humans and honey bees. We think of honey bees as our friends (they provide sweet honey) and our enemies (they sting), but we don’t think of us and honey bees as joined at the hip. And, indeed, we are not. We do, however, have a long and colorful history together. The relationship goes back millions of years and involves honey bees and primates, especially chimpanzees and our own ancestors.2 What both parties have in common is a love of honey. Bees love honey as their food for energy. We love honey for its sweetness and energy. In essence, honey bees are a special example of the arms race between defending stinging insects and attacking predators. Honey bees have outraced many potential nest predators, including most small entomophagous primates that likely would predate bees were it not for their stings and, hence, no longer attempt to exploit the vast honey and protein reserves. Honey bees also appear to have won against many larger primates, including gorillas, bonobos, and baboons. Ratels, those powerful African relatives of wolverines that are also called honey badgers, are the one major nonprimate predator of honey bees in Africa. Predators were the force driving the evolution of honey bee venom and defensive behavior. In Africa, ratels and non-human apes were the most powerful predatory driving forces in this evolution of honey bee defensive behavior. That is, until their role was replaced by humans. Honey bee resources had been and are today exploited by chimpanzees and humans. As Frank Marlowe, who spent decades among the Hadza honey hunters in Tanzania, frames it, “It is not only easy to imagine that humans were collecting honey long before this [cave paintings of 20,000 years ago], but hard to believe otherwise.” Almost certainly, early Homo lineages preceding modern humans were exploiting the honey and brood of honey bees for millions of years.

  The honey bee–hominid (the term for humans and our closest relatives) relationship is special for two reasons. First, of all social Hymenoptera, honey bees store vastly more resources than any other species. These resources include the protein and fat-rich bounty of larvae, pupae, and pollen, plus, uniquely among animals, a huge quantity of sweet and energy-rich honey. Second, chimpanzees and humans are the most intelligent animals in the bee environment. These combined properties set the stage for an amazing evolutionary battle of titans. The result is that bees possess the most powerful insect-stinging defense on Earth, and humans and chimpanzees possess the most sophisticated means of exploiting bee resources of any predators. These superlatives arose because of extreme selection pressure on both parties. To survive, bees needed to evolve the most effective stinging defenses. To exploit the rich, high-quality protein and energy of the hive, hominids needed to learn ways to breach colony defenses and endure many stings. We have no evidence that humans or chimpanzees have evolved any physiological resistance to bee stings—as the mongoose has to cobra venom—but they appear to have developed psychological resistance to the pain of the stings. In essence, they have broken the pain bluff stings signal. Chimpanzees and humans have come to associate little or no damage with dozens, even hundreds, of stings and simply ignore them, or slap at the stinging bees. Jane Goodall, the young English scientist famous for her singlehanded dedication to personal observations of chimpanzees and the discoverer of chimpanzee use of tools for fishing termites, wrote in 1986: “The raiders simply sat eating honey, surrounded by bees at which they merely slapped from time to time, albeit rather frenziedly. Two small infants, in fact, who were clinging to their mothers, whimpered and burrowed their faces into their mother’s breasts. Afterward the females spent some time pulling stings from themselves; one mother was also seen to pull them from her infant during a grooming period.”15 Mind over matter occurs when honey is involved. But size and psychological resistance to bee stings do have limits for chimpanzees and humans. Massive honey bee stinging attacks kill people occasionally and frequently drive off chimpanzees, as Goodall noted: “Nine times, after seizing one or two handfuls of honey, the chimpanzees were driven off by swarms of bees, and nine times they ran off without any honey.”15 Defending honey bees sometimes kill the other two specialist honey bee predators, ratels and honeyguide birds, those fascinating birds that lead humans to beehives.

  Evidence of the continuing arms race between honey bees and their predators, including humans and our ancestors, is seen in the venom properties and defensive behaviors of honey bees and in the robbing behaviors of humans and our ancestors. The stinging system of honey bees is unusual among stinging insects in the ease with which the sting apparatus pulls out of the honey bee and remains embedded in the flesh of the target. Numerous adaptations make this possible, including a series of sharp backward-facing barbs on the stinger. The barbs render the sting difficult to remove from the skin. Working in tandem with the barbs are preweakened parts of the sting apparatus that allow the apparatus to tear easily and be removed from the bee’s abdomen. The resulting torn-out sting apparatus is an independent, self-contained venom system that includes the venom sac and musculature necessary to deliver the venom, plus the nerve ganglion that operates to control the sting and venom movement. The advantage of such a system is that a predator might quickly and easily remove the relatively large bee from its skin before much venom is delivered, but the predator would have difficulty recognizing or removing the tiny speck of a stinger firmly attached in the flesh. By remaining in the flesh, the stinger can deliver all of the venom, not just a small percentage that might be delivered before the bee is brushed off. Another honey bee adaptation is its sting-based alarm pheromone that activates, orients, and stimulates a massive attack by hundreds or thousands of nestmates and other bees from neighboring colonies. Honey bees also behaviorally attack the eyes and nose/mouth area of an attacker, the two most vulnerable and potentially lethal areas on the predator.10 A final important bee adaptation is the venom. Honey bee venom is among the most lethal of insect venoms, and it is produced in large quantities. This large amount of venom per bee, plus the large number of stinging bees combine to yield a massive killing power of a colony. For example, if half the workers in a colony of 30,000 bees attack and sting, 820 kilograms of predators would receive sufficient venom to yield a 50 percent chance of death. This large colony lethal capacity is sufficient to threaten the lives of 10 or more adult humans and is one reason most humans do not attempt to harvest bee resources but instead leave the task to specialists among their population.

  Adaptations brought into play on the chimpanzee and the human lineage side of the relationship with bees include tool making for breaking into nest cavities, learning, use of a mutualistic relationship between honeyguide birds and humans to locate bee colonies, fire, and, recently, domestication and artificial selection and breeding. The tools used by chimpanzees to gain access to hive and honey consist of various clubs, prying and dipping sticks, and leaf sponges. The early human ancestor Homo erectus used a more elaborate set of tools in daily life than chimpanzees and that would probably have allowed them to extract honey and combs more efficiently.16 Present-day humans use a wide variety of traditional tools for robbing honey bee colonies, including various ladders, ropes, hammers and climbing pegs, harnesses, and vessels for collecting the combs. Modern beekeepers have added to the mix metal hive tools, manufactured bee homes (hive boxes), sting-resistant bee suits, and smokers for generating controlled amounts of smoke. Learning and cultural transmission via both spoken and written means are key to human success in managing and exploiting bee resources. Based on learning and cultural transmission of ant fishing methods in chimpanzees, chimpanzees would also be able to learn and transmit methods of exploiting honey bees.17

  A unique adaptation altering the relationship between humans and honey bees is the mutualism between the greater honeyguide bird, Indicator indicator, and humans. The honeyguide, a small brood-parasitic bird that possesses an unusual ability to digest beeswax, guides human honey hunters to a beehive throug
h a series of elaborate behaviors, including unique calls. The bird benefits in this relationship by obtaining comb and hive scraps left after the honey hunter has opened the beehive cavity and taken honey and brood. This mutualism exists only between humans and the bird, perhaps with an earlier relationship between H. erectus and the honeyguide.16 This unique, adaptive mutualistic relationship between bird and man tips the bee-human, predator-prey relationship toward favoring the human side.

  A crucial adaptation in the ongoing arms race between predatory humans (for purposes here, ignoring earlier possibilities involving H. erectus) and their honey bee prey was the acquisition and management of fire around 1.8 million years ago. Fire is a normal phenomenon in savanna regions of Africa to which bees adapted by filling their honey stomachs with honey in response to smoke and then abandoning the nest and cavity. Concurrently, smoke naturally reduces the defensiveness and stinging behavior of the bees, setting the stage for early humans to exploit the use of fire as an aid in robbing honey and brood from the bees. In this regard, humans turned the tables on the bees by mimicking wildfire, a real and dangerous threat, and thereby tricking them into adopting a weak defense of their hive or the outright abandonment of the hive with little or no defense.18 Just as Batesian mimicry of a dangerous animal by a harmless animal allows the “cheating” mimic to gain protective benefit, fire use by humans cheats honey bees of their ability to effectively use their stings to repel the attacker. Chimpanzees, though more able to endure stings than humans, do not match the success of human predators, likely because they did not tame fire and cannot endure the resultant massive number of stings. Evolution of increasingly painful and toxic venom cannot overcome the fire-based and disarming attack strategy of humans. The importance of the use of fire by human populations to gain the upper hand in this arms race can hardly be overstated and has resulted in major changes in human evolution.16

  The most recent addition of humans to their arsenal of weapons for use against honey bees is domestication through artificial selection of bees. From the discussion above, one might conclude that bees are ultimately losing the arms race to humans and might be on a path to extinction. But, instead, by possessing resources highly sought by humans, and by pollinating many human food crops, honey bees have become indispensable mutualists with humans. Humans learned how to manipulate honey bee genetics to reduce their normal defensiveness and to increase their investment in nectar collection and honey production compared to their investment in reproduction. In essence, humans generated a domesticated form of honey bees. This mutualism, like mutualisms in general, benefits both parties overall, even though the parties retain conflicting interests. In trade for a reduction in their tendency to sting and for increased tolerance in having their resources robbed, bees gained reduction in being killed, protection from other predators, and, most important, active dispersal by man from their original habitats of Africa and Europe to all inhabitable parts of the world. The sting set the stage for these benefits for bees by enabling them to defend against large predators and, thereby, to store large quantities of brood, pollen, and honey. These large stores, in turn, first enticed humans to predate bees and then, ultimately to protect, to maintain, and to disperse them throughout the world. In the end, a fine symbiosis was established.

  APPENDIX

  PAIN SCALE FOR STINGING INSECTS

  Note: CA = Central America; NA = North America; SA = South America.

  REFERENCES

  CHAPTER 1. STUNG

  General interest reference:

  Hrdy SB. 2011. Mothers and Others: The Evolutionary Origins of Mutual Understanding. Cambridge, MA: Harvard Univ. Press.

  1. Van Le Q, LA Isbell et al. 2013. Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes. PNAS 110: 19000–19005.

  2. New JJ and TC German. 2015. Spiders at the cocktail party: An ancestral threat that surmounts inattentional blindness. Evol. Human Behav. 36: 163–73.

  3. LoBue V, DH Rakison, and JS DeLoache. 2010. Threat perception across the life span: Evidence for multiple converging pathways. Psychol. Sci. 19: 375–79.

  CHAPTER 2. THE STINGER

  General interest reference:

  Grissell E. 2010. Bees, Wasps, and Ants. Portland, OR: Timber Press.

  1. Vollrath F and I Douglas-Hamilton. 2002. African bees to control African elephants. Naturwissenschaften 89: 508–11.

  2. Starr CK. 1990. Holding the fort: Colony defense in some primitively social wasps. In: Insect Defenses (DL Evans and JO Schmidt, eds.), pp. 421–63. Albany: State Univ. New York Press.

  3. Smith EL. 1970. Evolutionary morphology of the external insect genitalia. 2. Hymenoptera. Ann. Entomol. Soc. Am. 63: 1–27.

  4. Schmidt PJ, WC Sherbrooke, and JO Schmidt. 1989. The detoxification of ant (Pogonomyrmex) venom by a blood factor in horned lizards (Phrynosoma). Copeia 1989: 603–7.

  CHAPTER 3. THE FIRST STINGING INSECTS

  General interest reference:

  Evans DL and JO Schmidt, eds. 1990. Insect Defenses. Albany: State Univ. New York Press.

  1. Brower LP, WN Ryerson et al. 1968. Ecological chemistry and the palatability spectrum. Science 161: 1349–50.

  2. Hölldobler B and EO Wilson. 2009. The Superorganism. New York: Norton.

  CHAPTER 4. THE PAIN TRUTH

  General interest reference:

  Schmidt JO. 2008. Venoms and toxins in insects. In: Encyclopedia of Entomology, 2nd ed. (JL Capinera, ed.), pp. 4076–89. Heidelberg, Germany: Springer.

  1. Roberson DP, S Gudes et al. 2013. Activity-dependent silencing reveals functionally distinct itch-generating sensory neurons. Nat. Neurosci. 16: 910–18.

  2. Kingdon J. 1977. East African Mammals, vol. 3, Part A. London: Academic Press.

  CHAPTER 5. STING SCIENCE

  General interest reference:

  Evans DL and JO Schmidt, eds. 1990. Insect Defenses. Albany: State Univ. NY Press.

  1. Schmidt JO. 2015. Allergy to venomous insects. In: The Hive and the Honey Bee (J Graham, ed.), pp. 906–52. Hamilton, IL: Dadant and Sons.

  2. Aili SR, A Touchard et al. 2014. Diversity of peptide toxins from stinging ant venoms. Toxicon 92: 166–78.

  3. Hamilton WD, R Axelrod, and R Tanese. 1990. Sexual reproduction as an adaption to resist parasites (a review). PNAS 87: 3566–73.

  4. Schmidt JO. 2014. Evolutionary responses of solitary and social Hymenoptera to predation by primates and overwhelmingly powerful vertebrate predators. J. Human Evol. 71: 12–19.

  CHAPTER 6. SWEAT BEES AND FIRE ANTS

  General interest references for sweat bees:

  Michener CD. 1974. The Social Behavior of the Bees. Cambridge, MA: Harvard Univ. Press.

  Michener CD. 2007. The Bees of the World, 2nd ed. Baltimore: Johns Hopkins Univ. Press.

  1. Danforth BN, S Sipes et al. 2006. The history of early bee diversification based on five genes plus morphology. PNAS 103: 15118–23.

  2. Duffield RM, A Fernandes et al. 1981. Macrocyclic lactones and isopentenyl esters in the Dufour’s gland secretion of halictine bees (Hymenoptera: Halictidae). J. Chem. Ecol. 7: 319–31.

  3. Dufour L. 1835. Etude entomologiques VII Hymenopteres. Ann. Soc. Entomol. France 4: 594–607.

  4. Barrows EM. 1974. Aggregation behavior and responses to sodium chloride in females of a solitary bee, Augochlora pura (Hymenoptera; Halictidae). Fla. Entomol. 57: 189–93.

  5. Schmidt JO. 2014. Evolutionary responses of solitary and social Hymenoptera to predation by primates and overwhelmingly powerful vertebrate predators. J. Human Evol. 71: 12–19.

  Fire ants:

  1. Tschinkel WR. 2006. The Fire Ants. Cambridge, MA: Harvard Univ. Press.

  2. Wheeler WM. 1910. Ants: Their Structure, Development and Behavior. New York: Columbia Univ. Press.

  3. Snelling RR. 1963. The United States species of fire ants of the genus Solenopsis, subgenus Solenopsis Westwood, with synonymy of Solenopsis aurea Wheeler (Hymenoptera: Formicidae). Bureau Entomol
. Calif. Dept. Agr. Occasional Pap., no. 3: 1–15.

  4. Smith JD and EB Smith. 1971. Multiple fire ant stings a complication of alcoholism. Arch. Dermatol. 103: 438–41.

  5. DeShazo RD, BT Butcher, and WA Banks. 1990. Reactions to the stings of the imported fire ant. N. Engl. J. Med. 323: 462–66.

  6. Sonnett PE. 1967. Fire ant venom: Synthesis of a reported component of solenamine. Science 156: 1759–60.

  7. MacConnell JG, MS Blum, and HM Fales. 1970. Alkaloid and fire ant venom: Identification and synthesis. Science 168: 840–41.

  8. MacConnell JG, MS Blum et al. 1976. Fire ant venoms: Chemotaxonomic correlations with alkaloidal compositions. Toxicon 14: 69–78.

  CHAPTER 7. YELLOWJACKETS AND WASPS

  General interest references:

  Edwards R. 1980. Social Wasps. West Sussex, UK: Rentokil.

  Evans HE and MJ West-Eberhard. 1970. The Wasps. Ann Arbor: Univ. Michigan Press.

  Schmidt JO. 2009. Wasps. In: Encyclopedia of Insects, 2nd ed. (VH Resh and RT Cardé, eds.), pp. 1037–41. San Diego, CA: Academic Press.

  1. Wickler W. 1968. Mimicry in Plants and Animals. New York: McGraw-Hill.