The Sting of the Wild

by Justin O. Schmidt

  In response to their disparate cadre of predators, harvester ants evolved individualized suites of defenses for each type of predator, often for each situation. What works against one type of predator frequently is woefully inadequate, or outright ineffective, against another type of predator. Stings work really well against you or me, but they are worthless against web-spinning spiders. Biting works well against other attacking ants but not against befeathered birds. That said, some generalities do emerge: Stings are generally useful against vertebrate predators and are not useful against insect and other arthropod predators. Biting mandibles are generally useful against insect and other arthropod predators or competitors but are of little use against large vertebrate predators. As is the biological rule, exceptions occur. In two instances, I have found dead vinegaroons (whiptail scorpions) killed by a harvester ant sting successfully placed in the intersegmental membranes of the vinegaroon’s crushing, claw-like pedipalps (appendages near the mouth). Biting, a defense of little effect against many large vertebrates, is effective against horned lizard predators.

  Social insects are superorganisms in which the entire colony acts much as a single organism, albeit one with separate mobile parts. As cells and tissues in the human body act for the good of the whole, social insect individuals act for the benefit of the colony. As our skin cells operate to protect the rest of our body, ant workers operate to protect the queen and the rest of the colony. The harvester ant superorganism is generally little affected by small insect and other predators, just as we are not seriously damaged by bedbug bites. Bedbug bites are a nuisance, for sure, and do kill some blood cells, but otherwise, they have little effect on our survival or productivity. Likewise, the loss of a few individual harvester ant foragers to small predators barely affects the overall survival or success of a harvester ant colony. Invertebrate predators threaten individual units, the workers, rather than the whole colony. A common invertebrate predator that takes an occasional worker is the ant lion, famous for making conical pits in sand and lurking out of sight in the sand at the bottom. If a hapless harvester ant slips down the loose sandy side of the pit, a pair of ice-tong mandibles await to skewer it. The ant appears to instinctively recognize the risk and rapidly attempts to run upward out of the pit. The ant lion responds with a shower of sand flipped on and above the ant, causing continual landslides of sand plus ant cascading back toward the awaiting jaws. Fortunately, most harvester ant individuals are too big and too fast, allowing them to escape the sand-slide torrent and flee from the pit. The ant lion will need to find a smaller ant next time.

  A cadre of miscellaneous arthropod predators, including robber flies, assassin bugs, and a variety of spiders, ambush or trap a few harvester ant workers. Of this group, only a few spiders are of major potential consequence. Black widows and false black widows (Steatoda) can be most troublesome. False black widows have the temerity of building their webs directly over colony entrances of harvester ants and lurking out of reach a few centimeters above, ready to snag foragers. The success of this spider lifestyle rests on the extraordinary strength and stickiness of the silken web and on the ability of the spider to reside in its web safely above the fray. Although a spider will take only half a dozen ants per day—hardly enough to depopulate the colony—the ants respond strongly and negatively by moving their nest entrance or by shutting down all outside activity for days, thereby starving the spider and forcing it to leave. This heroic action by the ants seems economically counterproductive compared to lost foraging activity, although, perhaps, overall it is beneficial in ways not so obvious to simple economic bean counting. Web spiders, along with other predators inclined to reside near nest entrances, are believed to be a major reason western harvester ants clear all vegetation from around their colonies. Clearings remove anchors for the webs of false black widows and other spiders and expose these spiders or other predators to their own predators. These ant predators are less likely to risk their lives for just a few ants.19,20,21

  Nature never ceases to deliver surprising inventions. One amazing surprise is hidden in the story of the digger wasp, Clypeadon, and harvester ants. Some species in the small genus Clypeadon prey exclusively on worker harvester ants. The wasp grabs a worker ant either near the nest or, when few ants are outside, enters the nest and attacks an individual ant inside and underground in its own lair. In either case, the ant is stung into a deep, permanent paralysis and carried back to the wasp’s burrow. Despite having formidable mandibles that could easily dismember the wasp, the ants mysteriously rarely mount a strong defense against attack. We don’t know why. Ants may not attack because they lack the ability to smell meaningful foreign odor from the wasp. Much as we cannot see a black object in the dark, the ants would not be able to smell an apparently odorless or tasteless wasp, and a threat unseen or not smelled is a threat undetected. This scenario seems impossibly strange to visually based organisms such as us, but vision plays no meaningful role in recognition by most ants. They rely on body “odor” signatures.

  Clypeadon paralyzes and carries off between 16 and 26 ants to stock each larval cell of her nest. She lays an egg on one of the paralyzed ants, seals the cell, the egg hatches into a larva that eats all the ants, pupates, and then emerges as an adult. From this initial glance, Clypeadon’s life history description appears not that different from many other digger wasps. The departure from the usual digger wasp biology unfolds in the mechanism of transport of paralyzed ants. The standard digger wasp’s method of prey transport is to hold the prey with its mandibles, its middle pair of legs, or stuck on its barbed stinger. Not Clypeadon. She flies off with mandibles, all six legs, and the stinger free and with the ant appearing glued to the tip of her abdomen. She has a unique structure, not possessed by males or any other wasps, appropriately called the “ant clamp.” The wasp’s clamp is composed of an enlarged specialized biconcave upper part of the abdomen matched to a mobile lower bilobed abdominal structure that clamps and locks against the ant’s leg bases. This mechanism is ideal for unencumbered transport. Unfortunately, it is also ideal for lightning-fast parasitic flies to lay tiny maggots on the ant held behind the wasp. The maggots then appropriate the ants in the cell to make flies instead of wasps.22 No new invention by nature goes unnoticed.

  Remarkably few birds, and no mammals, have successfully exploited harvester ant colonies. George F. Knowlton of Utah State University devoted much of his life to studying vertebrate predators of insects, including harvester ants. Birds that at least occasionally might feed on harvester ants included rock wrens, sage thrashers, western meadowlarks, Brewer’s blackbirds, sage sparrows, sage grouse, and red-shafted flickers.23 How these birds avoided stings and bites is unclear—speed, agility, and, especially, slick feathers and hard crushing bills? Sage grouse, now an endangered species, eat the occasional western harvester ant and then add the insult of using their ant mounds as conspicuous high points to attract females to male strutting grounds.24 Flickers display an interesting behavior with western harvester ants. They visit the conical ant nests in the morning when ant larvae and pupae are brought to the warmth of the sunny side and pick off the thin protective soil crust exposing the white larvae and pupae. The flicker is primarily interested in these white morsels, rich in protein and fat and low in fiber, though a few low-protein, low-fat, high-fiber workers get consumed in the process.25

  Lizards are the most serious predators of harvester ants. Side-blotched lizards, long-nosed leopard lizards, and fringe-toed lizards eat worker ants, including harvester ants. Sagebrush lizards (Sceloporus graciosus) take the culinary fondness for ants a step further. Most analyzed individuals have harvester ants in their stomachs. Horned lizards, genus Phrynosoma, take eating ants to the extreme. Eighty-nine percent of the regal horned lizard’s diet is harvester ants.26 Horned lizards, squat, rotund creatures sporting a collar of vicious spikes at the back of their head, have long been favorite animals of people. Their rounded body shape and pathetically slow running ability make them
easy to catch, properties that have allowed pet-loving people to love them to extinction in some areas. Among their unusual properties is an enormous stomach able to hold 13.4 percent of their weight.26 No other lizard can match that feat. That’s like a 200-pound person eating a 27-pound meal. As Japanese sumo wrestlers cannot sprint or run marathons, horned lizards lost their ability to run fast or far. Such is the price of becoming a harvester ant specialist.

  If one is fat, slow, and eats mainly ants in exposed areas, some tricks are needed. An immediate trick that is not obvious until a horned lizard runs is its mastery of camouflage. They have color patterns closely matching the ground surface of their environment, and because they are short and broad, they leave no shadow. Some species even add fringes of scales to disrupt their body outline, thereby blending nearly perfectly with the substrate. Add to this very slow motion and enhanced awareness, and the lizard is rarely detected by either predator or ant. With a dietary necessity of up to a hundred ants per day, some tactical strategy is in order. The horned lizard strategy is to forgo frontal attack at the colony entrance, preferring to reside at the edge of a trunk trail or periphery of a colony clearing where individual ants can be picked off singly. A flick of the tongue and the ant disappears.

  The fact that harvester ant venom is the most mammalian-toxic insect venom known led several of us to wonder how horned lizards could eat harvester ants with impunity. The venom of one harvester ant is sufficiently potent to kill a horned-lizard-sized mouse several times over. How, then, does the lizard avoid a lethal encounter when eating a hundred ants? Wade Sherbrooke, the foremost horned lizard biologist, my wife, and I put our heads together (probably over some beers) to determine whether we could answer this question. Wade was completing his doctoral dissertation on the mechanism in horned lizards of skin color change to match the background. I asked him his method.

  “I just sacrifice a lizard and incubate its skin for hormone and other analyses.”

  “What do you do with the rest of the lizard?”

  “Oh, I just discard it.”

  “Aagh! You throw it away and waste all the rest of the lizard? You can’t do that. Give me the blood.”

  And so began the project. Wade provided lizard blood, my wife, a master of dissecting harvester ants for their venom, dissected thousands of ants, and I focused on determining the physiological mechanism of lizard tolerance to ant stings. The first question was, Are horned lizards susceptible to harvester ant venom? When tested with enough venom to kill 100 mice, the lizard was totally unaffected. That means they are not susceptible to the ant’s venom. So, get out the shovels and buckets, we have work to do. Back from the blazing Arizona sun with several more buckets filled with Maricopa harvester ants, we began the task of harvesting more, much more, venom. That done, we finally found a median lethal dose for horned lizards: more than 1,500 times the lethal dose for a mouse was required to kill a horned lizard, an amount that translates into the venom from 200 ants. Jarrow’s spiny lizard, a relative of horned lizards, was much more susceptible to the venom than horned lizards. Newborn horned lizards living in an area lacking harvester ants were about as resistant as lizards feasting on the ants. These findings indicated that horned lizard resistance was innate and not induced immunologically. Horned lizards were not undergoing self-vaccination through diet; they were eating harvester ants with impunity because they have a blood factor that neutralizes the ant venom. This was confirmed by classic antivenom + venom studies in which lizard blood plasma was mixed with 3.6 times a lethal dose of venom and injected into mice. The mice showed no adverse reactions. Horned lizards are the first known example of a vertebrate predator that has evolved an innate resistance to an insect venom.27

  The harvester ant–horned lizard story doesn’t end here. Both the horned lizard and the harvester ant have more surprises. Horned lizards secrete a special slippery and viscous mucus that lines their mouth and digestive system. When an ant is eaten, its sting, rather than piercing the delicate throat or stomach lining, usually slips off harmlessly. The ants, for their part, have two defenses. Ironically, although the lizard isn’t bothered by stings, it is intolerant of bites. If the ants become alerted to the lizard, they release alarm pheromone from glands at the base of their mandibles to recruit other ants to initiate a mass attack. This mobbing attack drives off the lizard, while providing an added bonus of exposing the fleeing lizard to the risk of being spotted by a roadrunner or another of its own predators. As a final insult to the lizard, the ants can bite and clamp so permanently to the lizard’s toes or soft underbelly that the head remains attached long after the ant has died, as a reminder of the ant’s ability.

  One species of harvester ant, the enigmatic Pogonomyrmex anzensis, lives in such a harsh environment that horned lizards do not live there. This ant, described from a single collection in the Anza-Borrego Desert of California, was subsequently lost to science for 45 years despite an intense search by some of the finest myrmecologists of the time. The “mystery” ant was rediscovered in 1997 by Gordon Snelling after years of careful search. The ants nest in an unimaginably harsh location among south-facing, hard, rocky hillside slopes that are exceptionally sunbaked, hot, and dry. No horned lizards live there; in fact, Gordon could find no potential predators living there. We asked, What happens to the venom of a species that has no vertebrate predators? To answer this question, Gordon collected these ants and shipped them to me where I ran some comparative tests. The venom sacs of these ants were collapsed and mostly empty, containing only about one-sixth the venom expected. The sacs were of normal size. They just contained little venom. Gordon also noted that the ants were very timid and could not be forced to sting readily. When analyzed for toxicity, the ants surprised us. They were among the most toxic of any harvester ants, some three times more toxic than Wheeler’s harvester ant, the largest and one of the most aggressive of all North American harvester ants. Apparently, the evolutionary response in P. anzensis to a harsh environment and the loss of major predators is not to lose or sacrifice venom activity but, rather, to spare the energy required to make venom by not producing much venom.28

  Lizards are not the only animals that eat hundreds of harvester ants at a sitting. Historically, people have also. One fine afternoon in 1994 I received a call from Kevin Groark, a master’s student at the University of California, Los Angeles, who was studying cultural traditions of California native peoples before the massive influx of the Anglo population. The young men of several tribes engaged in spiritual trips called “vision quests” in which they sought “dream helpers” to enhance their lives or to provide strength. Before they embarked on a vision quest, they fasted and vomited, often for several days in preparation. Vision quests were generally conducted in winter, which added another stress. When ready, they would ingest harvester ants in balls of eagle down feathers delivered by elder women. Kevin wondered whether the toxic nature of the venom could “poison” a youth into a state of hallucinations during which the religious spirits entered his body to give him guidance or strength.

  “Heavens no,” I replied. “A toxic dose of harvester ant venom for a person would be near a thousand stings. Perhaps the extreme pain alone could send them into a trance.”

  Kevin replied that they eat a lot of ants.

  “How many?”

  “Three hundred fifty or so.”

  “Wow. That could cause a sublethal effect that, combined with the rest of the ritual, might well induce hallucinations.”

  I can’t imagine the pain, much less the sheer determination, required to go through such a ritual. On the basis of careful field notes by early anthropologists and voucher specimens, the ants in question were identified as California harvester ants.4 As if the vision quests were not painful enough, some Indian groups “hardened” youths through puberty rites, as described by John Harrington in 1933, in which the early adolescent was “whipped with nettles and covered with ants that they [the boys] might become robust. This infliction was al
ways performed in summer during the months of July and August when the nettle was in its most fiery state. … [The boy was whipped] until he was unable to walk. He was then carried to the nest of the nearest and most furious species of ants, and laid down among them, while some of his friends, with sticks, kept annoying the insects to make them more violent. What torments did they not undergo! What pain! What hellish inflictions! Yet their faith gave them power to endure all without a murmur, and they remained as if dead.”4 Perhaps fortunately for the ants, young men in California no longer have such rites.

  Harvester ants are clearly special no matter from what angle they are viewed. Their stings and venom are particularly unique and extraordinary. Exactly what made them special captured my interest from my first experience. Love at first sting! Harvester ant stings were well noted and documented in the ant literature.

  H. C. McCook wrote in 1879 that harvester ants are “regarded with a wholesome fear by children, and adults have little wish to meddle with them. … I tried to engage him [a bright, stout youth] to assist in the digging, but my offer was rejected with an emphasis and facial expression of horror which was amusing. … ‘I wouldn’t do dat fur five dollas a day [= $845 in labor costs in 2014]’!”15 He continues that after the sting

  there was a sharp, severe pain, resembling that of the sting of a bee. Then followed twice, at short intervals, a nervous, chilling sensation, which seemed to sweep upwards, and was felt quite sensibly around the roots of the hair. This was a very peculiar feeling indeed, and appeared to me very like that caused by a sudden alarm, or excitement in which the element of horror predominates. Then followed a steady heavy pain about the wound, which continued for three hours more or less severely, a slight numbness accompanying. … Her sting pained me very much indeed, and was felt more than twenty-four hours afterwards.15