July threatened to leave our meadow hot, windy and in need of rain. The summer monsoons were delayed and the garden was asleep. Paper wasps were still zigzagging slowly through the tall clump grass looking for things to eat, but most everything else was waiting for a break from the heat.
One morning I walked outside before the sun came up and found four bucks - all sporting nearly full racks - nibbling on my grapes and cherry trees. I was mad. They had been taking their fill of the garden all year, and although I didn’t mind their leftover scat, I didn’t appreciate how much they had taken from some of my young trees. A small crabapple, a newly transplanted cherry tree, and a young serviceberry were almost completely defoliated and were barely hanging on.
Our yard is a magnet for deer. It doesn’t matter that I am surrounded by neighbors with traditional (I mean non-native) plants that they might eat. The deer know that there are many of their native favorites in our yard, and that these are mixed in with savory fruit trees that seem to add a tasty supplement to their typical diet. They are willing to walk several blocks through developed neighborhoods in order to get to our yard. And they remember the way. And, once they get here, they know where each of our tasty plants can be found.
Kathy is always slightly amused when I storm into the house cursing the deer. “We have created a meadow of native plants to encourage wildlife,” she reminds me. “And deer happen to be wildlife!” This is certainly true. And even though I am an entomologist and spend most of my efforts working with insects. The deer are not invasive in any natural sense. I grit my teeth and vow to keep waking up early to chase them away.
This time, as I shooed the interlopers out of the yard, I noticed that one of them stepped right on top of a harvester ant mound. I checked on it later that day. It was alive with ants in the act of repairing the damaged mound. They didn’t seem bothered by the heat, but the other four mounds in the yard remained quiet. It was too hot for them and they had closed their mounds, blocking the entrances and calling all foragers back inside.
Then we got an hour of rain on the last day of July. It was the first significant rain of the summer, the kind that makes your nares instinctively flare with delight. We sat out on the deck watching the sun go down enjoying the golden light on the cottonwoods in a kind of midsummer aromatherapy.
The next day was August and the forecast was for rain showers off and on for five days in a row. I was thrilled and went outside to let the ants know. They, of course, didn’t need any announcement from me. Their mounds were fully open and they were busy scouring the meadow for seeds and expiring arthropods. It’s funny how a large pogo mound can seem completely vacant one day and teeming with activity the next.
Not far away on a small berm near an aspen, I almost stepped on another creature that was very happy to see the ants again: one of the three horned lizards (Phrynosoma hernandesi) that I know live in our meadow. It was already fat before the ants closed their doors in July and it certainly didn’t look under-nourished now, but it had gone without its primary food (ants) long enough.
I’m always impressed every time I see one of these reptiles milling around pogo mounds. Occasionally they position themselves right on the mound itself. But most of the time they wait by the side of a trail and snatch up ants as they march past. It's fascinating to watch because they make it look so easy. There is no running and pouncing on their prey. And they don’t extrude a long tongue like a chameleon. They just capture one ant at a time in a lightning fast thrust of the head. If an ant moves out of range, it doesn’t bother to chase after it. It just waits until another ant comes marching along the trail.
This habit of remaining perfectly still with the occasional head thrust gives the horned lizard a virtual cloak of invisibility. Ants confront the world (and especially each other) via chemical signals. They have “taste buds” (scientists call them chemoreceptors) all over their bodies. One of these chemical signals is a distress signal that warns other ants of danger. But horned lizards can usually feed for many minutes without eliciting a warning signal of any kind. They are just too fast and take the hapless ants without warning and engulf them completely in their mouths. It appears as if the ants never even notice as their sisters get picked off one by one.
But it turns out that the lizards have more up their sleeves - or maybe it would be better to say that they have more in their stomachs. When they snatch up the ants, they don’t take time to chew them. They are grabbed and swallowed whole. Maybe this doesn't seem like a big deal. We swallow large chunks of food all the time and never give it a second thought (even though this is not really a good nor a safe practice). But pogos are not the typical food. They are listed in some studies as having the nastiest arthropod venom around. Patricia Schmidt et al. (1989) write that “their venom has the highest known lethality to mice.” You would think that the horned lizards might be a little more cautious.
The surprise is that they don’t have to be cautious. They aren’t in any danger. Something in their blood protects them from even very high concentrations of venom. And their stomachs are also unusual. When the ants are swallowed, most of them are still alive and capable of stinging. But the ants contain a viscous mucus that mucks them up. Even if the ants do sting a lizard’s stomach, it is many times more protected from the venom than other reptiles. Schmidt’s study found them over a thousand times more protected than mice.
It does happen that a horned lizard occasionally gets overwhelmed by ants. I have never seen this happen in Southern Utah where both the reptiles and the ants have lived together for millions of years and have worked out a symbiosis that works well. In other parts of the country, however, the situation is different. In Texas, the invasive red imported fire ant (Solenopsis invicta) has taken over many areas formerly occupied by native ant species.
Twenty years ago, a couple of herpetologists noticed that the horned lizards in their research area were behaving unusually. If the reptiles disturbed the aggressive fire ants and remained still, as this is their typical response, the ants would attack. If a few of the ants crawled over their bodies and started stinging them they would only close their eyes and wait. They would only eat the ants if they happened to get close to the mouth. If 20 or more ants ended up attacking them, however, this changed. They sprinted away from the fire ant mound and buried themselves in the soil. First they would wiggle their tails and then lower the rest of their bodies until they were completely covered. A few seconds later, the ants would emerge above ground, leaving the horned lizards alone (Webb and Henke, 2003). Somehow, the horned lizards intuited enough math to know the number of ants (and their toxins) that would swamp the protective enzymes in their blood.
Many ants (including pogos) demonstrate what scientists call sting autonomy. This is a practice seen in some social hymenoptera (like wasps, bees and ants) where individuals will sting a threatening animal for the protection of the colony even though it means death for the stinging individual. Not all of the hymenoptera that carry stingers die when they sting. The ones that do (like honeybees) have developed a stinger that gets stuck in the skin of the unlucky subject. I often hear students commenting on how bad this seems for the bees. Why haven’t they evolved stingers that don’t get embedded in the skin of the target animal - like wasps, for example?
In fact the barbed stingers - and the death that follows to the bees - are part of the reason for the success of this kind of sting. By leaving the stinger and the venom sack stuck in the victim after the adult bee has been swatted away, the pain of the venom is able to act more quickly and be delivered in greater quantity, thus reinforcing the warning to leave the bees, their home, and all that sweet honey alone (Schmidt, 2016).
We usually talk about the sting autonomy of honeybees but harvester ants are also known to sting this way, even though it isn’t a human that they typically sting. If a human happens to walk inadvertently on a pogo mound, she will likely feel the ants crawling on her legs before getting stung - and have time to brush them off. This is not always the case with other predators.
But horned lizards are rarely (if ever) attacked by native ants - not even harvester ants. I have never seen it happen, nor have I read any accounts of it happening. They aren’t agile enough to grab ants that might be crawling over their body. But they can run away and are quite fast if the need arises. And if they do get stung a few times, it doesn’t seem to bother them at all - at least that’s how it appears to humans that are not experiencing the stings themselves.
These handful of adaptations for eating ants are shared by a disparate group of animals known as myrmecophages. Myrmecophagy is the technical term for ant-eating. Some spiders are myrmecophagous. Vertebrates like pangolins, echidnas, numbats, ant-eaters and some woodpeckers are obvious examples as well. The acorn woodpecker is even named for the practice (Melanerpes formicivorus). In the tropics there are a number of species of ant wrens and ant-pittas that are also specialists. Some species of frogs should also be added to the list. But these are exceptions. Ants are not part of most animals’ diets.
The reason seems clear enough, it can be painful. And it requires several adaptations that most animals have never evolved. The ant-eating guild of vertebrates tend to have strong forearms and a stout claw for ripping into ant mounds. The teeth of many species have been reduced, or lost entirely, and a long tongue and a narrow mouth cavity have taken their place. The commitment to feed on ants is typically not a casual evolutionary development. Generalist predators tend to leave ants alone because of the grief they inflict.
The myrmecophages have had to evolve solutions to the various ant problems. Their salivary glands are usually expanded and full of enzymes to break down the outer covering of the ants. This covering is called a cuticle and can be hard and difficult to digest. The salivary glands also contain enzymes for breaking down formic acid and other nasty chemicals in the ants’ bodies.
Further along the digestive tract, many myrmecophages have a fortified (sometimes called a cornified) stomach. It is thick and can be stung much more often than the stomachs of other predators without causing serious damage. Once the ants make it to the small intestines, special enzymes actively begin breaking down trehalose, the distinct blood sugar found in ants and many other kinds of insects.
Some amphibians have become myrmecophages with the ability of separating the nasty chemicals within an ants body and moving them to their skin. The poison dart frogs of the Americas (of the family Dendrobatidae) are an example of this. We used to assume that the frogs made their own deadly skin toxins. We now know that most of these compounds are derived from the things that they eat. Plant alkaloids can be converted to toxins but also many insects end up being the source. Large tropical ladybird beetles with their orange blood provide some of these compounds. Millipedes do as well. But the majority of these toxins come from ants (Saporito et al., 2004).
I wonder if the horned toads of the American Southwest might not have similar capabilities. Are they protected from other predators because they taste bad? Two scientists (Sherbrooke and Middendorf) conducted an experiment in 2004 that seemed to suggest this. Kit foxes that were sprayed with blood from the eyes of horned lizards tended to avoid eating the lizards as prey. After such an encounter, the foxes shook their heads from side to side as if trying to mollify whatever nastiness happened to be in the blood. The two scientists then coated mice with the horned lizard blood and watched as the foxes behaved in the very same way. It seems reasonable that the lizards are able to create such foul blood because of the ants that they eat. Clearly they have stumbled onto an evolutionary strategy that works well. And in fact horned lizards can be common throughout the American Southwest in places where ancient habitats still prevail.
Unfortunately, not all horned lizards are as happy as the ones in our small desert meadow. They don’t survive when cattle are allowed to trample on their homes. In many places of the West, harvester ants and cattle do co-exist. The ants seem to manage getting stepped on. Their rate of reproduction is more than fast enough to make up the losses. But the horned lizards are not. There is also evidence that pesticides take their toll. This sort of misfortune is happening all over the world. Animals and plants with remarkable adaptations to survive are not able to handle the new toxins and invasions of the modern world.
Ant-eating animals are having to deal with these changes repeatedly. The example of horned lizards in Texas with fire ants is just one example. But what is the larger cost suffered by the lizards? How often can they be attacked by fire ants before they run out of defensive enzymes, or simply run out of energy by running away and burying themselves?
I noticed many years ago that my own body is often confronted with this kind of tug-o-war. I don’t mean that I regularly get attacked by fire ants (although this did happen once by a beautiful stream in Louisiana). But I do often feel strong and even well adapted to certain environmental situations (like hiking, swimming in a cold lake, or even just weeding the garden) only to be stymied by an unlucky meal of industrial food. Sometimes a bad air day can keep me inside feeling lousy as well.
How are we to deal with these problems? Harvester ants close up their mounds and wait for hard times to pass. They have proven (so far) to be resilient to the onslaughts of modernity. Horned lizards, not so much. As a result they are disappearing from many places where they used to be common. We humans seem to be proliferating successfully like ants, even as we as individuals and cultures are struggling to deal with a changing world. How long can we survive the industrial equivalents of fire ants? Maybe there is a lesson here in my own backyard.
References
Camargo, A., & Maneyro, R. (2007). Environmental and seasonal variation in the diet of Elachistocleis bicolor (Guérin-Méneville 1838)(Anura: Microhylidae) from Northern Uruguay. Zoological Science 24, 225-231.
Cheng, S. C., Liu, C. B., Yao, X. Q., Hu, J. Y., Yin, T. T., Lim, B. K., ... & Yu, L. (2023). Hologenomic insights into mammalian adaptations to myrmecophagy. National Science Review, 10(4), nwac174.
Saporito, R. A., Garraffo, H. M., Donnelly, M. A., Edwards, A. L., Longino, J. T., & Daly, J. W. (2004). Formicine ants: an arthropod source for the pumiliotoxin alkaloids of dendrobatid poison frogs. Proceedings of the National Academy of Sciences, 101(21), 8045-8050.
Schmidt, J.O. (2016). The sting of the wild, the story of the man who got stung for science. John Hopkins University Press, Baltimore.
Schmidt, P. J., Sherbrooke, W. C., & Schmidt, J. O. (1989). The detoxification of ant (Pogonomyrmex) venom by a blood factor in horned lizards (Phrynosoma). Copeia, 603-607.
Sherbrooke, W. C., & Middendorf III, G. A. (2004). Responses of kit foxes (Vulpes macrotis) to antipredator blood-squirting and blood of Texas horned lizards (Phrynosoma cornutum). Copeia, 2004(3), 652-658.
Webb, S. L., & Henke, S. E. (2003). Defensive strategies of Texas horned lizards (Phrynosoma cornutum) against red imported fire ants. Herpetological Review, 34(4), 327.
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