Summer World: A Season of Bounty - Bernd Heinrich (2009)
Chapter 9. Masters of Disguise
IT IS RARE FOR ANYONE NOT SPECIFICALLY LOOKING FOR a big plump caterpillar of a sphinx moth to find one. There is one exception, though—the tomato hornworms. We always have a tomato patch in our garden, and we almost always used to find several hornworms in it, although I have not seen any for years. The big green (and sometimes pale blue or black) horntail grub munching on tomato foliage in the garden transforms itself into a mummylike pupa encased in a hard brown shell and then remains in a deathlike stupor for the better part of a year in an underground crypt. The following summer it molts from its shell to be resurrected into a moth that flies only at night and feeds on the nectar of flowers, and superficially looks and acts like a hummingbird. But the moth is substantially more different from a hummingbird than a human is from an aardvark. Because they are unique and represent a strange breed that has been a favorite animal for unraveling many mysteries of development, I am always hoping to find one or several hornworms feeding on our tomato greens.
An insect’s metamorphosis in body and behavior from larva to imago (adult) is amazing, yet it is easily taken for granted because of its inflexible inevitability.
It is difficult enough to envision butterflies exercising choice in behavior, much less to imagine their immature grubs exercising options that determine how they will turn out physically after a molt. However, some insects do exercise options, on the basis of often subtle cues from their environment. For example, many species of aphids have optional wings if they experience the photoperiod of a summer.
The phenomenon of developmental plasticity was first discovered in some butterflies that had been described as different species but were later found to be different forms of the same species, which had experienced different seasons of the year. The summer environment had provided some cue that had switched their developmental patterns. Similarly, when young (nymphs) of the grasshopper Schistocerca gregaria are tickled—as when they encounter each other during high population densities—the adults from such “stimulated” nymphs molt into forms that look like a species totally different from those that grow up alone. Furthermore, the “tickled” nymphs are adapted to wander in search of new feeding areas as local supplies are depleted. Similarly, the caterpillars of some species of moths also respond to their environment by switching one developmental pathway into another one, to produce forms that are adapted to reduce their chances of being eaten by predators.
The appearance of a caterpillar from one instar (a stage separated by a shedding of its “skin,” or armor shell) to the next may commonly differ, but the new “uniform” that it wears is usually specific for all individuals. However, in some species there are two or more options for the “uniform,” depending on what the caterpillar experienced when it was younger. For example, in one sphinx moth species, Laothoe populi, when the caterpillars are raised on a white background they molt from green to white. In another moth, Nemaria arizonaria, when the young caterpillars perch and feed on oak catkins in the spring they resemble what they eat. Later—by summer, when they perch on twigs and eat leaves—they molt into a new form that resembles twigs.
For sheer number and variety of disguises in the same species, I vote for the Abbott’s sphinx moth, Sphecodina abbotti. Its caterpillar transforms inself through an amazing series of four disguises—a noxious insect, two different kinds of camouflage, and a snake. I made the acquaintance of these caterpillars at the University of Minnesota biological station at Lake Itasca, where I found three different forms of the caterpillar on the same food plant, wild grape.
The first four instars of all abbotti caterpillars are chalky white and thus conspicuous on green grape leaves. However, they curl up to resemble larvae of a cimbicid wasp. Cimbicid larvae are chemically protected—they can squirt a defensive fluid from glands along their sides. Apparently the young abbotti caterpillars mimic this distasteful model, because they do not have a “horn” at the end of the abdomen like other sphinx moth caterpillars (hence the common name, hornworms); instead, that structure is altered to look like a yellow translucent drop of fluid. It is unlikely that color, structure, and behavior would all converge to accidentally mimic the wasp larva, especially since the caterpillar’s appearance changes not partially but drastically when it molts into its last larval instar.
More startlingly, rather than just changing into a single totally different “uniform,” it morphs into either of two possible forms that are not only different from the previous form but also strikingly different from each other. One form is brown and streaked with black. This form is nearly invisible on a background of brown grape bark, where it hides in the daytime. At night it comes up to the leaves, and after finishing feeding on a grape leaf it snips off the remainder of the uneaten leaf and crawls back down and hides, staying immobile throughout the day while pressing itself tightly against the old growth of flaking grapevine bark. The other, rarer form of the same (fifth) instar of the same caterpillar on the same plant has large luminous pea green patches on its back and along its sides. This form feeds in the daytime and does not perch on old grapevines that have bark; instead, it stays on the young, smooth green grape stems.
The adaptive significance of simultaneously having two wildly contrasting forms of the abbotti sphinx moth in the last instar caterpillars on the same food plant is obscure. The brown form is clearly, in both appearance and behavior, adapted to hide on bark of grapevines (and Virginia creeper, another of its food plants). But the visually striking form with the green patches appears to be an anomaly with an as yet unknown selective advantage. I speculate that it is so different from the other that a predator who finds one form may be too distracted to search for and see the other. As already mentioned, a bird that has found a particularly juicy morsel will search for others that look like it. If a bird finds one caterpillar form on a grape plant—say, the bark mimic on a grape stem—it will search for others of the same type and in the same setting. It will thus, by knowing what it is looking for, more easily miss what is different. This is indeed the effect I tested with the students and the poplar sapling: some students searched an hour before finding the first caterpillar, but then after they found the first one they almost immediately found the second. A very common caterpillar, no matter how well camouflaged, is likely to be found eventually, and it is thus dangerous for an edible caterpillar to be on a bush with other edible company of the same appearance. However, one that is wildly different from that company has a good chance of not being noticed.
Fig. 19. The hind end of most sphinx moth caterpillars has a “horn,” as in this tobacco hornworm, Manduca sexta.
Neat as such tricks of the caterpillars in their game of hide-and-seek with predators and parasitoids might be, the question of mechanism always arises. How can two different morphs of the same age manage to be on the same food plant at the same time? Do some moths lay eggs that develop into only one form, whereas other individuals of the same moth species lay eggs that develop into the other form and then randomly lay their eggs on the same plant? Or are there instead two different morphs contained within any one individual moth? Alternatively, the different morphs could result from a developmental switch that is activated by an external cue, perhaps the mere presence of other caterpillars in the vicinity. A caterpillar cannot readily afford to leave its food plant, but changing its disguise may be almost equivalent, or even better, because it still retains the food. The presence of others could be the cue for such induction into the other (rarer) morph, since crowding causes a dramatic color change in another sphinx moth caterpillar, Erinnyis ello (Schneider 1973).
Fig. 20. Four disguises of Abbott’s sphinx caterpillar. The typical hornworm horn is adapted to look like a drop of yellow fluid in the young caterpillar; later, it looks like an eye in the mature larva, which mimics a snake.
Both of the final instar forms of the abbotti sphinx caterpillar rely on blending in so as not to be noticed, and this requires that they don’t move. No matter how well camouflaged a caterpillar is, it is likely to become dead meat if it moves when a bird is nearby. But what happens when the larva leaves the food plant and must crawl along the ground in order to search for a pupation site? Remarkably, Abbott’s sphinx caterpillars then take on a fourth disguise: both morphs now switch to the same disguise. The mottled green form darkens, and the other form stays brown. In both forms the “horn” then resembles a reptile’s eye, and the anal flap mimics a reptile’s mouth. The caterpillars also change their behavior to appropriately show off the “reptile” face when they are startled. When touched, they curl the end of their abdomen up and, eerily, look like a snake raising its head when it is ready to strike. To be sure, the caterpillar does not have two “eyes,” but to a small bird, even a one-eyed snake could be startling.
Most hornworms are large, and large size gives a caterpillar the option of mimicking an elongated scary or distasteful vertebrate animal. Abbotti sphinx moth caterpillars are not totally unique; the ground-dwelling caterpillar of the gallium sphinx, Hyles gallii, has one morph that is black with yellow spots, and thus has key features that mimic poisonous spotted salamanders, which are colored in that way as a warning. Among some large tropical sphinx moths, the caterpillars convincingly mimic a snake’s head (Miller et al. 2006), but in this case the effect of scales on the head comes from the folding of the front legs on the caterpillar’s underside, which is turned up in its snake display. The “eyes” (in this case, two of them) are derived from puffing out darkly pigmented skin on the sides of the head end. That is, the head of this snake mimic is fashioned from the front end, rather than the back as in abbotti. The snake head display is, in a butterfly, even found in the next stage, the chrysalis (Aiello and Silberglied 1978).
Coloration is an important component of many disguises, but color as such can also have another, equally important function. Dark coloration serves both to protect an animal from the sun and to increase the absorption of solar energy. Many butterflies are colored in ways that facilitate solar heating, which permits their flight muscles to operate in a cold environment. In caterpillars, instead, elevated body temperature speeds up the growth rate and greatly shortens the time until the relatively safe pupal stage is reached. In caterpillars, growth rate is perhaps one of the most critical factors in avoiding predators, because every day that the caterpillar stage can be shortened is a day when the gauntlet of both parasites and predators is avoided. Being black and exposed to the direct sun is, however, a two-edged sword. At the same time that it reduces the duration of exposure to predators and parasites, it also increases the intensity of selective pressure by making the animal more visible and more accessible to predation.
Fig. 21a and b. Snake head display of the caterpillars of the Central and South American sphinx moth, Hemeroplanes triptolemus; and of the chrysalis of the butterfly Dynastes darius (drawn from photographs in Miller et al. 2006).
Although I was working on thermoregulation of the tobacco hornworm Manduca sexta sphinx moths as a graduate student, and was aware of the importance of color in butterfly thermoregulation, I did not give much thought to the occasional “black sheep” caterpillar—one that was black rather than the typical camouflage green. I saw such caterpillars occasionally but passed them off as a curiosity or an aberration to be ignored. Fortunately, others didn’t see it that way, and through studies of this black mutation fundamental discoveries were made about nature versus nurture.
In 1973, Jim Truman and colleagues determined that the black mutant is not just the result of a new gene which codes for more melanin. Instead, the melanin deposition in the caterpillar’s skin results from a lowered level of the juvenile hormone (a key hormone for development in all insects’ metamorphosis as well as in their reproduction). Applying a minute amount of juvenile hormone to a black tobacco hornworm caterpillar reverses its color back to the “normal” green. However, it is apparently not just the amount of the hormone as such that determines the degree of color change. Instead, there is a specific threshold that tips the balance; furthermore, evolution works not by varying the amounts of hormone, but by shifting the threshold where the color change occurs (Suzuki and Nijhout 2006). In a related species, the tomato hornworm, Manduca quinquemaculata, the caterpillars develop black coloration when the temperature is 68°F or colder and green when it is 82°F or hotter. Are the color shifts adaptations to temperature, in which the advantage of sunshine to speed up feeding and growth rate exceeds the disadvantage of potentially being eaten?
We humans cannot change into any radically different body color, body shape, or behavior. We have evolved to maintain a certain homeostasis, or a status quo, that has proved to be adaptive in the past. However, the genes of a butterfly are the same as those in a caterpillar. The difference is which are turned on or off, and when. It’s all “environment” as well—in this case mostly the internal environment that keeps changing through development. Whenever I see a weight lifter, a runner, a mathematician, an actor, a sumo wrestler, or a dancer, I am reminded that, like caterpillars, we do have the capacity to accomplish amazing changes, and these are sometimes in response to simple, subtle cues, which are like switches that control development. No one develops with a complete predetermination of the features and faculties that he or she will eventually come to “own.” To the contrary, although we are built from pretty much the same blueprint, many of our specific, individual “talents” can be activated only if we exceed a certain threshold of effort, but probably this threshold is also specific to each individual. I was reminded of this while training to metamorphose from a slow cold-weather-adapted animal that conserved energy and heat to one who could expend energy at high rates and dissipate heat as fast as possible. If in a caterpillar a mere visual stimulus can change gene expression affecting development, then why not exercise in us?
Once an end result is achieved, it is hard for us to imagine an alternative that has proceeded along a different developmental trajectory without crediting it to magic or “talent.” When we see in others something that we find incomprehensible for ourselves, it is easy to pass this off as “genetic.” Naturally, it is exactly that; but this description still omits the essence of development, the miracle on the miracle. The possibility of individual caterpillars to generate amazingly different forms makes me appreciate what is possible in the debate over nature versus nurture. Much of what we are and become depends on minute subtleties, and that gives me hope in the reality of free will, and its power if we choose to exert it.