THE HUNGRY BIRD Caterpillar Tricks, Part 2 Dave Leatherman Editor s note: Part 1 of this article appeared in the October 2013 issue of Colorado Birds Vol. 47 No. 4. Bad Taste For me, it s eggplant or India Pale Ale. Try as I might, I don t like the taste of certain food and drink. Birds are no different. In some cases the deterrent might be outright toxicity, while in others a bird not eating a particular caterpillar might be just a preference, consistent across an entire species or limited to an individual bird. We all know about the Monarch butterfly (Danaus plexippus). All life stages of this iconic associate of milkweeds are generally unpalatable to birds. Also, the caterpillars of the checkerspot butterflies, of which Colorado has at least five species, feed on plants like Indian paintbrush, honeysuckle and certain penstemons known to contain potent bird repellants called iridoid glycosides. My friend and mentor of sorts on all things chemical, Dr. Frank Stermitz, did extensive research during his career at Colorado State University on the ways animals cope with toxic plants. Among the findings that Frank and others have gathered are that animals eating unsavory plants get away with consuming potentially malicious molecules by 1) modifying them into less troublesome compounds, 2) gathering and stashing them away (the fancy term is sequester ) or 3) isolating and passing them as quickly as possible out the end of the digestive tract. The Monarch caterpillar sequesters, having hidden away in various body cupboards (mostly in the wings and abdomen) significant quantities of milkweed-produced cardenolides (steroids that are particularly bad for the heart.) They even give birds fair warning with their bright stripes (called aposomatic coloration. ) In the lab, most birds given no choice but to feed on monarch caterpillars immediately throw them up. Exceptions exist and the game is ever changing, particularly in regard to adult Monarchs. Certain birds have higher tolerances to chemicals detrimental to most birds. These few, that include jays and thrashers, have learned to eat only body parts lowest in the bad chemicals (wing muscles in the thorax, for example) (Barbosa 1988.) On the Hawaiian island of Oahu, two introduced bulbuls (Pycnonotus cafer and P. jocosus) with apparent tolerance of cardenolides heavily prey on caterpillars, pupae and resting adults. Such pressure is leading to the emergence of a white morph that suf- 72 Colorado Birds Winter 2014 Vol. 48 No. 1
fers much less predation than normal orange individuals (Stimson 1990.) It sounds like evolution just might be catching on. On their Mexican wintering grounds, the Black-backed Oriole (Icterus abellei) and our familiar Black-headed Grosbeak prey heavily on adult Monarchs. They accomplish this feat through a combination of a natural, moderate tolerance for cardenolides, a preference for male Monarchs (which are less toxic than females and identifiable by the black spot ( androconium ) on their lower wings) and by taking periods of days off between major feeding episodes, presumably to cleanse their systems (Brower 1985.) Carrying the tactic a bit further are creatures that mimic badtasting peers or simply things that taste bad. They may or may not taste OK themselves, but just want the world to think otherwise or know for sure, as the case may be. The Viceroy butterfly (Limenitis archippus) adult looks a lot like a Monarch and also tastes bad. This is an example of Mullerian mimicry (where two poisonous species with common predators select for inviduals that look like their cohort, in this case for the reason of being avoided.) The caterpillars of certain butterflies including the Viceroy, Weidemeyer s Admiral, and the early stages of certain swallowtails remarkably resemble bird droppings (Fig. 6), an example of Batesian mimicry (whereby looking undesirable to a common enemy pays off in better survival for the copycat) (Ritland 1991). Fake Eye Spots Caterpillars often sport scary patterns that appear to be large eyes. Such fake eyespots are often brightly colored (blue, orange, etc.) and are situated on the head near the smaller, less conspicuous real eyes, or on the thorax (the segment behind the head to which the true legs are attached) (Fig. 7). Familiar examples include the late larval stages of swallowtail butterflies and skippers. The Spicebush Swallowtail of the east (rarely seen in Colorado) has fake eyespots thought to resemble a snake s. To my brown eyes, Fig. 6. Young Black Swallowtail caterpillar (Papilio polyxenes), a bird dropping (robin?) mimic on fennel, Lamar, CO. Colorado Birds Winter 2014 Vol. 48 No. 1 73
the blue eyes of our few species of Yellow and Black Tiger Swallowtails seem more a flirt than an ominous glare. Interpretation depends on the beholder. Startling Movements, Sounds and Ejections Upon detection, caterpillars can rise up on their haunches like a sphinx ( Boo! ) (see Fig. 10), wriggle violently as if on a frying pan (many leafrollers do this when removed from their wrap), emit a wad of juice from their mouths (like captured grasshoppers offering a bubble of disgusting tobacco juice ), shunt blood into long forked anal prolegs and wildly wave them around (the white furcula, Furcula borealis) producing a rather loud whistle by emitting air under pressure from abdominal breathing pores (the Walnut Sphinx, Amorpha juglandis) eject acid from the front of their thorax (the Black-etched Prominent, Cerura scitiscripta), and even force the sudden appearance of strange, brightly-colored, foul-smelling body parts (most swallowtails.) See the close of this article for more about pop-up anatomy (Wagner, 2005). Quick Get-away In contrast to some caterpillars that rely on motionlessness to live another day, others do just the opposite. Anyone attempting to collect an insect soon learns gravity is a reliable force on Earth and insects know it/use it. Upon sensing nearby danger, many, including caterpillars, will crawl very quickly. Most simply let go of whatever their true legs and prolegs are gripping at the moment and free-fall. One that hits the ground before it hits a mandible, your hand, jar or beating sheet is probably a successful escapee. Their coloration is part of it. Leaf litter, cracks and crevices and the sheer complexity of their new background is most of it. And in their Fig. 7. Duskywing Skipper (Erynnis sp.) on Gambel oak from north of Dolores, CO, showing fake, bright orange eyespots on the head capsule. encounters with me, I never seem to be wearing the right glasses, which helps their chances immensely. 74 Colorado Birds Winter 2014 Vol. 48 No. 1
Difficulty with Swallowing In general, woodland bird behavior indicates hairless, naked, nofrills caterpillars are more desired than hairy ones (i.e. hirsute. ) They are easier for birds to handle, don t sting or irritate as much, go down easier and tend to have more digestible matter per capture. Insect hairs are called setae and they have been in play long enough in the history of life that setal variety and function are now impressive. Some aid in disguise due to coloration. Others break up an otherwise eye-catching silhouette. Some are stiff and secondarily branched into spines. Some clump into imposing, tooth-brushy collections called tussocks (Fig. 8). Some are long and fine and, in some cases, may break off easily making a would-be predator whiff, if that s all it grabs. Or if an ambush is successful, such hairs could clog a throat, perhaps thwarting a swallow. Some warn of bad, even deadly taste. Some deliver potent venom. If you ve ever encountered the various plants with the common name nettles, you know somewhat the feeling a bird would have on the inside of its throat if it tried to down a caterpillar sporting so-called urticating spines. A Made-up Story That Could be True In closing, and to illustrate one possible scenario of how this all might work, imagine a newly fledged American Robin in a Lamar backyard. It s spotted with its own camouflage, but orange enough to know who its parents are. Flush with excitement about its ability to fly, it is simultaneously wide-eyed and green to the art of self-feeding. A plump Black Swallowtail caterpillar (Fig. 9) chowing some blue ribbon fennel, conspicuous by its size and referee stripes, focuses the bird s gaze. It glides from the top of the privacy fence to the ground and hops to the garden edge. Newly weaned from its jam diet (as in, Mom and Dad jammed whatever they wanted to the bottom of its gullet) the nowsolo, tentative young bird pokes once at the air close to the larva. Feeble. Suddenly remembering what its elder taught yesterday Fig. 8. A Pine Tussock moth (Dasychira probably grisefacta) armed with an array of hairs and spines deterrent to bird predation (on ponderosa pine in the Wildcat Hills of western Nebraska). Colorado Birds Winter 2014 Vol. 48 No. 1 75
about grasshopper vulnerability, it jabs again, this time for the head. But where s the head? Those black spots on the white segment at one body end look quite like those on the other end. Ah yes, the head is usually at the end showing narrow legs. The second peck, a bit off-target, lands behind the real head, indents the thorax, and WHOOSH! Up shoots a pair of shiny, half-inch horns that look and smell like something adorning a snail made of rotten oranges (Fig. 10). Whoa! Welcome to the newness of life, little robin, and the peculiar caterpillar organs called osmentaria. Strictly designed for shock and awe, their jack-in-a-box pop did the job, at least for the moment, with a tot of this age. Adult robins that have been around the yard a time or two do not all fall for such pranks (Fig. 11). Particular robins seem to have learned that confusing spots, a clown suit and stinky horns are mere bluffoonery between them and a full stomach. But maybe, just maybe, those swallowtail tricks, in combination, shift the concentration of one robin, or one brood of robins, over to easier pickings: say, earthworms. And maybe a fair number of fat caterpillars metamorphose into hard-to-see chrysali; a few black and yellow butterflies emerge sporting their own survival gear: breakaway tails, patterns and eyespots; copulation occurs; eggs are laid; it actually rains on the southeastern plains; the fennel sprouts next spring and one small cycle amid the many comes full. Like frass and copulation, trickery happens. All photos by Dave Leatherman unless specifically noted otherwise. Fig. 9 11. From L to R, undisturbed mature Black Swallowtail caterpillar, disturbed Black Swallowtail caterpillar rising up in threat posture and showing half-extended osmentaria, and undeterred adult robin with captured Black Swallowtail caterpillar (all Lamar, CO). Middle photo by Janeal Thompson 76 Colorado Birds Winter 2014 Vol. 48 No. 1
ACKNOWLEDGMENTS The author thanks Dr. Frank Stermitz and Janeal Thompson for their helpful reviews of the manuscript. I appreciate the use of Ms. Thompson s osmentaria photo. LITERATURE CITED Barbosa, Pedro; Deborah Kay Letourneau (1988). Novel Aspects of Insect-plant Interactions. Wiley-Interscience. pp. 29 31. Brower, L.P. and W.H. Calvert. 1985. Foraging dynamics of bird predators on overwintering monarch butterflies in Mexico. Evolution 39:852-868. David L. Wagner (2005). Caterpillars of Eastern North America. Princeton University Press, Princeton, NJ Ritland, D.; L. P. Brower (1991). The viceroy butterfly is not a Batesian mimic. Nature 350 (6318): 497 498. Stimson, John; Mark Berman (1990). Predator induced colour polymorphism in Danaus plexippus L. (Lepidoptera: Nymphalidae) in Hawaii. Heredity 65 (3): 401 406. Dave Leatherman, daleatherman@msn.com CFO Winter Field Trip: Red Rocks and Beyond Join CFO Director Mike Henwood and Vice President Christian Nunes on Sunday, February 9th on this journey through Front Range foothills and mountain communities in a search for winter finches and other seasonal birds of the area. We will meet at 8:00 a.m. at the Red Rocks Trading Post and then continue to other sites where winter birds are showing up. Plan on carpooling to minimize parking needs where space is a concern and returning to Red Rocks by 1:00 p.m. Dress warmly and bring water and snacks. This trip is limited to 15 participants. Contact Christian at vicepresident@cfobirds.org if you wish to participate. Colorado Birds Winter 2014 Vol. 48 No. 1 77