Who Says Swallowtail Butterflies Are Distasteful? Tell It to the Anole!

Most naïve predators learn the relationship between aposematism and unpalatability through direct experience, and anoles may be no exception. Batesian mimicry aside, the unpleasant physiological consequences that follow sampling of aposematic prey establishes this relationship. Given the enormous diversity of coloration in butterflies, however, it sometimes is difficult to discern what color patterns might or might not be aposematic. In contrast, the bright yellow banding pattern that overlies a black background in the wing coloration of the “zebra longwing” (Heliconius charithonia) seems unambiguous as warning coloration. Heliconius butterflies use passion vines (Passiflora sp.) exclusively as host plants, and these vines contain harmala alkaloids, cyanogenic glycosides, and other generally toxic compounds.

In the summer of 2014 Dr. Darrell Kemp (Macquarie University) and I ran an oviposition plant choice experiment with H. charithonia in a large tropical greenhouse. After rearing approximately 100 butterflies individually from eggs to adulthood on one of two Passiflora species, freshly emergent adults were released to fly freely in the greenhouse, mate, and lay eggs. It was there that we discovered to our horror that Anolis sagrei, which is extremely abundant in our area (Lakeland, FL), found these butterflies attractive as prey items. We first noticed a problem as we detected increasing numbers of the butterflies with bites taken out of their wings, and then witnessed an A. sagrei male stalking and capturing one of the butterflies. We became focused on attempting to save our time-consuming experiment by ridding the greenhouse of the anoles, but by the time few lizards remained in the greenhouse our experimental butterfly population had been decimated. Although A. sagrei may not have been responsible for most of the butterfly deaths, regularly finding dead and living butterflies with bites taken out of their wings suggested that many anoles were attacking the butterflies. We never seriously considered converting our host plant choice experiment into a study of how quickly anoles learn to avoid chemically defended aposematic prey, but in retrospect perhaps we should have done so.

Butterflies in the genus Battus (including Battus polydamus pictured in this post) feed as larvae on species of Aristolochia, which contain the potent alkaloid aristolochic acid. It would have been interesting to observe the anole afterwards for physiological effects of the toxin, but without an experimental test we still would not know if the lizard avoided this butterfly in the future. Skip Lazell’s suggestion of a controlled experiment is a good one. I have actually tried this using A. sagrei and milkweed bugs, to test the importance of memorability on learning in these lizards. The bugs were painted orange-on-black (control) or entirely black, and were reared on milkweed seeds or sunflower seeds. Results were inconclusive, as repeated tests with subjects housed in plastic “small pet” containers proved to be less than ideal for choice tests. However, chemical assays (e.g., HPLC) coupled with a good experimental setup for a learning experiment, such as past work conducted by Manuel Leal and Brian Powell (see post “Is An Anole Smarter Than a Fifth Grader?”), could provide some interesting insights into how anoles learn about chemically defended aposematic prey.