A Natural Toxic Defense System: Cardenolides in Butterflies versus Birds

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Abstract
We have verified that wild birds can become conditioned to reject naturally toxic insects either visually (experiment 1) or by taste (experiment 2). We have also verified, however, that unconditioned taste rejection of noxious chemicals by wild birds also occurs (experiment 3). Such unconditioned responses to the aposematic visual and taste cues of many insects, in fact, often appear to be as important as, or more important than, conditioned responses. In a large number of laboratory feeding experiments with wild birds as predators of aposematic insects, initial and/or long-term rejection occurs without prior laboratory conditioning experience. Although in some experiments the birds may have previously been exposed to (and therefore perhaps conditioned by) the aposematic prey in the wild, other experiments have used naive birds or insects whose ranges do not overlap those of the birds. Wiklund and Jarvi, for example, tested the response of 47 naive hand-raised birds of four species to five aposematic insect species, and found that 69/136 (51%) insects were rejected visually without even tasting, while 63 were tasted and then rejected. Only four of the insects were actually ingested. Similarly, in Bowers' study of the response of Massachusetts blue jays to aposematic western U.S. Euphydryas butterflies, several blue jays consistently rejected the butterflies visually or by taste without having eaten any. While these studies were not designed to separate neophobic effects from innate visual and/or taste aversions, they do differentiate between conditioned and unconditioned responses. Since both conditioned and unconditioned rejections can be demonstrated in the lab by insectivorous birds, and our available field evidence does not yet let us distinguish the mechanisms behind the observed patterns, our initial question, of the relative importance of conditioned versus unconditioned rejection mechanisms in different natural situations, is not yet answerable. The most important requirement of a food-rejection strategy is that it prevents both poisoning and starvation. We have shown, however, that rejection of a noxious insect by a bird can take place at four distinct levels (visual, non-destructive taste sampling, destructive taste sampling, or post-ingestional physiological rejection), the first three of which may be either unconditioned or conditioned by a physiological reaction to ingestion.(ABSTRACT TRUNCATED AT 400 WORDS)