Having multiple plastic responses to a change in the environment, such as increased temperature, can be adaptive for two major reasons: synergy (the plastic responses perform better when expressed simultaneously) or complementarity (each plastic response provides a greater net benefit in a different environmental context). We investigated these hypotheses for two forms of temperature-induced plasticity of Battus philenor caterpillars in southern Arizona populations: color change (from black to red at high temperatures) and heat avoidance behavior (movement from host to elevated refuges at high host temperatures). Field assays using aluminum models showed that the cooling effect of the red color is greatly reduced in a refuge position relative to that on a host. Field assays with live caterpillars demonstrated that refuge seeking is much more important for survival under hot conditions than coloration; however, in those assays, red coloration reduced the need to seek refuges. Our results support the complementarity hypothesis: refuge seeking facilitates survival during daily temperature peaks, while color change reduces the need to leave the host over longer warm periods. We propose that combinations of rapid but costly short-term behavioral responses and slow but efficient long-term morphological responses may be common when coping with temperature change.

Adaptive phenotypic plasticity is a key mechanism by which organisms deal with variation in many different aspects of their environment. Adaptive plasticity can occur in any trait, from aspects of biochemistry and morphology to behaviors. Because so many different traits can be plastic, organisms often respond plastically to a given change in their environment, such as an increase in temperature, with adaptive changes in multiple traits. Nevertheless, how these different plastic responses interact with each other and evolve together has received little attention. My research addresses these potential interactions among plastic traits and proposes new hypotheses regarding the causes and consequences of these interactions. It does so by focusing on heat avoidance in the caterpillars of Battus philenor (the pipevine swallowtail) which involves two distinct plastic mechanisms. First, the caterpillars can change color when they molt, a form of morphological plasticity in which they develop a red color under high temperatures which cools them by absorbing less solar radiation. Second, when the caterpillars become too hot, they will leave their host to seek cooler thermal refuges, a case of behavior as a form of plasticity. In terms of function, I demonstrated through field research that these two responses to high temperatures are largely redundant. Behavior provides a much stronger and faster response than color change, and red coloration provides little additional cooling when on a refuge. Instead, the primary benefit of color change is that it reduces the use of refuge seeking behavior, allowing the caterpillars to stay on their hosts longer. Using laboratory experiments, I demonstrated that this change in the use of refuge-seeking behavior with color occurs because color changes the cue for the behavior, body temperature, rather having any effect on how the caterpillar responds to that cue. Alternatively, similar experiments on caterpillars of varying sizes show that developmental size change lowers the body temperature at which caterpillars leave their host, demonstrating a change in the response to the cue (although larger caterpillars are also warmer, so both mechanisms are likely relevant for how size changes the expression of behavior). All of my research to this point was conducted on the local population in southern Arizona, which experiences quite high temperatures, but B. philenor is also found in much cooler environments, such as the Appalachian Mountains. Given this variation in their thermal environment, I used common garden experiments to compare the capacity for color change and refuge-seeking among B. philenor caterpillars from across the species range. Both color change and refuge seeking not only occurred in all populations, but also had the same reaction norms, occurring at the same temperatures and to the same degree. This is particularly notable for color change, which is not observed in the wild in northeastern populations, and thus has persisted despite minimal if any use. Overall, I have shown that studies of plasticity need to account for plasticity in different traits as well as the interactions between these forms of plasticity. My research on B. philenor provides a model for how to address these interactions, which future research can extend to additional organisms and environmental circumstances.

Aggregative feeding is widespread in Lepidopteran larvae suggesting that this behavior serves on adaptive function. Many studies of the potential benefits of aggregative feeding in Lepidopteran larvae have been conducted. However, no studies have directly examined the benefits of cryptic larvae being both chemically defended and gregarious. Group feeding occurs disproportionately more in chemically defended larvae than in larvae that have no chemical defense. Most of these larvae are cryptic when they are most highly aggregated and most vulnerable to predation. In this study, the benefits of group feeding in terms of decreased predation were explored in first instar larvae of pipevine swallowtail larvae, Battus philenor, a species that exhibits chemical sequestration. Contrary to our expectation, we found that groups of larvae fed a diet with high levels of the toxin aristolochic acid, which they sequester naturally and use as a defense against natural enemies, had significantly lower survivorship due to predation in both the field and in the laboratory experiments compared to groups of larvae fed a diet with low aristolochic acid content. We also found that aristolochic acid does not deter the generalist predator Hippodamia convergens, the ladybird beetle, suggesting that this compound is not a universal predator deterrent as previously assumed. Thus, instead of finding a benefit to group feeding and chemical defense in cryptic larvae, we have found a negative impact of group feeding in this population of B. philenor. Based on this evidence, we speculate that other benefits of group feeding might be outweighing the negative consequences of increased predation during the first instar. Future research on chemical defense, aposematism, and aggregative feeding should take into consideration that chemical defenses might not be universally effective against all natural enemies.

abstract: Warning coloration deters predators from attacking prey that are defended, usually by being distasteful, toxic, or otherwise costly for predators to pursue and consume. Predators may have an innate response to warning colors or learn to associate them with a defense through trial and error. In general, predators should select for warning signals that are easy to learn and recognize. Previous research demonstrates long-wavelength colors (e.g. red and yellow) are effective because they are readily detected and learned. However, a number of defended animals display short-wavelength coloration (e.g. blue and violet), such as the pipevine swallowtail butterfly (Battus philenor). The role of blue coloration in warning signals had not previously been explicitly tested. My research showed in laboratory experiments that curve-billed thrashers (Toxostoma curvirostre) and Gambel's quail (Callipepla gambelii) can learn and recognize the iridescent blue of B. philenor as a warning signal and that it is innately avoided. I tested the attack rates of these colors in the field and blue was not as effective as orange. I concluded that blue colors may function as warning signals, but the effectiveness is likely dependent on the context and predator. Blue colors are often iridescent in nature and the effect of iridescence on warning signal function was unknown. I reared B. philenor larvae under varied food deprivation treatments. Iridescent colors did not have more variation than pigment-based colors under these conditions; variation which could affect predator learning. Learning could also be affected by changes in appearance, as iridescent colors change in both hue and brightness as the angle of illuminating light and viewer change in relation to the color surface. Iridescent colors can also be much brighter than pigment-based colors and iridescent animals can statically display different hues. I tested these potential effects on warning signal learning by domestic chickens (Gallus gallus domesticus) and found that variation due to the directionality of iridescence and a brighter warning signal did not influence learning. However, blue-violet was learned more readily than blue-green. These experiments revealed that the directionality of iridescent coloration does not likely negatively affect its potential effectiveness as a warning signal. / Dissertation/Thesis / Doctoral Dissertation Biology 2015