Defensive coloration and behavior in insects: function, sensory perception mechanism, and evolution

Abstract

Cryptic color patterns in prey are classical examples of adaptations to avoid predation, but we still know little about behaviors that reinforce the match between animal body and the background. From observations of geometrid moths, Hypomecis roboraria and Jankowskia fuscaria, I determined that the positioning behavior, which consists of walking and turning the body while repeatedly lifting and lowering the wings, resulted in new resting spots and body orientations in J. fuscaria, and in new resting spots in H. roboraria. The body positioning behavior of the two species significantly decreased the probability of visual detection by humans, who viewed photos of the moths taken before and after the positioning behavior. This implies that body positioning significantly increases the camouflage effect provided by moths cryptic color pattern regardless of whether the behavior involves a new body orientation or not. However, this positioning behavior is not always performed: some moths stay put on the initial landing position. We hypothesized that the moths decision of whether or not to re-position itself is related to its crypticity at the landing spot. We determined the crypticity from a detection task experiment, in which human foragers searched for the moths in photos of moths at their landing spots. Moths that landed on the less cryptic positions were more likely to reposition themselves to the more cryptic positions. In contrast, moths that already landed on substantially cryptic positions were less likely to reposition themselves. Next I explored how a moth finds an appropriate resting position and orientation. Here, I used a geometrid moth Jankowskia fuscaria to examine i) whether a choice of resting orientation by moths depends on the properties of natural background, and ii) what sensory cues moths use. We studied moths behavior on natural (a tree log) and artificial backgrounds, each of which was designed to mimic one of the hypothetical cues that moths may perceive on a tree trunk (visual pattern, directional furrow structure, and curvature). We found that moths mainly used structural cues from the background when choosing their resting position and orientation. Then I tested through which sensory organs (which are directly related to sensory information types) moths perceive bark structures to find adaptive resting orientations. We amputated (or blocked) one of the hypothetical sensory organs from moths (antennae, forelegs, wings, and eyes) and tested whether they were still able to perceive bark structures properly. We found that moths use visual information from eyes and tactile information from wings to perceive bark structure and to adopt cryptic resting orientations. These studies collectively show how behavior mediates the camouflage of moths in nature and how moths perceive background information to find a cryptic spot. Next. I tackled the questions about a new strategy of chemically defended prey to show warning coloration to predators. Aposematic coloration in prey promotes its survival by conspicuously advertising unpalatability to predators. Although classical examples of aposematic signals involve constant presentation of a signal at a distance, some animals suddenly display warning colors only when they are attacked. Characteristics of body parts suddenly displayed, such as conspicuous coloration or eyespot pattern, may increase the survival of the prey by startling the predator, and/or by signaling unpalatability to the predators at the moment of attack. The adaptive value of such color patterns suddenly displayed by unpalatable prey has not been studied. We experimentally blackened the red patch in the conspicuous red-white-black hindwing pattern displayed by an unpalatable insect Lycorma delicatula (Hemiptera: Fulgoridae) in response to predators attack. There was no evidence that the presence of the red patch increased prey survival over several weeks. Next I asked the adaptive significance of this hidden-warning coloration and explored the mechanistic question how it provides survival benefits to the bearer. The main advantage of aposematism is that it enhances learning by predators to avoid the prey. Using wild birds (Parus minor) and novel prey models, I tested whether hidden conspicuous display of defended prey accelerates the avoidance learning rate of predators and how does it compare with the typical conspicuous/non-conspicuous signal. We found the evidence that hidden aposematic signal indeed accelerates the avoidance learning rate of predators by two stages: i) enhancing the learning rate of the association between non-conspicuous (normal) state of the prey and prey defense, ii) promoting rejection after an attack has occurred by showing hidden conspicuous coloration. We show here the unique defensive coloration of prey which may provide dual benefits of crypsis and aposematism and highlight the specific mechanisms that hidden-aposematic signal provide the prey with survival benefits.