The struggle for safety: effectiveness of caterpillar defenses against bird predation

Abstract

The effectiveness of anti‐predator traits, such as warning signals and camouflage, has rarely been quantified from a phylogenetic community ecology perspective. Here we use a phylogenetic comparative analysis to test the association between several putative anti‐predator traits and bird predation risk in an assemblage of caterpillar species. We synthesize eight years of field and laboratory study of a temperate forest community, including a four‐year bird exclusion experiment that provided comparative measures of bird predation risk for 38 caterpillar species from a phylogenetic community. We then conducted a phylogenetic generalized least‐squares and information‐theoretic model selection analysis of warning signals (aposematism or mimicry), camouflage (crypsis or masquerade), and behavioral responses to physical attack as predictors of bird predation, while also accounting for putatively important effects of the abundance, mean body size, and phenology of caterpillar species. The most behaviorally specialized caterpillar species possessing warning signals experienced the lowest bird predation risk, supporting aposematism theory and highlighting the role of prey behavior in the visual signaling of predators. Among the camouflaged caterpillar species, those with the greatest latency to detection by human proxy predators experienced the lowest bird predation risk, supporting camouflage theory. Caterpillar behavioral responses to physical attack, however, predicted increased bird predation risk among camouflaged caterpillars. Although caterpillar abundance, body size, and phenology were expected to be important based on inference from optimal foraging theory and previous field observations, these factors had limited predictive power. This study provides methodologically unique evidence for the importance of morphological and behavioral components of primary, visual defenses of caterpillars against their avian predators in a natural community.

Material affects attack rates on dummy caterpillars in tropical forest where arthropod predators dominate: an experiment using clay and dough dummies with green colourants on various plant species

“…Although birds hunt caterpillars mostly visually, chemical clues given off by caterpillars tend to be more important to predacious arthropods such as ants. Indeed, specific characteristics of colouration can render insects more or less vulnerable to bird predation (Cuthill et al, 2006;Stevens & Ruxton, 2012;Farkas et al, 2013;Lichter-Marck et al, 2014). This is in contrast to temperate systems where (dummy) caterpillar colouration has a large influence on predation Mappes et al, 2014;Singer et al, 2014) but material of dummy caterpillars does not (e.g., dough, clay; ).…”

Dietary specialization is conditionally associated with increased ant predation risk in a temperate forest caterpillar community

“…As a possible explanation for the ineffective defenses of dietary specialist caterpillars against ant predation, we suggest that their chemical defenses are especially weak, at least during early larval stages when ants would be predominant predators (Remmel et al, ). We note the high frequency of camouflage as a visual defense strategy of caterpillars in the temperate forest community we studied (Lichter‐Marck et al, ). Like visual aposematism (Zvereva & Kozlov, ), visual camouflage is expected to be more effective against selective, visual predators (birds) than against opportunistic, nonvisual predators (ants).…”

“…The most important ant predators of caterpillars in this community are Formica neogagates , Camponotus chromaiodes , and Camponotus pennsylvanicus (Clark, Farkas, Lichter‐Marck, Johnson, & Singer, ). As in previous studies of this community that focus on bird predation of caterpillars (Lichter‐Marck et al, ; Singer et al, , ), we conducted fieldwork at three sites (Cockaponset State Forest, Haddam; Hurd State Park, East Hampton; Millers Pond State Park, Durham (all in Middlesex County, CT), each with six spatially replicated experimental blocks (ca. 1 ha in size) containing each tree species.…”

Evolution of ontogenic change in color defenses of swallowtail butterflies

“…Natural selection imposed by predation has led to the evolution of antipredatory, morphological, behavioral, and life historical defenses in prey species (Abrams, ; Brodie & Brodie, ; Langerhans, ; Schmidt, ). Prey species may also reduce the risk of predation from visually hunting predators using color defense strategies such as masquerade, crypsis, and aposematism (Booth, ; Caro, Sherratt, & Stevens, ; Cuthill et al., ; Higginson & Ruxton, ; Lichter‐Marck, Wylde, Aaron, Oliver, & Singer, ; Skelhorn, Rowland, Speed, & Ruxton, ; Speed, ). Masquerading prey resemble some inedible objects (at times, objects aversive to their predators, such as bird droppings) in their natural environment and are misidentified by predators, whereas cryptic prey avoid detection by matching the color and pattern of their body with those of the background (Duarte, Flores, & Stevens, ).…”

“…The globally distributed swallowtail butterflies (family Papilionidae) serve as an excellent model to study the evolution of defensive coloration. Their distinct lifestages in a complex life cycle experience differential predation risk from visually hunting predators such as insectivorous birds, reptiles, and mammals that detect prey using body size and motion (Greeney, Dyer, & Smilanich, ; Johansen et al., ; Lichter‐Marck et al., ). Swallowtail caterpillars progressively increase in body size with development and in motion levels, due to increase in foraging demands and during pupation, which attracts attention of motion‐detecting, visually hunting predators.…”