Multimodal Aposematic Defenses Through the Predation Sequence

Abstract

Aposematic organisms warn predators of their unprofitability using a combination of defenses, including visual warning signals, startling sounds, noxious odors, or aversive tastes. Using multiple lines of defense can help prey avoid predators by stimulating multiple senses and/or by acting at different stages of predation. We tested the efficacy of three lines of defense (color, smell, taste) during the predation sequence of aposematic wood tiger moths (Arctia plantaginis) using blue tit (Cyanistes caeruleus) predators. Moths with two hindwing phenotypes (genotypes: WW/Wy = white, yy = yellow) were manipulated to have defense fluid with aversive smell (methoxypyrazines), body tissues with aversive taste (pyrrolizidine alkaloids) or both. In early predation stages, moth color and smell had additive effects on bird approach latency and dropping the prey, with the strongest effect for moths of the white morph with defense fluids. Pyrrolizidine alkaloid sequestration was detrimental in early attack stages, suggesting a trade-off between pyrrolizidine alkaloid sequestration and investment in other defenses. In addition, pyrrolizidine alkaloid taste alone did not deter bird predators. Birds could only effectively discriminate toxic moths from non-toxic moths when neck fluids containing methoxypyrazines were present, at which point they abandoned attack at the consumption stage. As a result, moths of the white morph with an aversive methoxypyrazine smell and moths in the treatment with both chemical defenses had the greatest chance of survival. We suggest that methoxypyrazines act as context setting signals for warning colors and as attention alerting or “go-slow” signals for distasteful toxins, thereby mediating the relationship between warning signal and toxicity. Furthermore, we found that moths that were heterozygous for hindwing coloration had more effective defense fluids compared to other genotypes in terms of delaying approach and reducing the latency to drop the moth, suggesting a genetic link between coloration and defense that could help to explain the color polymorphism. Conclusively, these results indicate that color, smell, and taste constitute a multimodal warning signal that impedes predator attack and improves prey survival. This work highlights the importance of understanding the separate roles of color, smell and taste through the predation sequence and also within-species variation in chemical defenses.

Aposematic Coloration of Moths Decreases Strongly along an Elevational Gradient in the Andes

“…For example, resources need to be allocated between defense and reproduction, sequestered plant secondary compounds need to be handled, modified and stored in the body, and certain traits may be advantageous against some predators, but not against others. Hence, for each species the balance between the costs and benefits of expressing defensive traits needs to be met [3]. In addition, potentially suitable secondary plant compounds to be sequestered for defense are not equally available in all host plants.…”

“…In contrast, many other Arctiinae species have wing patterns with colorful bright red, orange, yellow or green-blue spots often contrasting with a dark ground color (Figure 1). Their aposematic appearance is usually coupled with chemical defense, either using secondary plant metabolites sequestered from their larval host plants [11], or collected during the adult stage through pharmacophagy (e.g., [12,13]), or by de novo synthesis of toxic compounds by the insects [3]-yet detailed information is unavailable for most tropical species so far. As a result, colorful tiger and lichen moths are often times unpalatable, or even toxic, to their predators, and they signal their unpalatability through their visual appearance [9], in some cases also supplemented by acoustic signals that address bats as nocturnal predators [2,14].…”

Genetic colour variation visible for predators and conspecifics is concealed from humans in a polymorphic moth

“…Moreover, recent studies in other species have shown that UV may facilitate separation of incipient species as recently demonstrated in Colias butterflies (Ficarrotta et al, 2022) and that the differences in UV reflection may arise from novel duplication of the gene producing sex‐specific differences in reflectance as in Zerene cesonia butterfly (Rodriguez‐Caro et al, 2021). Previous experiments have shown that birds learn to avoid red wood tiger moths more effectively than yellow or white ones (Ham et al, 2006; Lindstedt et al, 2011; Rönkä et al, 2018), but the selection for visual signals may be altered due to multimodal signalling (Rojas et al, 2018; Winters et al, 2021). Also, avian predators may distinguish between the nuances in colouration among the genotypes as they, and wood tiger moths, perceive UV wavelengths that are beyond human perception (Henze et al, 2018).…”

Not just the sum of its parts: geographic variation and non-additive effects of pyrazines in the chemical defence of an aposematic moth

“…Predators can indeed use more than one cue to assess the toxicity of prey, so multiple defensive compounds can be used as a multimodal signal (Marples et al, 1994; Rojas et al 2019). A recent study found that wood tiger moth PAs can also provoke disgust reactions in wild birds (Winters et al, 2021). The presence of PAs alone did not deter the predators, but the combination of both pyrazines and PAs confers better defences to the moths (Winters et al, 2021).…”