Beyond masquerade: Grasping the predator prevents swallowing in a bird‐dropping‐like weevil

Animals possess various defensive strategies to avoid predation (Endler, 1991; Ruxton et al., 2018; Sugiura, 2020). Defenses that act before predator contact are defined as primary defenses, whereas those that function after contact are defined as secondary defenses (Ruxton et al., 2018). Among primary defenses, masquerade—where prey resembles a twig, leaf, pebble, or bird dropping—enables prey to avoid predation by being misclassified as an inedible object, even after detection (Skelhorn, 2015). However, masquerading prey may face increased predation risk when they move for feeding or reproduction, as the effectiveness of their masquerade declines (Yin et al., 2015). Such prey may therefore possess secondary defenses in addition to masquerade. Despite this possibility, little attention has been paid to how masquerading species defend themselves after their masquerade fails. Adults of the weevil Sternuchopsis trifida (Coleoptera: Curculionidae) are commonly found on the leaves and stems of the kudzu vine, Pueraria lobata (Fabaceae), in Japan (Figure 1a,b; Appendix S1: Table S1). When resting on leaves, their contrasting white-and-black body coloration appears conspicuous against the green background, resembling a bird dropping when viewed from a distance (Figure 1c,d). Such bird-dropping-like coloration, which occurs in various arthropods, is known to function as masquerade to avoid predation (Liu et al., 2014; Skelhorn, 2015). On days in May and June 2025, we observed many adults actively moving on kudzu plants at a grassland site in Hyogo, central Japan, a behavior likely to increase their risk of recognition as prey by predators such as frogs, which respond to movement. At the same site during the same season, the Japanese tree frog Dryophytes japonicus (Anura: Hylidae) was also found on kudzu (Figure 1e). Adult D. japonicus are known to prey on a wide variety of arthropods, including adult weevils (Hirai & Matsui, 2000; Sano & Shinohara, 2012). This species forages both during the day and at night (Hirai & Matsui, 2000; Taniguchi et al., 2005) and has been observed to attack diurnal insects in daylight (Matsubara & Sugiura, 2017). Therefore, D. japonicus potentially attacks moving adult S. trifida on kudzu leaves. To investigate how adult weevils can defend against tree frogs, we presented adult S. trifida (body length: 8.5–9.6 mm; body mass: 69.4–107.8 mg) to adult D. japonicus (snout–vent length: 27.4–33.4 mm; mass: 1.9–3.5 g) under laboratory conditions at 25°C (see Appendix S1: Materials and Methods, Table S2). All tree frogs (N = 20) reacted to weevil movements and attacked them. However, only two frogs (10%) successfully swallowed them (Figure 2). Six frogs rejected the weevils immediately after their tongues contacted them. Thirteen frogs had their tongues or lips grasped by weevils (Figure 1f), and 12 of these (92%) failed to swallow them (Figure 2; Video S1). During grasping, weevils did not appear to use their sharp tarsal claws. Instead, adult S. trifida possess inward-facing tibial and femoral spines (Appendix S1: Figure S1; Morimoto, 1984) that were observed to cling to the frog's tongue or mouthparts, likely helping them maintain a firm hold on the predator. In the 11 frogs whose tongues were firmly grasped (Figure 1f), frogs required 3–73 min (median: 14 min) to dislodge the weevils. To test whether grasping behavior is essential for successful defense against tree frogs, we provided adult D. japonicus (26.2–34.5 mm; 1.7–3.5 g) with adult S. trifida (8.1–9.8 mm; 57.2–104.9 mg) whose legs had been amputated at the mid-femur (thigh segment) with scissors (Appendix S1: Materials and Methods, Table S2). All tree frogs attacked the treated weevils, and none of the treated weevils were able to grasp the frogs. Of the 20 tree frogs, nine (45%) successfully swallowed the treated weevils (Figure 2). Other frogs rejected the weevils immediately after their tongues contacted them. Leg amputation increased the predation rate by tree frogs from 10% to 45% (Figure 2). A generalized linear model (GLM) analysis revealed a significant effect of leg removal (Appendix S1: Table S3). Therefore, adult S. trifida possess an effective secondary defensive strategy, in which they grasp the frog's tongue or lip with their legs to prevent swallowing. To investigate whether adult S. trifida can successfully defend against another frog species, we presented adult S. trifida (8.2–9.7 mm; 63.7–111.0 mg) to the black-spotted pond frog Pelophylax nigromaculatus (Anura: Ranidae) (36.4–78.4 mm; 4.1–50.0 g), which is larger than tree frogs. All pond frogs (N = 20) attacked the weevils, and 90% successfully swallowed them (Figure 2). Sixteen pond frogs consumed the weevils without being grasped by their legs. While four were grasped, two of these consumed the weevils. When leg-amputated weevils were presented, 95% of the 20 pond frogs successfully swallowed them (Figure 2). A GLM analysis showed no significant difference in predation rate between the control and leg-removal treatments (Appendix S1: Table S4). Only a few adult S. trifida managed to grasp the tongue or lip of pond frogs, suggesting that grasping defenses are not effective against larger frog species. Grasping behavior has been reported as a defensive response in which animals cling firmly to a substrate to prevent capture or ingestion by predators (Borne et al., 2021; Eisner & Aneshansley, 2000). Adult S. trifida are also observed clinging tightly to kudzu stems (Figure 1b), suggesting that this behavior may serve a similar function. In contrast, the grasping observed in the present study represents a previously undocumented defensive strategy, in which the prey holds onto the predator itself rather than onto the substrate (Figure 1f). Even when the legs were amputated, 55% of attacks by tree frogs resulted in rejection of adult S. trifida (Figure 2). This suggests that additional defenses other than grasping contribute to rejection. First, adult S. trifida possess a long and rigid rostrum (Figure 1a), which sometimes contacts the frog's tongue or mouthparts during attacks. Because the rostrum projects forward as a stiff, elongated structure, it can press against the inner surfaces of the frog's mouth when the prey is being transported toward the esophagus. Such contact may mechanically interfere with prey handling, making it difficult for the frog to reposition the prey for swallowing and thereby increasing the likelihood of rejection. Second, some tree frogs may have responded to chemical cues from adult S. trifida, as frogs can detect chemicals using their tongues (Matsubara & Sugiura, 2017). Although no glands or defensive chemical secretions have been detected in adult S. trifida, leg amputation occasionally caused a small amount of hemolymph to exude from the cut surface. Other morphological or behavioral traits might also play a role in rejection. Determining the relative importance of these potential factors will require further analyses, such as chemical profiling of the hemolymph or behavioral assays manipulating the rostrum. The movement of prey profoundly affects how their visual signals are perceived by predators (Cuthill et al., 2019). In masquerading species, such movement can either disrupt or preserve misclassification by predators, depending on the ecological context (Hall et al., 2017; Yin et al., 2015). In S. trifida, movement increases the likelihood of being recognized as prey, because the species is solitary, occurs on visually contrasting backgrounds, and mimics a non-moving model. We observed that adult S. trifida were attacked by tree frogs but avoided being swallowed by clinging tightly to the frog's tongue or lip (Figure 1f; Video S1). Their grip was so strong that the frogs required considerable time to dislodge them. Such handling difficulty may cause frogs to associate the weevil's conspicuous coloration with an unpleasant experience, thereby discouraging future attacks. We therefore hypothesize that the white-and-black coloration of S. trifida functions as masquerade when stationary, but in combination with strong secondary defenses, acts as aposematism when the insect is moving. A dual function of body coloration has been reported in some insects (Barnett & Cuthill, 2014; Kikuchi et al., 2017; Tullberg et al., 2005), with one example being the coexistence of camouflage and aposematism—blending into the background at a distance but becoming conspicuous at close range (Tullberg et al., 2005). However, few previous studies have focused on the defensive role of bird-dropping-like coloration as aposematism. To test this hypothesis, behavioral experiments are required to determine whether predators that have experienced weevil defenses subsequently avoid individuals with this coloration. We thank the editor and the anonymous reviewers for their constructive comments and helpful suggestions on an earlier version of this manuscript. We also thank K. Urano, D. Morimoto, H. Yoshii, K. Imasato, and Y. Nogawa for their assistance in maintaining the frogs, and Y. Nakabayashi for providing insect samples. This work was partially supported by the Sasakawa Scientific Research Grant (no. 2025-5006) and by JSPS KAKENHI (no. JP24K02099). The authors declare no conflicts of interest. Data (Sumi & Sugiura, 2026) are available in Figshare at https://doi.org/10.6084/m9.figshare.30000910.v1. Appendix S1. Video S1 Metadata. Video S1. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.