A Quantitative Analysis of Micrurus Coral Snakes Reveals Unexpected Variation in Stereotyped Anti-Predator Displays Within a Mimicry System.

Venomous prey animals often use conspicuous phenotypes to communicate their lethal toxicity to potential predators (Ruxton et al. 2018). These aposematic signals can be visual, chemical, acoustic, or can involve complex interactions between multiple distinct components, such as color patterning and body motion (Rowe and Halpin 2013; Dalziell and Welbergen 2016). According to the theory of mimicry, toxic prey animals can reinforce the aposematic signal to their predators by converging on a common phenotype, even across multimodal components (e.g., conspicuous color and behavioral display; Wallace 1867; Muller 1878; Sherratt 2008). Coral snakes are highly venomous elapid snakes in the genus Micrurus that have been described as a mimicry system using visual warning signals of their chemical defense (Campbell and Lamar 2004). Most coral snake species are found in the Neotropics, with the highest sympatric species richness in the Western Amazon Basin (Davis Rabosky et al. 2016a). Coral snakes are well known for their conspicuous red and black coloration (Fig. 1A), a high-contrast banding pattern that effectively creates an aposematic signal deterring avian (Smith 1975; Smith 1977) and potentially mammalian predators (Greene and McDiarmid 1981; Savage and Slowinski 1992; Martins 1996; Buasso et al. 2006). In addition to their bright coloration, coral snakes encountering a threat that also produce a distinctive anti-predator display that includes elements such as body flattening, intermittent thrashing, head hiding, and coiling of the tail, which is often elevated and waved or “waggled” (Greene 1973, 1979; Fig. 1A;Supplementary Video S1). In some species, this display is also accompanied by an auditory cloacal “popping” sound, eversion of the hemipenes, and emission of cloacal musk and feces (Greene 1973; Sazima and Abe 1991). Because such similar elements of this behavioral display have been reported across many coral snake species in both Asia and the Americas (Brown et al. 2013b), this anti-predator response is expected to have (1) an old origin that predates the arrival of this clade in the Western Hemisphere ∼35mya and (2) a significant genetic basis like other homologous traits derived from shared ancestry (Wake et al. 2011). The main purpose of this display has been hypothesized as inducing an effective cognitive illusion that reduces the ability of the attacking predator to identify and target the head (Roze 1996). The intermittent, self-occluding thrashing is described as the foundational display component driving this effect in all species examined. Open in a separate window Fig. 1 (a) An illustration of a coral snake thrashing display. Each of the four illustrations depicts an individual coral snake progressing through different phases of a thrashing display (based on data in this study). Arrows represent direction of movement for corresponding body segments. The snake position with respect to the red dot shows that there is negligible translocation of the snake, despite vigorous movements. The snake head is on the left side of each illustration, and the coiled tail is elevated throughout the display. See Supplementary Video S1 to see a full thrashing trial. (B) A map of Peru showing our four field sites, all in lowland Amazonian rainforest. (C) A schematic of the pop-up behavioral arena. The bottom and sides of the arena are constructed from corrugated plastic and connected using brass fasteners. Lines are drawn 2 cm apart using permanent ink and covered with a clear adhesive plastic (Con-Tact). Three Go-Pro cameras were positioned so that their fields of view partially overlapped and included the entire floor-space of the arena (shown in yellow, red, and blue). An opaque plastic bowl with a portion removed was placed in one end of the arena to provide a refuge for the snake.