Introduction
Conspicuous coloration is a very effective signal to warn and deter predators (Wallace 1876; Endler 1990), particularly when combined with prey unpalatability and predator learning (Shettleworth 1972; Turner 1977; Siddiqui et al. 2004). The evolution of aposematic coloration has been thoroughly studied in adult anurans (Summers and Clough 2001; Darst et al. 2006; Mann and Cummings 2012; Barnett et al. 2018), despite the intense predation pressure experienced by anuran larvae; they are attacked by insects (Caldwell et al. 1980), fish (Smith et al. 2008), snakes (Warkentin 1995), spiders (Luiz et al. 2013), crabs (Gray and Christy 2000), and birds (Gontijo 2018). Unsurprisingly, tadpoles of many species evolved traits that increase the probability of survival, by avoiding, confusing, or escaping the potential predators. Tadpoles may also be toxic or unpalatable (Brodie and Formanowicz 1978), and cryptic or conspicuous in coloration (Wassersug 1971; Thibaudeau and Altig 2012). In response to chemical cues, they often adjust their activity (Hews and Blaustein 1985; Petranka et al. 1987) and distribution (Lima and Dill 1990; Spieler and Linsenmair 1999). A single species can exhibit several of these strategies, which combined represent an antipredator syndrome (Cooper and Blumstein 2015).
In some species of anuran larvae, the dark or patterned coloration of the eyes, mouth, or tail may reduce predation risk by concealing their body shape (Blair and Wassersug 2000), or redirecting attacks to other areas of the body (Van Buskirk et al. 2003). However, the role of conspicuous coloration in anuran larvae is mostly unknown (Thibaudeau and Altig 2012; Gontijo 2018); some hypotheses suggest that conspicuous coloration in some body areas may confound or intimidate predators (Altig 1972); it may also produce a ”lure effect” redirecting the attack to less vulnerable areas of the animal such as the tail (Caldwell 1982). Importantly, some of these colorations appear as phenotypic plasticity, after exposing the larvae to various species of predators, which further supports its alleged functional value in reducing predation risk (Van Buskirk et al. 2004; Touchon and Warkentin 2008).
The skin of adult phyllomedusine treefrogs secrete peptides such as bradykinin and dermorphin peptides, which are known to be highly unpleasant to predators and cause highly noxious effects (Sazima 1974; Lacombe et al. 2000; Birth 2013). The tadpoles of Phyllomedusa bicolor and P. vaillanti display metallic colorations in various regions of the body (Branch 1983; Thibaudeau and Altig 2012), which are clearly visible and contrasting to the human naked eye. At their breeding pond, they coexist with predator insect larvae and even with some fish, which are known as voracious predators that exclude anuran larvae from many water bodies (Magnusson and Hero 1991). Also, these phyllomedusinae tadpoles appear to be gregarious, a behavioral trait alleged to increase the survival of aposematic animals (Bertram 1978). Tested predators learn faster and retain the information longer when exposed to gregarious prey that exhibits contrasting coloration (Gamberale and Tullberg 1998). Altogether, the conspicuous metallic coloration, the co-existence with fish, and the gregarious behavior strongly suggest aposematism as an antipredator strategy in these anuran larvae.
In this study, we aimed at collecting evidence to test the hypothesis that the larvae of P. bicolor and P. vaillanti exhibits an antipredator syndrome consisting of conspicuous coloration, non-palatability or toxicity, and body size. Because metallic coloration occurs on the head and would be visible particularly to aerial predators, we further tested whether these tadpoles differentially use the water surface in the water column. Because coloration appears to change throughout ontogenetic stages, we further tested the effect of this variation on most measured traits. Lastly, to strengthen the interpretation of our results, we conducted the same measurements onCallymedusa tomopterna , a closely related species (Duellman et al. 2016), that lacks both the metallic coloration and the gregarious behavior.