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.