Developments in the study of poison frog evolutionary ecology II: decoding hidden messages in their coloration and unique behaviours

Evolutionary Ecology (2024) 38:551–570 https://doi.org/10.1007/s10682-024-10316-1 EDITORIAL Developments in the study of poison frog evolutionary ecology II: decoding hidden messages in their coloration and unique behaviours Bibiana Rojas1 · Fernando Vargas-Salinas2 Published online: 16 October 2024 © The Author(s), under exclusive licence to Springer Nature Switzerland AG 2024 Poison frogs, especially those species with bright colours and potent toxins in their bodies (Fig. 1), have fascinated people for decades. As stated in the first part of this Special Issue, research on poison frogs sensu lato has blossomed in the last two decades on different topics and taxa (Vargas-Salinas and Rojas 2024). Studies in the previous issue focused mostly on different aspects of parental care, larval biology, and space use at different scales. This second part brings 13 studies focusing on the extent, function and genetic underpinnings of colour variation, both in time and space (Bieri et al. 2024; Muell and Brown 2024; Plewnia et al. 2024; Rubio et al. 2024; Sommaro and Martínez 2024; Stuckert et al. 2024a); the dietary preferences of conspicuous and non-conspicuous species (Sánchez-Loja et al. 2024); alkaloid variation, synthesis and sequestration, and mechanisms to resist (own) toxins (Coleman and Cannatella 2024; Sague et al. 2024; Waters et al. 2024; Yeager et al. 2024); and behaviours either involving underexplored sensory modalities (Vergara-Herrera et al. 2024) or in need of improved methods for their quantification (Betancourth-Cundar et al. 2024a). Colours vary in space and time Several studies have demonstrated that frog dorsal coloration can have a signalling function (see next section below) in interactions between predators and their prey and between conspecifics (reviewed in: Rojas 2017; Rojas et al. 2023). Ventral coloration, however, is more challenging to explain as a signalling trait, as it is hidden most of the time. Despite Bibiana Rojas Fernando Vargas-Salinas 1 Department of Interdisciplinary Life Sciences, Konrad Lorenz Institute of Ethology, University of Veterinary Medicine Vienna, Savoyenstraße 1, Vienna 1160, Austria 2 Grupo de Investigación en Evolución, Ecología y Conservación (EECO), Universidad del Quindío, Armenia, Colombia 13 552 Evolutionary Ecology (2024) 38:551–570 Fig. 1 (A) Conspicuous ventral coloration in the genus Atelopus; (B) Phyllobates terribilis, the most toxic frog in the world, advertises the possession of powerful skin alkaloids with its bright yellow coloration. Note the tadpoles on the dorsum, which are being transported to a waterbody; (C) Alkaloid-containing skin secretions in Dendrobates tinctorius. More than 1200 alkaloids have been characterised in poison frogs to date; (D) Male of Ameerega trivittata calling while carrying a tag (pointed at by the arrow). This is one of the species whose movement patterns and homing abilities have been studied in detail in the field; (E) Leucostethus brachistriatus is one of the species documented to exhibit swollen fingers which are presumably involved in the production of a sex pheromone. Note the swelling in the third finger (from left to right) in comparison to the other three; (G) Tadpoles of Dendrobates tinctorius (large) and Allobates femoralis developing in a phytotelma. There are high chances that the latter does not make it to metamorphosis given the voracious nature of D. tinctorius tadpoles. Photo credits: A, C, F: Bibiana Rojas; B: Sebastián Duarte Marín; D: Andrius Pašukonis; E: frog: Fernando Vargas Salinas; insert: Diana Abondano Almeida this, many species display bright, conspicuous coloration in the venter, throat, and the soles of their hands and feet (Fig. 1A; Schaefer et al. 2002; Drinkwater et al. 2022). Recently, a macroevolutionary comparative analysis involving over 300 frog species concluded that the so-called hidden signals have been a key step in the evolution of aposematism (LoefflerHenry et al. 2023), an anti-predator strategy in which an often conspicuous warning signal is coupled with a secondary (e.g. chemical) defence (Poulton 1890). Zooming in on a group 13 Evolutionary Ecology (2024) 38:551–570 553 of putatively aposematic species displaying conspicuous ventral coloration, and using a combination of visual modelling, behavioural observations, and clay model experiments, Rößler et al. (2019) demonstrated that bright red sole coloration can act as a warning signal towards avian predators in harlequin toads (Atelopus spumarius). Red soles are more conspicuous for avian predators, easier to detect (by human observers), and associated with bolder behaviours than soles with other coloration. Furthermore, clay models displaying red soles were much less attacked than models with yellow soles (Rößler et al. 2019). Plewnia et al. (2024; this issue) report another form of hidden coloration across Amazonian species of harlequin toads. These toads often display ventral sexual dichromatism, whereby males show lower (or no) degree of melanisation than females. The authors collected data from the literature on 113 Atelopus species and found ventral dichromatism to be widespread in the genus, but most common across the Amazonian species. Ventral melanisation was further correlated with temperature. While there is evidence that melanisation could be advantageous as protection from UV radiation and for thermoregulation (Trullas et al. 2007; Rudh and Qvarnström 2013), the authors argue that this potential function is less likely to apply for ventral coloration, as the ventral side of the body is not directly exposed to sunlight. The function of sexual dichromatism has been commonly attributed to intraspecific communication, either in agonistic encounters or during mate choice or mate attraction. However, as pointed out by the authors, these differences between the sexes can be due to environmental or ontogenetic factors as well, but further research is needed to determine what exactly is the case in Atelopus toads. While Harlequin toads offer a great system to study variation in colouration across their geographic distribution range, colours (and patterns) can also vary across time. Such is the case, for example, of the red-eyed tree frog, Agalychnis callidryas, whose flank coloration has shifted in several populations over a 38-year period, leading to a clear differentiation of populations at a regional scale (Robertson and Robertson 2008). The Yungas red-belly toad, Melanophryniscus rubriventris, is a species with great variation in coloration across and within populations (Bonansea and Vaira 2012). Sommaro and Martínez (2024; this issue) analysed the colour patterns and body size variation of a polymorphic population of M. rubriventris over six years, which comprised five reproductive seasons. Their study aimed to investigate whether the frequencies of the different morphs found in the population were stable over time, and to test the hypothesis that (...truncated)