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Poison frogs

2015; Elsevier BV; Volume: 25; Issue: 21 Linguagem: Inglês

10.1016/j.cub.2015.06.044

1879-0445

Jennifer L. Stynoski, Lisa M. Schulte, Bibiana Rojas,

Species Distribution and Climate Change

What are poison frogs? Poison frogs, also commonly called 'dart poison frogs' or 'poison arrow frogs', are charismatic amphibians forming a spectacular adaptive radiation, comparable to that of African cichlids. Many of the diurnally active species have skin toxins and bright coloration (Figure 1), and display numerous terrestrial reproductive modes including elaborate parental care and complex social behaviors. The most diverse and well-studied group, superfamily Dendrobatoidea, consists of two families, Dendrobatidae and Aromobatidae, and is found from Nicaragua to northern South America. Although less popular, other groups known as poison frogs exist in South America (family Bufonidae, genus Melanophryniscus), Madagascar (family Mantellidae) and Australia (family Myobatrachidae, genus Pseudophryne), as well as two species in Cuba (family Eleutherodactylidae). Here, we focus on the traditional 'poison frogs', the dendrobatids. Are they called poison dart frogs, poison arrow frogs, dart-poison frogs, or just poison frogs? There are three species of poison frog (genus Phyllobates) to which common names including 'arrow' or 'dart' can be justly attributed. The epithet comes from the use that some Colombian native tribes made of these species' secretions, which when rubbed on darts provide a lethal hunting weapon. The exudate of a single golden arrow frog (Phyllobates terribilis) — one of the most toxic vertebrates — can kill up to six humans. Why are poison frogs interesting? Besides being poisonous, many species display bright colors and unique behaviors. Exceptional polymorphism and variation in coloration is due to both natural and sexual selection. Predator learning and recognition, as well as mating preferences in different species for novel, brighter, or familiar colors, have both played a role in producing a brilliant spectrum of color and pattern across the family. Coloration is an honest indicator of toxicity in some species, but not in others, and is associated with territorial aggressiveness and boldness in some cases. Recently, one Peruvian species, Ranitomeya imitator, was found to be a true Müllerian mimic of sympatric congeneric species. In addition, the males and females of several species are territorial and have particularly good orientation and homing ability. Male communication includes both acoustic (calls) and visual (vocal sac inflation) signals (Figure 1H); each of these signals is not as effective to repel intruders as the multimodal signal. How do they reproduce? Several species guard mates and some are completely monogamous. These strategies are associated with the most striking behavior observed in poison frogs: elaborate parental care. Parents guard terrestrial egg clutches and transport newly hatched tadpoles to water bodies (Figure 1G). Some species transport all tadpoles at once to small streams or puddles (Figure 1E,K). Other species transport tadpoles to very small pools in plants (phytotelmata; Figure 1C) where there is less predation risk (Figure 1F). Parents that place offspring in smaller pools generally transport tadpoles individually to separate pools to avoid competition for scarce food resources and even larval cannibalism (Figure 1B). Parents assess the quality and potential danger of tadpole deposition sites via chemical or visual cues. In some species, parental care goes a step further: after deposition, adults feed tadpoles with unfertilized eggs. In addition to providing food in resource poor environments, this behavior supplies tadpoles with alkaloids to protect them from predators. Hungry tadpoles distinguish between mothers and predators using visual and tactile cues, and then proceed to communicate with mother frogs by vibrating vigorously (Figure 1I), which appears to stimulate egg laying. Parental care can be performed by mothers, fathers or both parents, depending on the species. What do we know about the poison frogs' toxins? Like all terrestrial amphibians, poison frogs face predators such as birds, spiders, bats, and snakes. Poison frogs use toxic alkaloids as chemical defenses against predators. They sequester alkaloids from their diet of mostly mites and ants, and accumulate them in granular skin glands. To date, over 500 different alkaloids have been described in Dendrobatoidea, of which about two-thirds are unique to them. For example, batrachotoxin, the most toxic poison frog alkaloid, binds irreversibly to voltage-gated sodium channels in neuron- and muscle-cell membranes, causing permanent depolarization by sodium influx and thus paralysis, heart arrhythmia and ultimately cardiac arrest. Other less toxic alkaloids, such as histrionicotoxins, act as antagonists of nicotinic acetylcholine receptors at the neuromuscular junction, inhibiting signal transduction. Epipedobatine also acts on acetylcholine receptors, ultimately triggering the release of dopamine and norepinephrine; it was a promising candidate for a non-opioid analgesic, but is not suitable for humans because the pharmaceutical concentration is too similar to the lethal dose. Phantasmidine, a recently identified and more selective alkaloid might lead to useful pharmaceuticals. Are poison frogs endangered? Many species are indeed on the IUCN Red List of Threatened Species due in large part to devastation by habitat loss. Also, some populations have shown to be affected by the Chytrid fungus (Batrachochytrium dendrobatidis), which is contributing to amphibian declines worldwide. Today, dendrobatids are generally found in dense but isolated populations in the remaining forest patches throughout their natural ranges. Also, in the 1960s and 1970s, poison frogs became very popular among hobbyists in North America and Europe because of their beauty. For decades this pet trade has posed a serious threat to natural populations, as traders looking to sell new color variants extract countless frogs. International trade regulations and captive breeding efforts exist, but the illegal pet trade still places pressure on natural populations. What can we learn from poison frogs in the future? The study of these animals is brewing strong amidst a robust foundation of literature and an energetic research community. Exciting new work in poison frogs will incorporate collaborative and interdisciplinary perspectives to elucidate patterns and mechanisms of behavior and evolution. For example, we will likely see research on learning and memory in the context of parental care, the evolution of complex behavior, flexibility and constraints of local speciation and polymorphism, resistance and adaptation to emergent diseases and habitat disturbance, and cellular and physiological mechanisms that regulate poison sequestration, orientation, and communication.