Current Biology Magazine appetite for grasshoppers, crickets, Quick guide preferences in different species for beetles, and caterpillars likely benefi t novel, brighter, or familiar colors, gardeners and farmers, and one early Poison frogs have both played a role in producing explorer of the American west actually a brilliant spectrum of color and kept a pair of grasshopper mice in pattern across the family. Coloration 1 2 his basement as an effective form of Jennifer L. Stynoski , Lisa M. Schulte , is an honest indicator of toxicity in 3 ‘cockroach control’, opening the door to and Bibiana Rojas some species, but not in others, their cage each evening, closing the door and is associated with territorial when the mice returned, contentedly What are poison frogs? Poison aggressiveness and boldness in satiated, in the morning. And although frogs, also commonly called ‘dart some cases. Recently, one Peruvian still a long way off, the novel mechanism poison frogs’ or ‘poison arrow frogs’, species, Ranitomeya imitator, was evolved by the mice for dealing with are charismatic amphibians forming found to be a true Müllerian mimic the intense and prolonged pain from a a spectacular adaptive radiation, of sympatric congeneric species. In bark scorpion sting could lead to the comparable to that of African cichlids. addition, the males and females of development of a completely new class Many of the diurnally active species several species are territorial and of analgesics, perhaps one lacking the have skin toxins and bright coloration have particularly good orientation and unfortunate side effects of opiates — the (Figure 1), and display numerous homing ability. Male communication benefi ts for people suffering chronic pain terrestrial reproductive modes includes both acoustic (calls) and would be incalculable. including elaborate parental care visual (vocal sac infl ation) signals But maybe we should rethink the and complex social behaviors. The (Figure 1H); each of these signals is question. Most biologists consider most diverse and well-studied group, not as effective to repel intruders as all species ‘good’ in the sense that superfamily Dendrobatoidea, consists the multimodal signal. every plant, animal, fungus, virus, of two families, Dendrobatidae and and bacterium is interesting and thus Aromobatidae, and is found from How do they reproduce? Several meritorious in its own right, worthy of Nicaragua to northern South America. species guard mates and some are our curiosity, investigation, and respect. Although less popular, other groups completely monogamous. These Many species, if not most, may also play known as poison frogs exist in South strategies are associated with the most some critical role in their community we America (family Bufonidae, genus striking behavior observed in poison don’t understand until it is too late — Melanophryniscus), Madagascar frogs: elaborate parental care. Parents dodos, for example, appear to have (family Mantellidae) and Australia guard terrestrial egg clutches and been important to forest regeneration (family Myobatrachidae, genus transport newly hatched tadpoles to on Mauritius, while sea otters serve a Pseudophryne), as well as two species water bodies (Figure 1G). Some species keystone function promoting healthy kelp in Cuba (family Eleutherodactylidae). transport all tadpoles at once to small beds in the Pacifi c. Who knows what Here, we focus on the traditional streams or puddles (Figure 1E,K). Other critical roles grasshopper mice might ‘poison frogs’, the dendrobatids. species transport tadpoles to very small play in the deserts and grasslands they pools in plants (phytotelmata; Figure currently patrol, howling? Are they called poison dart frogs, 1C) where there is less predation risk poison arrow frogs, dart-poison (Figure 1F). Parents that place offspring Where can I learn more about frogs, or just poison frogs? in smaller pools generally transport grasshopper mice? There are three species of poison tadpoles individually to separate pools Bailey, V., and Sperry, C.C. (1929). Life history and habits of grasshopper mice, genus Onychomys, frog (genus Phyllobates) to which to avoid competition for scarce food USDA Techn. Bull. 145, 1–19. common names including ‘arrow’ or resources and even larval cannibalism Horner, B.E., Taylor, J.M., and Padykula, H.A. (1965). ‘dart’ can be justly attributed. The (Figure 1B). Parents assess the quality Food habits and gastric morphology of the grasshopper mouse. J. Mamm. 45, 513–535. epithet comes from the use that and potential danger of tadpole Langley, W.M. (1994). Comparison of predatory some Colombian native tribes made deposition sites via chemical or visual behaviors of deer mice (Peromyscus maniculatus) and grasshopper mice (Onychomys leucogaster). of these species’ secretions, which cues. In some species, parental care J. Comp. Psychol. 108, 394–400. when rubbed on darts provide a lethal goes a step further: after deposition, Rowe, A.H., and Rowe, M.P. (2006). Risk assessment hunting weapon. The exudate of a adults feed tadpoles with unfertilized by grasshopper mice (Onychomys spp.) feeding on neurotoxic prey (Centruroides spp.). Anim. single golden arrow frog (Phyllobates eggs. In addition to providing food Behav. 71, 725–734. terribilis) — one of the most toxic in resource poor environments, Rowe, A.H., and Rowe, M.P. (2008). Physiological resistance of grasshopper mice (Onychomys spp.) vertebrates — can kill up to six this behavior supplies tadpoles to Arizona bark scorpion (Centruroides exilicauda) humans. with alkaloids to protect them from venom. Toxicon 52, 597–605. predators. Hungry tadpoles distinguish Rowe, A.H., Xiao, Y., Rowe, M.P., Cummins, T.R., and Zakon, H.H. (2013). Voltage-gated sodium channel Why are poison frogs interesting? between mothers and predators using in grasshopper mice defends against bark Besides being poisonous, many visual and tactile cues, and then scorpion toxin. Science 342, 441–446. species display bright colors and proceed to communicate with mother unique behaviors. Exceptional frogs by vibrating vigorously (Figure Neuroscience Program and Department of polymorphism and variation in 1I), which appears to stimulate egg Integrative Biology, Michigan State University, 293 Farm Lane, Room 108 Giltner Hall, East coloration is due to both natural and laying. Parental care can be performed Lansing, MI 48824, USA. sexual selection. Predator learning by mothers, fathers or both parents, *E-mail: [email protected] and recognition, as well as mating depending on the species.

R1026 Current Biology 25, R1019–R1031, November 2, 2015 ©2015 Elsevier Ltd All rights reserved Current Biology Magazine

Figure 1. Examples of diversity of coloration and behaviors in poison frogs. (A) Mating pair of Dendrobates tinctorius in French Guiana and (B) tadpole of the same species which was bitten by a cannibalistic conspecifi c; (C) Excidobates mysteriosus in a bromeliad; (D) Peruvian Ranitomeya fantastica; (E) male Ameerega hahneli transporting all his tadpoles at once; (F) male of the monogamous R. imitator transporting a single tadpole and (G) embryo of same species; (H) calling male Oophaga granulifera; (I) ‘blue jeans’ female O. pumilio (one of the many different color morphs of this species) and its tadpole begging for nutritive eggs; (J) Allobates granti, an example of a poison frog species that is not brightly coloured; (K);Hyloxalus nexipus transporting tadpoles to a stream; (L) D. auratus from Costa Rica.

What do we know about the poison heart arrhythmia and ultimately cardiac IUCN Red List of Threatened Species frogs’ toxins? Like all terrestrial arrest. Other less toxic alkaloids, such due in large part to devastation by amphibians, poison frogs face as histrionicotoxins, act as antagonists habitat loss. Also, some populations predators such as birds, spiders, bats, of nicotinic acetylcholine receptors at have shown to be affected by the and snakes. Poison frogs use toxic the neuromuscular junction, inhibiting Chytrid fungus (Batrachochytrium alkaloids as chemical defenses against signal transduction. Epipedobatine dendrobatidis), which is contributing predators. They sequester alkaloids also acts on acetylcholine receptors, to amphibian declines worldwide. from their diet of mostly mites and ultimately triggering the release of Today, dendrobatids are generally ants, and accumulate them in granular dopamine and norepinephrine; it was found in dense but isolated skin glands. To date, over 500 different a promising candidate for a non- populations in the remaining forest alkaloids have been described in opioid analgesic, but is not suitable for patches throughout their natural Dendrobatoidea, of which about humans because the pharmaceutical ranges. Also, in the 1960s and two-thirds are unique to them. For concentration is too similar to the 1970s, poison frogs became very example, batrachotoxin, the most toxic lethal dose. Phantasmidine, a recently popular among hobbyists in North poison frog alkaloid, binds irreversibly identifi ed and more selective alkaloid America and Europe because of their to voltage-gated sodium channels in might lead to useful pharmaceuticals. beauty. For decades this pet trade neuron- and muscle-cell membranes, has posed a serious threat to natural causing permanent depolarization Are poison frogs endangered? populations, as traders looking to sell by sodium infl ux and thus paralysis, Many species are indeed on the new color variants extract countless

Current Biology 25, R1019–R1031, November 2, 2015 ©2015 Elsevier Ltd All rights reserved R1027 Current Biology Magazine frogs. International trade regulations Correspondence a human repeatedly offered his/her and captive breeding efforts exist, favorite food in a series of choice but the illegal pet trade still places Is there any trials (the authors’ measure of pressure on natural populations. preference). Regardless of how stable evidence for preference for this food remains, this What can we learn from poison person is surely going to be more frogs in the future? The study of vocal learning in excited to have their favorite food these animals is brewing strong chimpanzee food for the fi rst time in months than for amidst a robust foundation of the third time in a week. No data are literature and an energetic research calls? presented on apple feeding rates that community. Exciting new work BB individuals experienced in the in poison frogs will incorporate Netherlands vs Edinburgh. It is thus Julia Fischer1, Brandon C. Wheeler1,2, collaborative and interdisciplinary plausible that BB individuals have an and James P. Higham3 perspectives to elucidate patterns established preference for apples that and mechanisms of behavior and is maintained, while the apple feeding evolution. For example, we will In their study “Vocal Learning in at Edinburgh Zoo nonetheless led to a likely see research on learning the Functionally Referential Food reduced state of arousal over time. A and memory in the context of Grunts of Chimpanzees”, Watson higher level of arousal of BB individuals parental care, the evolution of et al. [1] claimed that they “provide at the start of the study could also complex behavior, fl exibility and the fi rst evidence for vocal learning be related to more excitement or constraints of local speciation and in a referential call in non-humans”. higher levels of stress due to feeding polymorphism, resistance and We challenge this conclusion, on in new environments and social adaptation to emergent diseases two counts. For one, we are not contexts. Either way, it is important and habitat disturbance, and cellular convinced that the authors controlled to rule out changes in arousal as the and physiological mechanisms for arousal (or at least they did not simplest explanation for the results, that regulate poison sequestration, report such data); furthermore, the by collecting data on other aspects orientation, and communication. vocal characteristics of the two groups of behavior, such as submissive or largely overlapped already at the self-directed behaviors [3], and/or beginning of the study. Accordingly, physiology. Where can I fi nd out more? Brown, J.L. (Issue Editor) (2013). Special Issue: we also question the authors’ claim Secondly, there is an issue with the Evolutionary Ecology of Poison Frogs. Evol. that their fi nding “sheds new light interpretation of the data. Despite Ecol. 24 (4) and articles within. on the evolutionary history of human the signifi cant interaction reported Crothers, L.R. and Cummings, M.E. (2013). Warning signal brightness variation: sexual selection referential words”. for year and group, we observed that may work under the radar of natural selection in Firstly, Watson et al. [1] argue that only seven calls from three subjects populations of a polytypic poison frog. Am. Nat. 181, E116–E124. “call structure was not tied to arousal (out of a total of 20 calls from seven Grant, T., Frost, D.R., Caldwell, J.P., Gagliardo, as calls changed while preferences subjects) of the BB group recorded at R., Haddad, C.F.B., Kok, P., et al. (2006). stayed stable”. Given the theoretical the beginning of the study fell outside Phylogenetic systematics of dart-poison frogs and their relatives (Amphibia: Athesphatanura: and empirical basis for linking two standard deviations of the mean Dendrobatidae). Bull. Am. Mus. Nat. Hist. 299, vocalization structure (especially of the ED group (Figure 1). In other 6–262. Lötters, S., Jungfer, K.-H., Henkel, F.W., Schmidt, aspects related to frequency) to words, the majority of calls did not W. (2007). Poison frogs: biology, species and affective states [2], we agree with the differ in the fi rst place, indicating that captive husbandry, In Edition Chimaira (Frankfurt authors that controlling for arousal irrespective of their provenance, most am Main, Germany: Edition Chimaira). Saporito, R.A., Donnelly, M.A., Spande, T.F., and (degree of stimulation) is critical to subjects of both populations had Garraffo, H.M. (2012). A review of chemical their conclusion. The authors had always responded with the general ecology in poison frogs. Chemoecology 22, 159–168. investigated the structure of food same call type to the presentation of Summers, K., and McKeon, C.S. (2004). The grunts before and after an integration apples. Moreover, the pattern whereby evolutionary ecology of phytotelmata use in of individuals from a Safari Park in BB group individuals give calls above Neotropical poison frogs. Misc. Publ. Mus. Zool. Univ. Mich. 193, 55–73. the Netherlands (BB) into a group of the range of ED individuals does not Wells, K.D. (2007). The Ecology and Behavior of chimpanzees residing at the Edinburgh convincingly converge when looking Amphibians. (Chicago: University of Chicago Press.) Zoo (ED). If the BB individuals were at the data (Figure 1) — the seven simply highly aroused by apples when BB calls above the ED range before they moved to Edinburgh compared group integration (2010) become fi ve 1Department of Biology, Colorado State University, 200 West Lake Street, Fort Collins, to ED individuals, and if this arousal calls above the ED range following CO 80521, USA. 2Vrije Universiteit Brussel, declined over time, any changes to integration (2013) — weak evidence at Biology Department - Amphibian Evolution BB calls would be best explained best. Obviously two groups of humans Lab, Pleinlaan 2, 1050 Brussels, Belgium. by simple habituation to a stimulus from different linguistic backgrounds 3 University of Jyvaskyla, Centre of Excellence (apples). would most likely have entirely in Biological Interactions, Department of Watson et al.’s [1] conclusion relies different words for the same things, not Biology and Environmental Sciences, PO Box 35, FI 40014, Finland. on equating arousal and preference, vocalizations that largely overlap. E-mail: [email protected]; which is fallacious. To demonstrate More generally, even if Watson et al. [email protected]; bibiana.rojas@jyu.fi how different these two are, imagine [1] can provide new data that rule

R1028 Current Biology 25, R1019–R1031, November 2, 2015 ©2015 Elsevier Ltd All rights reserved