ArticlePDF Available
Current Biology
Magazine
R1026 Current Biology 25, R1019–R1031, November 2, 2015 ©2015 Elsevier Ltd All rights reserved
appetite for grasshoppers, crickets,
beetles, and caterpillars likely benefi t
gardeners and farmers, and one early
explorer of the American west actually
kept a pair of grasshopper mice in
his basement as an effective form of
‘cockroach control’, opening the door to
their cage each evening, closing the door
when the mice returned, contentedly
satiated, in the morning. And although
still a long way off, the novel mechanism
evolved by the mice for dealing with
the intense and prolonged pain from a
bark scorpion sting could lead to the
development of a completely new class
of analgesics, perhaps one lacking the
unfortunate side effects of opiates — the
benefi ts for people suffering chronic pain
would be incalculable.
But maybe we should rethink the
question. Most biologists consider
all species ‘good’ in the sense that
every plant, animal, fungus, virus,
and bacterium is interesting and thus
meritorious in its own right, worthy of
our curiosity, investigation, and respect.
Many species, if not most, may also play
some critical role in their community we
don’t understand until it is too late —
dodos, for example, appear to have
been important to forest regeneration
on Mauritius, while sea otters serve a
keystone function promoting healthy kelp
beds in the Pacifi c. Who knows what
critical roles grasshopper mice might
play in the deserts and grasslands they
currently patrol, howling?
Where can I learn more about
grasshopper mice?
Bailey, V., and Sperry, C.C. (1929). Life history and
habits of grasshopper mice, genus Onychomys,
USDA Techn. Bull. 145, 1–19.
Horner, B.E., Taylor, J.M., and Padykula, H.A. (1965).
Food habits and gastric morphology of the
grasshopper mouse. J. Mamm. 45, 513–535.
Langley, W.M. (1994). Comparison of predatory
behaviors of deer mice (Peromyscus maniculatus)
and grasshopper mice (Onychomys leucogaster).
J. Comp. Psychol. 108, 394–400.
Rowe, A.H., and Rowe, M.P. (2006). Risk assessment
by grasshopper mice (Onychomys spp.) feeding
on neurotoxic prey (Centruroides spp.). Anim.
Behav. 71, 725–734.
Rowe, A.H., and Rowe, M.P. (2008). Physiological
resistance of grasshopper mice (Onychomys spp.)
to Arizona bark scorpion (Centruroides exilicauda)
venom. Toxicon 52, 597–605.
Rowe, A.H., Xiao, Y., Rowe, M.P., Cummins, T.R., and
Zakon, H.H. (2013). Voltage-gated sodium channel
in grasshopper mice defends against bark
scorpion toxin. Science 342, 441–446.
Neuroscience Program and Department of
Integrative Biology, Michigan State University,
293 Farm Lane, Room 108 Giltner Hall, East
Lansing, MI 48824, USA.
*E-mail: roweashl@msu.edu
Poison frogs
Jennifer L. Stynoski1, Lisa M. Schulte2,
and Bibiana Rojas3
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
Quick guide 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 infl ation) 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.
Current Biology
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Current Biology 25, R1019–R1031, November 2, 2015 ©2015 Elsevier Ltd All rights reserved R1027
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 infl ux 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
identifi ed and more selective alkaloid
might lead to useful pharmaceuticals.
Are poison frogs endangered?
Many species are indeed on the
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.
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
Current Biology
Magazine
R1028 Current Biology 25, R1019–R1031, November 2, 2015 ©2015 Elsevier Ltd All rights reserved
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, fl exibility 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.
Where can I fi nd out more?
Brown, J.L. (Issue Editor) (2013). Special Issue:
Evolutionary Ecology of Poison Frogs. Evol.
Ecol. 24 (4) and articles within.
Crothers, L.R. and Cummings, M.E. (2013). Warning
signal brightness variation: sexual selection
may work under the radar of natural selection in
populations of a polytypic poison frog. Am. Nat.
181, E116–E124.
Grant, T., Frost, D.R., Caldwell, J.P., Gagliardo,
R., Haddad, C.F.B., Kok, P., et al. (2006).
Phylogenetic systematics of dart-poison frogs
and their relatives (Amphibia: Athesphatanura:
Dendrobatidae). Bull. Am. Mus. Nat. Hist. 299,
6–262.
Lötters, S., Jungfer, K.-H., Henkel, F.W., Schmidt,
W. (2007). Poison frogs: biology, species and
captive husbandry, In Edition Chimaira (Frankfurt
am Main, Germany: Edition Chimaira).
Saporito, R.A., Donnelly, M.A., Spande, T.F., and
Garraffo, H.M. (2012). A review of chemical
ecology in poison frogs. Chemoecology 22,
159–168.
Summers, K., and McKeon, C.S. (2004). The
evolutionary ecology of phytotelmata use in
Neotropical poison frogs. Misc. Publ. Mus. Zool.
Univ. Mich. 193, 55–73.
Wells, K.D. (2007). The Ecology and Behavior of
Amphibians. (Chicago: University of Chicago
Press.)
1Department of Biology, Colorado State
University, 200 West Lake Street, Fort Collins,
CO 80521, USA. 2Vrije Universiteit Brussel,
Biology Department - Amphibian Evolution
Lab, Pleinlaan 2, 1050 Brussels, Belgium.
3University of Jyvaskyla, Centre of Excellence
in Biological Interactions, Department of
Biology and Environmental Sciences, PO Box
35, FI 40014, Finland.
E-mail: stynoski@gmail.com;
Lisa_Schulte@gmx.de; bibiana.rojas@jyu.fi
Is there any
evidence for
vocal learning in
chimpanzee food
calls?
Julia Fischer1, Brandon C. Wheeler1,2,
and James P. Higham3
In their study “Vocal Learning in
the Functionally Referential Food
Grunts of Chimpanzees”, Watson
et al. [1] claimed that they “provide
the fi rst evidence for vocal learning
in a referential call in non-humans”.
We challenge this conclusion, on
two counts. For one, we are not
convinced that the authors controlled
for arousal (or at least they did not
report such data); furthermore, the
vocal characteristics of the two groups
largely overlapped already at the
beginning of the study. Accordingly,
we also question the authors’ claim
that their fi nding “sheds new light
on the evolutionary history of human
referential words”.
Firstly, Watson et al. [1] argue that
“call structure was not tied to arousal
as calls changed while preferences
stayed stable”. Given the theoretical
and empirical basis for linking
vocalization structure (especially
aspects related to frequency) to
affective states [2], we agree with the
authors that controlling for arousal
(degree of stimulation) is critical to
their conclusion. The authors had
investigated the structure of food
grunts before and after an integration
of individuals from a Safari Park in
the Netherlands (BB) into a group of
chimpanzees residing at the Edinburgh
Zoo (ED). If the BB individuals were
simply highly aroused by apples when
they moved to Edinburgh compared
to ED individuals, and if this arousal
declined over time, any changes to
BB calls would be best explained
by simple habituation to a stimulus
(apples).
Watson et al.’s [1] conclusion relies
on equating arousal and preference,
which is fallacious. To demonstrate
how different these two are, imagine
a human repeatedly offered his/her
favorite food in a series of choice
trials (the authors’ measure of
preference). Regardless of how stable
preference for this food remains, this
person is surely going to be more
excited to have their favorite food
for the fi rst time in months than for
the third time in a week. No data are
presented on apple feeding rates that
BB individuals experienced in the
Netherlands vs Edinburgh. It is thus
plausible that BB individuals have an
established preference for apples that
is maintained, while the apple feeding
at Edinburgh Zoo nonetheless led to a
reduced state of arousal over time. A
higher level of arousal of BB individuals
at the start of the study could also
be related to more excitement or
higher levels of stress due to feeding
in new environments and social
contexts. Either way, it is important
to rule out changes in arousal as the
simplest explanation for the results,
by collecting data on other aspects
of behavior, such as submissive or
self-directed behaviors [3], and/or
physiology.
Secondly, there is an issue with the
interpretation of the data. Despite
the signifi cant interaction reported
for year and group, we observed that
only seven calls from three subjects
(out of a total of 20 calls from seven
subjects) of the BB group recorded at
the beginning of the study fell outside
two standard deviations of the mean
of the ED group (Figure 1). In other
words, the majority of calls did not
differ in the fi rst place, indicating that
irrespective of their provenance, most
subjects of both populations had
always responded with the general
same call type to the presentation of
apples. Moreover, the pattern whereby
BB group individuals give calls above
the range of ED individuals does not
convincingly converge when looking
at the data (Figure 1) — the seven
BB calls above the ED range before
group integration (2010) become fi ve
calls above the ED range following
integration (2013) — weak evidence at
best. Obviously two groups of humans
from different linguistic backgrounds
would most likely have entirely
different words for the same things, not
vocalizations that largely overlap.
More generally, even if Watson et al.
[1] can provide new data that rule
Correspondence
... These brazen prey warn predators of the cost of attack with clear and salient signals. Vivid poison dart frogs warn visually specialized predators of toxins stockpiled in their skin glands (2,3), sea slugs reek odors to alert olfactory-specialist predators of stinging nematocysts (4), and tiger moths produce sonar-triggered bursts of ultrasound to warn echolocating bats of noxious taste (5,6). Given the demonstrated efficacy of unisensory warnings, why do defended animals routinely integrate multiple sensory channels in their displays? ...
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Many defended animals prevent attacks by displaying warning signals that are highly conspicuous to their predators. We hypothesized that bioluminescing fireflies, widely known for their vibrant courtship signals, also advertise their noxiousness to echolocating bats. To test this postulate, we pit naïve big brown bats (Eptesicus fuscus) against chemically defended fireflies (Photinus pyralis) to examine whether and how these beetles transmit salient warnings to bats. We demonstrate that these nocturnal predators learn to avoid noxious fireflies using either vision or echolocation and that bats learn faster when integrating information from both sensory streams—providing fundamental evidence that multisensory integration increases the efficacy of warning signals in a natural predator-prey system. Our findings add support for a warning signal origin of firefly bioluminescence and suggest that bat predation may have driven evolution of firefly bioluminescence.
... Junc a, Altig & Gascon, 1994;Rodrigues et al., 2011), egg, tadpole or froglet transportation (e.g. Bickford, 2002;M arquez, 1992;Stynoski, Schulte & Rojas, 2015) and tadpole feeding (e.g. Brust, 1993;Kam & Yang, 2002). ...
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Parental care is a limited resource which in many species is acquired by the offspring through begging behaviours and often causes competition between siblings. The Neotropical poison frog Ranitomeya variabilis provides a very specific form of parental care: because its tadpoles are cannibalistic males usually separate them from their siblings after hatching by transporting them singly to small water bodies. However, in some cases parents do not transport their tadpoles but let them all hatch into the same pool. Here, we investigate if abandoned tadpoles of R. variabilis actively seek parental care in form of transportation. We conducted experiments where tadpoles of the same clutch were presented with con- and heterospecific frogs, and both moving and non-moving frog models. Our results revealed that abandoned tadpoles actively approached all frogs and sometimes even climbed onto their backs. We suggest that this tadpole behaviour may function to allow tadpoles to escape sibling competition and cannibalism. Being the first (and possibly the only one) to leave the shared pool should give a tadpole a high survival advantage over its brood-mates. We further found that tadpoles did not approach artificial models, suggesting that these where either not natural enough or that tadpoles do not recognize frogs by visual or tactile cues but might use chemical or multiple stimuli. The latter is also the case in related egg-feeding species where tadpoles beg for food. We therefore discuss our results in relation to potential begging behaviours, as well as fixed action patterns and parent–offspring conflict, being potential questions opening up for future examinations regarding our findings.
... Several species of frogs exhibit conspicuous colouration and have a wide array of skin toxins (Wells, 2007), such as various species of Mantella ( Fig. 2A, B) and the 'Tomato frogs' (genus Dyscophus, Microhylidae; Fig. 2C) from Madagascar (Garraffo et al., 1993a); the Corroboree frogs (Pseudophryne corroboree; Fig. 2D) and other myobatrachids from Australia (Daly et al., 1990); Brachycephalus ephippium from Brazil ( Fig. 2E) (Sebben et al., 1986); and numerous species of Bufonids in the genera Melanophryniscus ( Fig. 2F) (Garraffo et al., 1993b;Grant et al., 2012) and Atelopus (Fig. 3A, B; Kim, Kim & Yotsu-Yamashita, 2003) from South and Central America. However, probably the best-known example of aposematic frogs are the dart poison frogs (Dendrobatidae; Fig. 4) (Stynoski, Schulte & Rojas, 2015). The varied toxins found in this Neotropical frog family (Daly & Myers, 1967;Myers & Daly, 1976Daly et al., 1994Daly et al., , 2002 are sequestered from their specialised diet (Saporito et al., 2004(Saporito et al., , 2007a, which consists mainly of ants, termites, mites and other arthropods found in the leaf litter (Toft, 1995;Darst et al., 2005). ...
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The role of colours and colour patterns in behavioural ecology has been extensively studied in a variety of contexts and taxa, while almost overlooked in many others. For decades anurans have been the focus of research on acoustic signalling due to the prominence of vocalisations in their communication. Much less attention has been paid to the enormous diversity of colours, colour patterns, and other types of putative visual signals exhibited by frogs. With the exception of some anecdotal observations and studies, the link between colour patterns and the behavioural and evolutionary ecology of anurans had not been addressed until approximately two decades ago. Since then, there has been ever-increasing interest in studying how colouration is tied to different aspects of frog behaviour, ecology and evolution. Here I review the literature on three different contexts in which frog colouration has been recently studied: predator–prey interactions, intraspecific communication, and habitat use; and I highlight those aspects that make frogs an excellent, yet understudied, group to examine the role of colour in the evolution of anti-predation strategies and animal communication systems. Further, I argue that in addition to natural-history observations, more experiments are needed in order to elucidate the functions of anuran colouration and the selective pressures involved in its diversity. To conclude, I encourage researchers to strengthen current experimental approaches, and suggest future directions that may broaden our current understanding of the adaptive value of anuran colour pattern diversity.
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Many organisms have evolved adaptations to increase the odds of survival of their offspring. Parental care has evolved several times in animals including ectotherms. In amphibians, ~ 10% of species exhibit parental care. Among these, poison frogs (Dendrobatidae) are well-known for their extensive care, which includes egg guarding, larval transport, and specialized tadpole provisioning with trophic eggs. At least one third of dendrobatids displaying aposematism by exhibiting warning coloration that informs potential predators about the presence of defensive skin toxins. Aposematism has a central role in poison frog diversification, including diet specialization, and visual and acoustic communication; and it is thought to have impacted their reproductive biology as well. We tested the latter association using multivariate phylogenetic methods at the family level. Our results show complex relationships between aposematism and certain aspects of the reproductive biology in dendrobatids. In particular, aposematic species tend to use more specialized tadpole-deposition sites, such as phytotelmata, and ferry fewer tadpoles than non-aposematic species. We propose that aposematism may have facilitated the diversification of microhabitat use in dendrobatids in the context of reproduction. Furthermore, the use of resource-limited tadpole-deposition environments may have evolved in tandem with an optimal reproductive strategy characterized by few offspring, biparental care, and female provisioning of food in the form of unfertilized eggs. We also found that in phytotelm-breeders, the rate of transition from cryptic to aposematic phenotype is 17 to 19 times higher than vice versa. Therefore, we infer that the aposematism in dendrobatids might serve as an umbrella trait for the evolution and maintenance of their complex offspring-caring activities.
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Warning signals are often characterized by highly contrasting, distinctive, and memorable colors. Greater chromatic (hue) and achromatic (brightness) contrast have both been found to contribute to greater signal efficacy, making longwave colored signals (e.g., red and yellow), that are perceived by both chromatic and achromatic visual pathways, particularly common. Conversely, shortwave colors (e.g., blue and ultraviolet) do not contribute to luminance perception yet are also commonly found in warning signals. Our understanding of the role of UV in aposematic signals is currently incomplete as UV perception is not universal, and evidence for its utility is at best mixed. We used visual modeling to quantify how UV affects signal contrast in aposematic heliconiian butterflies and poison frogs both of which reflect UV wavelengths, occupy similar habitats, and share similar classes of predators. Previous work on butterflies has found that UV reflectance does not affect predation risk but is involved in mate choice. As the butterflies, but not the frogs, have UV-sensitive vision, the function of UV reflectance in poison frogs is currently unknown. We found that despite showing up strongly in UV photographs, UV reflectance only appreciably affected visual contrast in the butterflies. As such, these results support the notion that although UV reflectance is associated with intraspecific communication in butterflies, it appears to be nonfunctional in frogs. Consequently, our data highlight that we should be careful when assigning a selection-based benefit to the presence of UV reflectance.
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Abstract Though theory predicts consistency of warning signals in aposematic species to facilitate predator learning, variation in these signals often occurs in nature. The strawberry poison frog Dendrobates pumilio is an exceptionally polytypic (populations are phenotypically distinct) aposematic frog exhibiting variation in warning color and brightness. In the Solarte population, males and females both respond differentially to male brightness variation. Here, we demonstrate through spectrophotometry and visual modeling that aposematic brightness variation within this population is likely visible to two putative predators (crabs, snakes) and conspecifics but not to the presumed major predator (birds). This study thus suggests that signal brightness within D. pumilio populations can be shaped by sexual selection, with limited opportunity for natural selection to influence this trait due to predator sensory constraints. Because signal brightness changes can ultimately lead to changes in hue, our findings at the within-population level can provide insights into understanding this polytypism at across-population scales.
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Though theory predicts consistency of warning signals in aposematic species to facilitate predator learning, variation in these signals often occurs in nature. The strawberry poison frog Dendrob- ates pumilio is an exceptionally polytypic (populations are pheno- typically distinct) aposematic frog exhibiting variation in warning color and brightness. In the Solarte population, males and females both respond differentially to male brightness variation. Here, we demonstrate through spectrophotometry and visual modeling that aposematic brightness variation within this population is likely visible to two putative predators (crabs, snakes) and conspecifics but not to the presumed major predator (birds). This study thus suggests that signal brightness within D. pumilio populations can be shaped by sexual selection, with limited opportunity for natural selection to influence this trait due to predator sensory constraints. Because signal brightness changes can ultimately lead to changes in hue, our findings at the within-population level can provide insights into understand- ing this polytypism at across-population scales.
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The known diversity of dart-poison frog species has grown from 70 in the 1960s to 247 at present, with no sign that the discovery of new species will wane in the foreseeable future. Although this growth in knowledge of the diversity of this group has been accompanied by detailed investigations of many aspects of the biology of dendrobatids, their phylogenetic relationships remain poorly understood. This study was designed to test hypotheses of dendrobatid diversification by combining new and prior genotypic and phenotypic evidence in a total evidence analysis. DNA sequences were sampled for five mitochondrial and six nuclear loci (approximately 6,100 base pairs [bp]; x¯ = 3,740 bp per terminal; total dataset composed of approximately 1.55 million bp), and 174 phenotypic characters were scored from adult and larval morphology, alkaloid profiles, and behavior. These data were combined with relevant published DNA sequences. Ingroup sampling targeted several previously unsampled species, including Aromobates nocturnus, which was hypothesized previously to be the sister of all other dendrobatids. Undescribed and problematic species were sampled from multiple localities when possible. The final dataset consisted of 414 terminals: 367 ingroup terminals of 156 species and 47 outgroup terminals of 46 species. Direct optimization parsimony analysis of the equally weighted evidence resulted in 25,872 optimal trees. Forty nodes collapse in the strict consensus, with all conflict restricted to conspecific terminals. Dendrobatids were recovered as monophyletic, and their sister group consisted of Crossodactylus, Hylodes, and Megaelosia, recognized herein as Hylodidae. Among outgroup taxa, Centrolenidae was found to be the sister group of all athesphatanurans except Hylidae, Leptodactyidae was polyphyletic, Thoropa was nested within Cycloramphidae, and Ceratophryinae was paraphyletic with respect to Telmatobiinae. Among dendrobatids, the monophyly and content of Mannophryne and Phyllobates were corroborated. Aromobates nocturnus and Colostethus saltuensis were found to be nested within Nephelobates, and Minyobates was paraphyletic and nested within Dendrobates. Colostethus was shown to be rampantly nonmonophyletic, with most species falling into two unrelated cis- and trans-Andean clades. A morphologically and behaviorally diverse clade of median lingual process-possessing species was discovered. In light of these findings and the growth in knowledge of the diversity of this large clade over the past 40 years, we propose a new, monophyletic taxonomy for dendrobatids, recognizing the inclusive clade as a superfamily (Dendrobatoidea) composed of two families (one of which is new), six subfamilies (three new), and 16 genera (four new). Although poisonous frogs did not form a monophyletic group, the three poisonous lineages are all confined to the revised family Dendrobatidae, in keeping with the traditional application of this name. We also propose changes to achieve a monophyletic higher-level taxonomy for the athesphatanuran outgroup taxa. Analysis of character evolution revealed multiple origins of phytotelm-breeding, parental provisioning of nutritive oocytes for larval consumption (larval oophagy), and endotrophy. Available evidence indicates that transport of tadpoles on the dorsum of parent nurse frogs—a dendrobatid synapomorphy—is carried out primitively by male nurse frogs, with three independent origins of female transport and five independent origins of biparental transport. Reproductive amplexus is optimally explained as having been lost in the most recent common ancestor of Dendrobatoidea, with cephalic amplexus arising independently three times.
Article
Herein we review what is known about the chemical ecology of poison frogs with a focus on dendrobatid poison frogs. While five anuran families are known to have an alkaloid-derived chemical defense, the dendrobatids have been studied in greatest detail and provides chemical ecologists with a complex model system for understanding how chemical defenses operate in real time and may have evolved through evolutionary time. We describe the diversity of alkaloid defenses known from frogs, alkaloid sequestration, biosynthesis and modification, and we review what is known concerning arthropod sources for alkaloids. There is variation in nearly every attribute of the system and we try to describe some of the challenges associated with unraveling the complexities of this model system. KeywordsAnts–Bufonids–Chemical defense–Dendrobatids–Mantellids– Melanophryniscus –Oribatid mites– Pseudophryne –Sequestration
Article
Consisting of more than six thousand species, amphibians are more diverse than mammals and are found on every continent save Antarctica. Despite the abundance and diversity of these animals, many aspects of the biology of amphibians remain unstudied or misunderstood. The Ecology and Behavior of Amphibians aims to fill this gap in the literature on this remarkable taxon. It is a celebration of the diversity of amphibian life and the ecological and behavioral adaptations that have made it a successful component of terrestrial and aquatic ecosystems. Synthesizing seventy years of research on amphibian biology, Kentwood D. Wells addresses all major areas of inquiry, including phylogeny, classification, and morphology; aspects of physiological ecology such as water and temperature relations, respiration, metabolism, and energetics; movements and orientation; communication and social behavior; reproduction and parental care; ecology and behavior of amphibian larvae and ecological aspects of metamorphosis; ecological impact of predation on amphibian populations and antipredator defenses; and aspects of amphibian community ecology. With an eye towards modern concerns, The Ecology and Behavior of Amphibians concludes with a chapter devoted to amphibian conservation. An unprecedented scholarly contribution to amphibian biology, this book is eagerly anticipated among specialists.
Special Issue: Evolutionary Ecology of Poison Frogs
  • J L Brown
Brown, J.L. (Issue Editor) (2013). Special Issue: Evolutionary Ecology of Poison Frogs. Evol. Ecol. 24 (4) and articles within.
Poison frogs: biology, species and captive husbandry
  • S Lötters
  • K.-H Jungfer
  • F W Henkel
  • W Schmidt
Lötters, S., Jungfer, K.-H., Henkel, F.W., Schmidt, W. (2007). Poison frogs: biology, species and captive husbandry, In Edition Chimaira (Frankfurt am Main, Germany: Edition Chimaira).
The evolutionary ecology of phytotelmata use in Neotropical poison frogs
  • K Summers
  • C S Mckeon
Summers, K., and McKeon, C.S. (2004). The evolutionary ecology of phytotelmata use in Neotropical poison frogs. Misc. Publ. Mus. Zool. Univ. Mich. 193, 55-73.