# Colors and Some Morphological Traits as Defensive Mechanisms

Authors: Luís Felipe Toledo; Célio F. B. Haddad
Journal: International Journal of Zoology
 (2009)

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## Abstract

Anurans may be brightly colored or completely cryptic. Generally, in the
former situation, we are dealing with aposematism, and the latter is
an example of camouflage. However, these are only simple views of what
such colorations really mean and which defensive strategy is implied.
For instance, a brightly colored frog may be part of a mimicry ring,
which could be either Batesian, Müllerian, or Browerian.
These are only examples of the diversity of color-usage systems as
defensive strategies. Unfortunately, reports on the use of colors as
defensive mechanisms are widespread in the available literature, and
the possible functions are rarely mentioned. Therefore, we reviewed
the literature and added new data to this subject. Then, we
the use of colors (as defensive mechanism) into categories. Mimicry
was divided into the subcategories camouflage, homotypy, and
nondeceitful homotypy, and these groups were also subcategorized.
Dissuasive coloration was divided into behavioral display of colors,
polymorphism, and polyphenism. Aposematism was treated apart, but
aposematic colorations may be present in other defensive strategies.
Finally, we propose functions and forms of evolution for some color
systems in post-metamorphic anurans and hope that this review can be
the basis for future research, even on other animal groups.


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## Body

## 1. Introduction

Anuran coloration results from
natural selection acting simultaneously on different aspects of natural
history, such as protection against solar radiation, thermoregulation, osmoregulation, nitrogen metabolism (e.g., [1–4]),
reproductive biology (e.g., [5]),
and defensive strategy (e.g., [6]).Anurans are remarkable for their
color patterns, which may range from a uniform black dorsum, as inCycloramphus boraceiensis (Cycloramphidae), to bright blue, orange, red, yellow, and green in the same
individual, as in Agalychnis
callidryas (Hylidae). In the
context of defensive strategies, these two distinct situations may be related to
two different types of primary defenses, which operate regardless of whether or
not a predator is in the vicinity [7]. Both situations: crypsis and
aposematism, as generally understood, help anurans to survive in nature. The former
may improve chances of avoiding detection, and the latter may signalize that
the individual is dangerous in one or several ways, where being toxic is the
most common [7]. Besides these, there are several other defensive
strategies involving coloration, such as body rising, mimicry, or flash color
(e.g., [6, 8, 9]).The presence of these and other defensive colorations in
anurans has been published for several species in a fragmented way, and has never
been reviewed. Herein, in order to organize current knowledge and ground future
research, we reviewed this subject, added new data, and provided information
about the evolution of color usage in anurans, with special reference to
Neotropical species.


## 2. Materials and Methods

We
reviewed the literature by searching for coloration-related defensive
strategies in anurans. Both natural and experimental observations were
considered. Additional data were obtained during several field expeditions in Brazil from 1972 to 2007, mainly in the Cerrado
and Atlantic Forest  domains in the southeast.All amphibian
scientific names follow Frost [10], and the specific nomenclature for coloration
categories was adapted from Pasteur [11]. It has been suggested that the terms
“dupe” and “selective agent” be preferentially used instead of “predator," due
to their broader meaning [11, 12]. In other words, an
anuran’s coloration is not always selected or maintained to warn or avoid a
predator; the “signal receiver" [13] may often be another anuran
(e.g., in intraspecific communication) or their prey (i.e., the anuran may
benefit from not being perceived by its prey). However, in the present paper, we
choose to use “predator" to designate any animal that could be a potential risk
to the anuran because we are analyzing coloration as a defensive strategy. For
the same reason, we will not cover aggressive and reproductive mimicry in this
paper.


## 3. Results

The use of colors can be divided into three major
categories: mimicry, deceptive coloration, and aposematism (Table1).Table 1
Major categories and subcategories of colors used as
defensive strategies in post-metamorphic anurans.
Major2nd major3rd majorSubcategoriesEucrypsisVisible
color spectrum mimesisCamouflageNonvisible
color spectrum mimesisMimesisCryptic
mimesisPhaneric mimesisMimicryConcrete
homotypyBatesian
mimicry*HomotypyBrowerian
mimicry*Abstract
homotypyDefinable
modelModel
not definable*Nondeceitful
homotypyMüllerian
mimicry*Arithmetic mimicryDeceptive
colorationBehavioral
display of colors*Polymorphism*PolyphenismAposematism*Indication*
for where aposematic coloration may or must be present.


### 3.1. Mimicry

Mimicry is generally considered as per the Batesian
mimicry concept, in which a nontoxic (or, otherwise, dangerous, e.g., the species
may bite) species mimics a dangerous model species (generally toxic). However, Batesian
mimicry is one of several types of mimicry into which anurans may be included (see
Table1). Mimicry (as presently defined) occurs when a group of organisms, the
mimics, has evolved to share common perceived characteristics with another
group of organisms, the models, through the selective action of a predator.
Collectively, they are known as a mimicry complex. Mimicry was herein divided
into three major groups: camouflage, homotypy, and nondeceitful homotypy (see what follows).


#### 3.1.1. Camouflage

Camouflage
may be defined as the resemblance of an animal with a part of the
environment [7], especially as viewed by the predator at the time
and place in which the prey is most vulnerable to predation  (Endler [19]).In
post-metamorphic anurans, camouflage may be optical, chemical (e.g., production
of floral, leaf-like, and ammonia odors), or acoustic (may occur, e.g., when
frogs stop calling in the presence of a predator; e.g., [20]). In
what follows, we will give special reference to optical camouflage, which
implies avoidance of detection by possible predators.(1) Eucrypsis
Definition:
homochromy (imitation of reflected light) which is acting alone. The model is
undefined, that is, it is the background.(a) Visible Color Spectrum Mimesis
Many
frogs are cryptic with the substrate they use, and there are a great variety of
backgrounds and mimic frogs. As substrates, anurans may use rocks with lichens,
tree trunks, leaves, forest litter, as well as mossy and rocky fields, for
example. For any such substrates, there are mimic frogs that live there (Figure1). Eucrypsis may be strengthened or weakened by a predator's angle of vision; that
is, the anuran may be more cryptic from a lateral view than from a dorsal view
(Figures 1(f) and 1(e), resp.).
The
more distant predator is from the site occupied by an anuran, the higher may be
the crypsis benefits. For instance, it is easy to find aDendropsophus nanus in its reproductive site when we are close to it.
However, from a certain distance, the colors and shape of this hylid get mixed
with the general view of the area. The size and colors of D. nanus are generally similar to part of the foliage, and it is
hard to distinguish them from yellowish leaves (Figures 1(k), 1(l)).Different
situations of cryptic mimicry in anurans: (a)Dendropsophus
acreanus (Hylidae) on a tree trunk, (b) Bokermannohyla
alvarengai (Hylidae) on a rock with lichens,
(c) Ischnocnema guentheri (Brachycephalidae) on litter,  (d) green morph
of Hypsiboas prasinus (Hylidae)
perched on a leaf, ((e)-(f), resp.) dorsal and lateral views of Theloderma horridum (Rhacophoridae) on a tree, (g) Lankanectes corrugatus (Nyctibatrachidae) in a lotic
water body,  (h) Hylodes asper (Hylodidae) on a wet rock, (i) Proceratophrys
boiei (Cycloramphidae) on litter,  (j) Scythrophrys
sawayae (Leptodactylidae) on a dead leaf, (k) an adult male of Dendropsophus nanus (Hylidae) of
practically the same size and shape as the leaves  and (l) its reproductive site.(b) Nonvisible Color Spectrum Mimesis
Some studies
have shown that several anuran species, from different families, may show a
pronounced rise in reflectance in the infrared part of the spectrum (e.g., [21–23]). Furthermore, some predators of anurans, such as pit
vipers, may be able to perceive infrared wavebands [24]. Others, such
as rodents, other amphibians, lizards, and mainly birds, have tetrachromatic
color vision (including ultraviolet cones), and may, therefore, perceive ultraviolet
wavelengths (e.g., [25]). Therefore, it is possible that infrared reflectance
may have evolved for anurans to remain cryptic in the foliage (which also has the
same infrared reflectance property), even against those predators who are able
to detect infrared or ultraviolet spectra (e.g., [22, 26]).(2) Mimesis
Definition: it is homomorphy (imitation of morphology)
and/or homokinemy (imitation of movements), in addition to homochromy (defined before).
The model is defined, that is, it is an object.(a) Cryptic Mimesis
It holds when the model
is a dominant element of the mimic's environment, such as green or brown
leaves, sticks, rocks, lichens, and mosses. Many examples may be cited, but to mention
some, we may refer to species of generaProceratophrys and Scythrophrys which resemble fallen leaves (Figures 1(i), 1(j),
resp.), as well as some species of Theloderma and Bokermannohyla that resemble mosses
and lichens, respectively (Figure 1(b)).
The
phyllomedusines of genusPhasmahyla,
when walking, sway slightly as if caught by the movement of the wind (=
homokinemy). Indeed, their genus name Phasmahyla was coined in allusion to the similarity of their moving style with the walking-sticks of order Phasmatodea [27]. The illusion
created by this behavior is increased with the leaf-like color pattern of this
species.(b) Phaneric Mimesis
It holds when the
model is an isolated and conspicuous inanimate element of the mimic’s
environment, such as animal droppings or rocks (when there are few rocks in the
environment). As examples, we may cite someTheloderma spp. and Dendropsophus marmoratus,
which resemble bird droppings, and many species of Rhinella and Bufo that
resemble stones on the floor.(3) Factors of Camouflage Enhancement
Both eucrypsis
and mimesis imply camouflage, which could be strengthened by (a) countershading,
(b) disruptive coloration, (c) shadow camouflage, (d) wetting, and (e)
integumentary structures.(a) Countershading
Countershading
occurs when the anuran's pigmentation is darker dorsally and lighter ventrally.
This transition may be gradual or abrupt, which could involve different
camouflage strategies (see [28, 29]).
Two
main functions have been attributed to countershading. (i) it is believed to have
the effect of reducing conspicuous shadows cast on the ventral region of an
animal's body. In essence, the distribution of light on objects lit from above
will cause unequal reflection of light by a solid body of uniform color. Such
shadows could provide predators with visual cues to a prey's shape and
projection. Countershading, therefore, reduces the ease with which prey is
detected by potential predators by counterbalancing the effects of shadowing.
This effect occurs mainly in animals that present a gradual transition of colors [28], and should be properly named “self-shadow concealment” [29]. (ii) Countershading coloration would work via background
matching; that is, when seen from the top, the dorsum (if cryptic colored) blends
into the background below, which could be a body of water (when the anuran is
swimming or floating) or dry-to-flooded ground (when the anuran is on the floor
or perched in the vegetation). When seen from below, the lighter ventral area
blends into the sun or moonlight (see [29]). This second
explanation generally occurs with an abrupt
transition of colors and seems to
be the more adequate for anurans.
Countershading
could result from selective pressures other than predation avoidance. For
example, the dorsal surface must be protected against the damaging properties
of UV light and/or abrasion Kiltie [30, 31], and the
ventral side does not need to be pigmented, as pigmentation may be costly
[29]. Therefore, the occurrence of countershading may result
from multiple factors.
This
system is so widespread among aquatic and terrestrial fauna that several
authors have stated that it is perhaps the most universal feature of animal
coloration (see [29] and references therein). Likewise, it is
present in several anuran species and might work against terrestrial predators,
for example, which may be on the ground when the anuran is perched on a tree branch.
In aquatic species, such as the pipids (e.g., Pipa spp. and Xenopus spp.), the system may work as described for fishes.(b) Disruptive Coloration
Disruptive
coloration is a color pattern that breaks the appearance of body form. Several anuran
species have dorsal lines and/or blotches that may be considered constitutive
of disruptive coloration, breaking the general outline of the body. Some
species may enhance their camouflage by having high-contrast lines on the edges
of colored patterns (see [32]). In addition to this,
several species present lateral lines that cross the eyes, breaking their
rounded shape (Figure 1(j)). These are the most common forms of disruptive
coloration in anurans.
A
possible variation is the presence of aposematic coloration (see what follows for
an explanation of aposematism) simultaneously with disruptive coloration,
depending on the predator and/or brightness of the night. This may occur
because the colorful stripes and/or blotches of an aposematic anuran (Figure2(a))
may become a disruptive pattern when seen by a color-blind predator, or by a
color vision predator hunting on dark nights (Figure 2(b); see also [33, 34]).
Recently,
it has been suggested and/or demonstrated that disruptive coloration is
advantageous compared to simple eucrypsis (see [35, 36], and references therein).(a) An
aposematicOophaga lehmanni (Dendrobatidae)
(b) may have disruptive coloration on dark nights or when searched for by a
color-blind predator. (c)  An adult and a juvenile Hypsiboas semilineatus (Hylidae),  (d) an amplectant pair of Rhinella icterica (Bufonidae), and ((e)-(f))
two morphs of Physalaemus cuvieri (Leiuperidae)  are examples
of polyphenism. ((g)-(h)) Flash color exhibited by Hypsiboas
caingua (Hylidae), ((i)-(j)) deimatic
behavior by Eupemphix nattereri (Leiuperidae), and ((k)–(l)) thanatosis
by Melanophryniscus moreirae (Bufonidae).(c) Shadow Camouflage
Anurans may rest in areas with combined spots of sunlight
and shade, making it difficult to recognize the animals on the substrate. If
part of the anuran is exposed to sunlight and the other part is in shadow, such
light play may enhance the anuran’s disruptive pattern (e.g., [32]).(d) Wetting
Some individuals may remain in lotic water bodies,
covered by a film of water or by water drops. This situation may enhance an
animal’s crypsis against terrestrial predators, by creating reflected shiny
spots on its dorsum matching the shiny spots in the water or substrate, for
example, rocks (Figures1(g)-1(h)).(e) Integumentary Structures
Some
integumentary structures seem to be associated with disruptive outlines and
thereby aid in concealment. Such structures include small, irregular ridges,
supraciliary processes (e.g., species ofProceratophrys and Ceratophrys), scalloped folds on
the outer edges of limbs (e.g., Cruziohyla
craspedopus), and calcars (e.g., several Hypsiboas spp.). Dorsal glands may also enhance crypsis by
promoting resemblance with lichens (e.g., Bokermannohyla
alvarengai, Itapotihyla langsdorffii, and Scinax
nebulosus) or mosses (e.g., Theloderma
corticale and other Vietnamese mossy frogs) (Figure 1).


#### 3.1.2. Homotypy (Assimilation to Another Type)

It acts differently from camouflage: in homotypy animals
can be perceived by the predator. Homotypy involves the mimetic imitation of
another object (which can be the same or another species, an object of the
environment, or an undefined model), being, therefore, included as mimicry.(1) Concrete Homotypy (Actual Model)
The
model is definite or an existing species (or cluster of similar species).(a) Batesian Mimicry
The concept of Batesian mimicry [37] involves
the success of a specific coloration against a predator’s experience; that is,
predators learn to avoid unpalatable species, which are identified by their
aposematic coloration (which does not always mean bright colors: e.g., [11, 38]), odor, sound, or another signal. Thus, a mimic could
obtain protection by resembling the unpalatable or less palatable model. For
anurans, there are few cases described wherein some palatable frogs may mimic some
poison frogs (Table 2).
Batesian mimicry involves the predator’s ability to learn
or have innate knowledge. Several predators, such as invertebrates in general,
are not as well-endowed in terms of sight and memory as are mammals, and,
therefore, may not have been the promoters of selective pressures for the evolution
and persistence of Batesian mimicry (see also [11]).
A
Batesian mimic does not necessarily need to be identical to its model.
Sometimes, it may exhibit intermediate resemblances to two (or more) models. In
this manner, the mimic may escape from some predators that avoid one model and from
others that avoid the other model. This dual mimicry system has been proposed for
coral snake mimics [39] and may be present in anurans.
An intriguing situation is the Batesian mimicry
proposed for theLeptodactylus lineatus and Allobates femoralis complex. This
complex would actually represent a case of Müllerian mimicry (where both
species are unpalatable; see further explanations below), instead of Batesian
mimicry as initially proposed [16], as L. lineatus seems to be a noxious
species as well. Upon handling and fixing individuals of L. lineatus, they exude a great amount of milky, probably noxious
secretions (C. F. B. Haddad, personal observation). However, some tests performed
on A. femoralis indicated that this
species is not toxic (see [40], and references therein). If A. femoralis is not toxic and L. lineatus is, this would be once again
a case of Batesian mimicry where L.
lineatus is the model. If both species are discovered to be nontoxic, it
would be a case of Arithmetic mimicry (where both species are palatable; see further
explanations below). Therefore, the relationship of this complex remains unresolved
and requires further research.Table 2
Occurrence of Batesian and Müllerian mimicry in anurans, and distribution
overlap between species.
MimicModelMimetism typeSympatric speciesSourceAromobatidaeDendrobatidaeAllobates
zaparoAmeerega bilinguisBatesianYes[14]Allobates zaparoAmeerega parvulaBatesianYes[14]BrachycephalidaeDendrobatidaePristimantis gaigeaePhyllobates lugubrisBatesianYes[15]Pristimantis gaigeaePhyllobates aurotaeniaBatesianYes[15]LeptodactylidaeAromobatidaeLeptodactylus
lineatus**Allobates femoralis**BatesianYes[16]DendrobatidaeDendrobatidaeRanitomeya imitatorRanitomeya fantasticusMüllerianYes[9]Ranitomeya imitatorRanitomeya variabilisMüllerianYes[9]Ranitomeya imitatorRanitomeya ventrimaculataMüllerianYes[9]MantellidaeMantellidaeMantella laevigata*Mantella manery*MüllerianYes[17]Mantella baroni*Mantella madagascariensis*MüllerianYes[17]Mantella pulchra*Mantellacowanii*MüllerianYes[18]DendrobatidaeDendrobatidaePhyllobates aurotaenia*Phyllobates lugubris*MüllerianNoPresent studyIn* these cases, definition of the mimic and model is not possible.**Further studies are needed in this case: see text.(b) Browerian Mimicry
When individuals within a species differ in palatability to
predators, the more palatable individuals (mimics) will gain benefits from those
less palatable (models). The models can be of the same or opposite sex to the
mimics. Albeit never reported that this type of mimicry may be present in aromobatids,
bufonids, dendrobatids, mantellids, and myobatrachids, at least. Individuals of
the same noxious species of these families (cited above) acquire the alkaloids contained
in their noxious secretions from dietary arthropods (e.g., [41–43], and references therein). Therefore, if for
any reason a group of individuals within a species either does not feed on arthropods
that carry the alkaloids, feeds on them but at a lower rate/proportion, or does
not sequester these components, they will be less poisonous than the others
(e.g., [44–47]).
Indeed, there are reports that show spatial (geographic)
and temporal (seasonal) variation in the alkaloid profiles of poison frogs [48], which may support the Browerian mimicry theory for
anurans.(2) Abstract Homotypy (Virtual Model)
When the model is not an actual species, homotypy is an abstract.(a) Definable Model
It occurs
when the model looks like a general type of organism, or part or indirect
vestiges of another organism, but is not identifiable at species level. For
example, the deimatic eyespots present on the back of leiuperids, which could
resemble snakes’ eyes (see, e.g., [6]), but not of a
specific species of snake. Other examples are frogs that rest on leaves and
look like bird droppings (e.g., Dendropsophus
marmoratus and Theloderma spp.).
Besides this, the presence of calcars on many species of rainforest tree frogs,
and their absence in other anurans, may suggest that they might serve as points
of water runoff, mimicking drip tips of leaves [49, page 371].(b) Model Not Definable
Occurs
when the model is not identifiable at all, but a frightening or cryptic form is
conjured up. This seems to be the case for the leg interweaving behavior described
elsewhere (see [50]).


#### 3.1.3. Nondeceitful Homotypy

This category was created (sensu [11]) basically for the inclusion of Müllerian
mimicry [51, 52] and Arithmetic mimicry [53]. In both
cases, the predator is not deceived, that is, the predator can recognize whether
the anuran is palatable or unpalatable. In this category, both the model and
the mimic are either unpalatable and/or dangerous in some way (Müllerian
mimicry), or palatable (arithmetic mimicry).These mimicry complexes are formed by species with similar
(or even exactly the same) color pattern. However, it is sometimes hard to
distinguish real nondeceitful homotypy from a possible phylogenetic influence; that
is, closely related species, such as two species ofDendrobates, may resemble one another due to a simplesiomorphy
(sharing of an ancestral character) and not because of coloration convergence (homoplasy).
Whether a convergence or a simplesiomorphy, the resemblance would benefit the
two (or more) species involved.(a) Müllerian Mimicry
Müllerian mimicry involves the mutual benefit of two dangerous (e.g., toxic,
noxious, unpalatable, able to harm the aggressor by any means, such as biting
and scratching, etc.) species by sharing similar phenotypes [51, 52]. To our
knowledge, there are only few cases of Müllerian mimicry in anurans (see Table 2);
however, other possible mimicry relationships may be suggested based on the
current reports. We may join two mimicry complexes of Mantella (M. baroni/madagascariensis and M. pulchra/cowanii) into a larger group of mimicry species, as all individuals
are sympatric and exhibit homochromy and homomorphy [17, 18]. Furthermore,
from the evidence of Batesian mimicry by Pristimantis
gaigeae with both Phyllobates aurotaenia and P. lugubris as models, we may
suggest another Müllerian mimicry system. This system would be comprised of P. aurotaenia and P. lugubris. These two species
are not sympatric, however, chronosympatry (presence of model and mimic in the
same time and place) is not a rule for the existence of mimicry [54, 55]; for instance, their past distributions could have overlapped (see also [15]), and/or the present distribution of selective agents
(predators) may overlap with the distribution of both species (including Batesian
mimic P. gaigeae).
Furthermore, it is possible that other Müllerian
mimicry systems exist that are not based on coloration but still comprise visual
mimetism. For example, if two different-colored species, or different morphs of
the same species, present the same toxic substances, they could be chemical
mimics. Therefore, based on properties other than color, such as body shape and
brightness, they could be part of a Müllerian mimicry ring (see also [56]). This would partly explain the several cases of polymorphism
among aposematic species (see below).(b) Arithmetic Mimicry
Similar sympatric edible species share the burden of
predation in proportion to their relative frequencies. In other words, the
higher the abundance of a certain (color) morph in the predator foraging area, the
lower the chances of an individual prey being preyed upon. In this case,
predator learning (ontogenetic or inherited) is irrelevant. To our knowledge,
arithmetic mimicry has never been reported for anurans; however, it may be a
very widespread phenomenon involving several sympatric (or even syntopic) similar
(e.g., in simultaneous homochromy, homomorphy, and homokinemy) species. As
examples of species pairs (or more), there are syntopicLeptodactylus furnarius and L.
jolyi; Dendropsophus nanus, D. sanborni, and D. minutus; Proceratophrys appendiculata, P. boiei, and P. melanopogon; as well as several species of Ischnocnema, all of them found
chronosympatrically in the Neotropical region.
Furthermore, two species with differences in
coloration (for instance), but of similar sizes (for instance), may also be
arithmetic mimics. Both of these edible species sharing a predator foraging
area may be equally nutritive; therefore, provided that the predator can
perceive that they are both nutritive, they will be nutritional arithmetic
mimics, benefited by the saturating theory (see [56]).


### 3.2. Deceptive Coloration

#### 3.2.1. Behavioral Display of Colors

Many
anurans may exhibit deceptive coloration, either intentionally or not, by
performing movements (e.g., flash color behavior) or by adopting specific
postures (e.g., body raising).A
fleeing anuran may escape from predators by displaying a flash of aposematic
color(s), generally followed by remaining motionless. This is known as flash
color behavior. This coloration is only visible when the anuran is moving
(generally while jumping), and concealed during resting posture (Figures2(g)-2(h)). Flash color
is widespread among anurans, occurring in several species and families. In the
Neotropics, it is very common in species of genera Scinax and Hypsiboas (Hylidae).Flash
color behavior may serve to disorientate and confuse an attacking predator [7] and/or warn predators of the presence of toxins [57]. These two distinct functions, and the implied predator responses, may
vary among individuals or species of predator. In other words, some predators
may be warned, while some may get confused. In this latter case, the predator
may lose the anuran: the flash behavior may precede the motionless behavior,
creating a prey search image that quickly disappears [7, 58]. Also, flash color behavior may halt the predator’s attack for an
instant and, thus, provide extra time for the frog to escape [59].Another
possibility of color display is body raising. For example, in some leiuperids
(e.g.,Eupemphix nattereri, Physalaemus deimaticus, and Pleurodema brachyops), when individuals
lift their hindparts, they exhibit a pair of black eyespots (Figures 2(i)-2(j)). Similarly to
flash color behavior, this exhibition may be viewed as an aposematic signal (as
these species have large poison glands below the eye-spots) or may be a deceptive
signal. In this latter case, the predator may have the illusion of facing a
different (and larger) animal. Therefore, it would be better classified as an abstract
homotypy where the model is definable (see above).


#### 3.2.2. Polymorphism

Polymorphism
in anurans is characterized by the presence of fixed chromatic phenotypes
within or between populations. The individuals seem unable to change their
color, so there must be genetic control involved. Polymorphism may benefit the
anuran in such a way that one or more of the phenotypes are not included in the
predator’s search image. Several species are known to present different
chromatic morphotypes, and such polymorphism may occur in three ways as
follows.(a) between Individuals, Independent of Sex and Life Stage
Two
morphotypes: for example, some adult individuals ofPhysalaemus cuvieri (Leiuperidae) and Paratelmatobius spp. (Leptodactylidae) are green, while others are
brown (Figures 2(e)-2(f)). Another type
of color dimorphism is exhibited by individuals of Leptodactylus fuscus (Leptodactylidae), which may or may not have a
dorso-vertebral white line.
More
than two morphotypes: several species of cryptic generaEleutherodactylus and Ischnocnema (Brachycephalidae) exhibit many different color morphotypes [60]. Even in aposematic species, this sort of
polymorphism can also be observed; for example, in Anomaloglossus
beebei (Aromobatidae), there are five color morphotypes [61], and in Oophaga pumilio (Dendrobatidae), there are at least 15 color
morphotypes (see, e.g., [5, 23]).
Multiple aposematic phenotypes are also observed in other dendrobatids [62] and African mantellids (see, e.g., [63]). Multiple
aposematic phenotypes may add the benefits of aposematism to the benefit
regarding predator search image (see before).(b) between Life Stages: Juveniles Different from Adults
This is
the case ofHypsiboas geographicus, H. semilineatus, H. lundii, H. pardalis, and H. raniceps (Hylidae), for instance, where juveniles have a totally
different coloration from adults, independent of sex (Figure 2(c)).(c) between Sexes: Males Different from Females
As
examples, we may citeRhinella icterica (Bufonidae),
where males are light yellowish and females are black and white (Figure 2(d)); Leptopelis vermiculatus (Arthroleptidae), where males are green and females are brown; and most
contrasting is Incilius periglenes (Bufonidae),
where males are bright orange and females are black, red, and yellow.


#### 3.2.3. Polyphenism

Polyphenism is the ability to
generate different phenotypes, by color changing in this case, by the same
individual. Polyphenism may be a better term to describe this phenomenon than
polymorphism, which generally implies a stronger genetic element for each
particular appearance [64].Many anurans can change their dorsal
coloration by rearranging their chromatophores, which involves sophisticated
physiological control of skin structures. There
is a continuous gradient of color change timing in anurans: the change may
occur instantaneously, or may take a few minutes, hours, days, or even weeks to
occur.Some
species may change their color very quickly. We placed one individual ofBokermannohyla circumdata (Hylidae) in a
dark place (under tree bark) and left another individual exposed to the
laboratory light. After 15 minutes, they were completely different from their
initial, dark reddish-brownish coloration. The first individual (kept in the
dark) was much darker, almost black, whereas the second individual (exposed)
was almost white. A similar polyphenism was described for Bokermannohyla alvarengai, but in this case, the color change was
studied with regard to physiological adjustments for temperature and water loss
control [4].The
dorsal coloration ofScinax
fuscomarginatus (Hylidae) males is yellowish during the night (during reproductive
activity) and grayish or brownish during the day. This may be related to the
specific site they use: during the night, they remain perched on yellowish
grass vegetation [65], while during the day they can be
found in dark sites, such as tree holes, under tree bark, and in the middle of
clumps of grass. Conversely, this color change may be due to testosterone
amount during reproductive activity (calling), as the yellowish males also have
an odor which is distinct from the one they have during the daytime resting period.
Additionally, individuals killed while still yellowish left a yellow tinge in
the preservative liquid (formalin, alcohol). We recorded the same phenomenon
for Scinax fuscovarius and S. hayii. Furthermore, some
phyllomedusines can change from purplish during night activity to greenish
during daytime resting. Such polyphenism was observed in Phasmahyla cochranae, P.
guttata, and P. jandaia. This
phenomenon can occasionally be observed in Phyllomedusa
azurea, P. megacephala, and P. rohdei (see colored pictures in [66]).We observed a seasonal
polyphenism inHypsiboas prasinus (Hylidae), in which a higher presence of green individuals occurred mainly in
the hot, rainy season of the year, whereas a higher presence of brown
individuals occurred in the cold, dry season of the year. This pattern overlaps
with the frequency of green and brown leaves in the Mesophytic Semideciduos Forest where this species dwells [67]: the peak of leaf fall precedes the peak of brown
morphs and the peak of leaf flushing precedes the peak of green morphs (Figure 3). Seasonal color changing has also been observed in Pseudacris regilla (Hylidae), and has been considered a response to divergent selection for crypsis in
a heterogeneous, seasonally variable environment [68]. This is likely to be an explanation for the
polymorphism of H. prasinus as well.Seasonal
variation (March 1988 to May 1989) in the dorsal coloration of reproductive
males ofHypsiboas prasinus (Hylidae),
and number of plants that exhibited leaf fall (brown lines) and leaf flushing
(green lines), in Serra do Japi, Jundiaí, São Paulo, Brazil. Brown bars
represent brown morphs (upper picture), green bars represent green morphs
(lower picture), and olive bars represent intermediate (olive) coloration
morphs. Plant phenology data were obtained from Morellato et al. [67].Polyphenism may be
advantageous over polymorphism because the anuran may select a substrate and then
adjust its color pattern. Polymorphic anurans may find adequate substrates to
fit their general coloration, and such are not necessarily hard to find, but
polyphenic species may have a wider range of substrates that they can use.


### 3.3. Aposematism

Aposematic
coloration has also been referred to as sematic, conspicuous, or warning
coloration. Aposematism is the presence of contrasting and conspicuous coloration
that is generally related to the presence of skin toxins in the individuals [7, 58]. Furthermore, it may also signalize that the
anuran is dangerous or unpleasant in any other way. For example, aposematic
anurans may bite, exhibit spine aggression, and/or produce loud defensive
screams.Aposematic
coloration is generally bright red, orange, yellow, and/or blue on a dark
(generally black), contrasting background. This aposematic coloration is most
commonly widespread over the entire body, such as in species ofAllobates (Aromobatidae), Ameerega and Dendrobates (Dendrobatidae), Mantella (Mantellidae), Atelopus (Bufonidae), and Brachycephalus (Brachycephalidae).Aposematic
coloration is often confined to parts that are usually concealed when the frog
is in its resting posture (e.g., some leiuperids (Eupemphix nattereri and Physalaemus spp.), bombinatorids (Bombina spp.), hylids (Phyllomedusa spp. and Hypsiboas of the marmoratus group), bufonids (Melanophryniscus spp.), and leptodactylids (Leptodactylus of the pentadactylus group)). In
this case, the bright coloration is generally present on the back of the
thighs, the underside of the body, the limbs, feet, and hands, and is displayed
by specific posturing such as the unken reflex [69] or body raising [65].In
species ofCeratoprhys and Hemiphractus, aposematic coloration may
be present on the lips or on the tongue, respectively, which are displayed when
the individuals perform the mouth-gapping display or emit defensive screams. In Phyllomedusa spp., the bright, contrasting
coloration may be displayed intentionally (e.g., during foot flagging) or when
the individuals walk on tree branches. The foot signaling of Atelopus zeteki, in addition to being an
intraspecific communication, may be a visual display, including aposematic
coloration (bright yellow contrasting with black stripes) for potential
predators [70]. In Ameerega flavopicta, there
seems to be a relationship between parental care and body raising [71]. Several species have a conspicuously colored belly (or other
underside parts; e.g., Paratelmatobius spp., Leptodactylus pustulatus, or Melanophryniscus spp.). When facing a
predator, they might not present any specific behavior to display these colors.
However, they may display thanatosis (a widespread behavior in frogs) and,
during handling by the predator, the anurans may be turned upside down and
would thus display the aposematic coloration (Figures 2(k)-2(l)). Species of Oreophrynella, after displaying “balling
behavior" while fleeing, may stop belly-side-up, exposing their bright,
contrasting ventral coloration [72].Several factors are involved in the evolution of
aposematism, such as unpalatability, honest signals, relative predator-prey
abundance-dependence, and kin selection (review in [73]). In
anurans, aposematism has evolved multiple times (e.g., [74–76]). However, some of these authors have based
their results on the hypothesis of evolutionary relationships that have been
recently modified or complemented [40, 77].
Therefore, a new overview of these evolutionary approaches to defense is
needed, because their assumptions may be modified. For example, Summers and
Clough [74] did their study based on the assumption that family Dendrobatidae
(as considered at that time) was monophyletic, and that the toxic aposematic
dendrobatids clade was also monophyletic. However, this apparent monophyly has been
rejected [75, 76], the former dendrobatid
family has been divided into two sister families (Dendrobatidae and
Aromobatidae), and the toxic species are divided into several genera (e.g., Adelphobates,
Allobates, Ameerega, Dendrobates, Epipedobates, Hyloxalus, Myniobates, and Oophaga) in both families [40].Although
there may be changes to the phylogenetic hypotheses, it is still possible that aposematic
coloration has evolved in tandem with toxicity in anurans of the Bufonidae,
Dendrobatidae, Aromobatidae, and Mantellidae families, as previously proposed (e.g., [43, 74]). “If differences among species in
dietary preferences or predatory capabilities are heritable, then natural
selection could act to favor brighter coloration in species that consistently
have preferences for or access to prey with more or more potent toxins”
[74]. Speculations apart, the most evident fact is that
anuran aposematism has evolved by means of multiple convergent radiations,
within the order, its families, and/or its genera (e.g., [43, 75, 76, 78]).


## 3.1. Mimicry

Mimicry is generally considered as per the Batesian
mimicry concept, in which a nontoxic (or, otherwise, dangerous, e.g., the species
may bite) species mimics a dangerous model species (generally toxic). However, Batesian
mimicry is one of several types of mimicry into which anurans may be included (see
Table1). Mimicry (as presently defined) occurs when a group of organisms, the
mimics, has evolved to share common perceived characteristics with another
group of organisms, the models, through the selective action of a predator.
Collectively, they are known as a mimicry complex. Mimicry was herein divided
into three major groups: camouflage, homotypy, and nondeceitful homotypy (see what follows).


### 3.1.1. Camouflage

Camouflage
may be defined as the resemblance of an animal with a part of the
environment [7], especially as viewed by the predator at the time
and place in which the prey is most vulnerable to predation  (Endler [19]).In
post-metamorphic anurans, camouflage may be optical, chemical (e.g., production
of floral, leaf-like, and ammonia odors), or acoustic (may occur, e.g., when
frogs stop calling in the presence of a predator; e.g., [20]). In
what follows, we will give special reference to optical camouflage, which
implies avoidance of detection by possible predators.(1) Eucrypsis
Definition:
homochromy (imitation of reflected light) which is acting alone. The model is
undefined, that is, it is the background.(a) Visible Color Spectrum Mimesis
Many
frogs are cryptic with the substrate they use, and there are a great variety of
backgrounds and mimic frogs. As substrates, anurans may use rocks with lichens,
tree trunks, leaves, forest litter, as well as mossy and rocky fields, for
example. For any such substrates, there are mimic frogs that live there (Figure1). Eucrypsis may be strengthened or weakened by a predator's angle of vision; that
is, the anuran may be more cryptic from a lateral view than from a dorsal view
(Figures 1(f) and 1(e), resp.).
The
more distant predator is from the site occupied by an anuran, the higher may be
the crypsis benefits. For instance, it is easy to find aDendropsophus nanus in its reproductive site when we are close to it.
However, from a certain distance, the colors and shape of this hylid get mixed
with the general view of the area. The size and colors of D. nanus are generally similar to part of the foliage, and it is
hard to distinguish them from yellowish leaves (Figures 1(k), 1(l)).Different
situations of cryptic mimicry in anurans: (a)Dendropsophus
acreanus (Hylidae) on a tree trunk, (b) Bokermannohyla
alvarengai (Hylidae) on a rock with lichens,
(c) Ischnocnema guentheri (Brachycephalidae) on litter,  (d) green morph
of Hypsiboas prasinus (Hylidae)
perched on a leaf, ((e)-(f), resp.) dorsal and lateral views of Theloderma horridum (Rhacophoridae) on a tree, (g) Lankanectes corrugatus (Nyctibatrachidae) in a lotic
water body,  (h) Hylodes asper (Hylodidae) on a wet rock, (i) Proceratophrys
boiei (Cycloramphidae) on litter,  (j) Scythrophrys
sawayae (Leptodactylidae) on a dead leaf, (k) an adult male of Dendropsophus nanus (Hylidae) of
practically the same size and shape as the leaves  and (l) its reproductive site.(b) Nonvisible Color Spectrum Mimesis
Some studies
have shown that several anuran species, from different families, may show a
pronounced rise in reflectance in the infrared part of the spectrum (e.g., [21–23]). Furthermore, some predators of anurans, such as pit
vipers, may be able to perceive infrared wavebands [24]. Others, such
as rodents, other amphibians, lizards, and mainly birds, have tetrachromatic
color vision (including ultraviolet cones), and may, therefore, perceive ultraviolet
wavelengths (e.g., [25]). Therefore, it is possible that infrared reflectance
may have evolved for anurans to remain cryptic in the foliage (which also has the
same infrared reflectance property), even against those predators who are able
to detect infrared or ultraviolet spectra (e.g., [22, 26]).(2) Mimesis
Definition: it is homomorphy (imitation of morphology)
and/or homokinemy (imitation of movements), in addition to homochromy (defined before).
The model is defined, that is, it is an object.(a) Cryptic Mimesis
It holds when the model
is a dominant element of the mimic's environment, such as green or brown
leaves, sticks, rocks, lichens, and mosses. Many examples may be cited, but to mention
some, we may refer to species of generaProceratophrys and Scythrophrys which resemble fallen leaves (Figures 1(i), 1(j),
resp.), as well as some species of Theloderma and Bokermannohyla that resemble mosses
and lichens, respectively (Figure 1(b)).
The
phyllomedusines of genusPhasmahyla,
when walking, sway slightly as if caught by the movement of the wind (=
homokinemy). Indeed, their genus name Phasmahyla was coined in allusion to the similarity of their moving style with the walking-sticks of order Phasmatodea [27]. The illusion
created by this behavior is increased with the leaf-like color pattern of this
species.(b) Phaneric Mimesis
It holds when the
model is an isolated and conspicuous inanimate element of the mimic’s
environment, such as animal droppings or rocks (when there are few rocks in the
environment). As examples, we may cite someTheloderma spp. and Dendropsophus marmoratus,
which resemble bird droppings, and many species of Rhinella and Bufo that
resemble stones on the floor.(3) Factors of Camouflage Enhancement
Both eucrypsis
and mimesis imply camouflage, which could be strengthened by (a) countershading,
(b) disruptive coloration, (c) shadow camouflage, (d) wetting, and (e)
integumentary structures.(a) Countershading
Countershading
occurs when the anuran's pigmentation is darker dorsally and lighter ventrally.
This transition may be gradual or abrupt, which could involve different
camouflage strategies (see [28, 29]).
Two
main functions have been attributed to countershading. (i) it is believed to have
the effect of reducing conspicuous shadows cast on the ventral region of an
animal's body. In essence, the distribution of light on objects lit from above
will cause unequal reflection of light by a solid body of uniform color. Such
shadows could provide predators with visual cues to a prey's shape and
projection. Countershading, therefore, reduces the ease with which prey is
detected by potential predators by counterbalancing the effects of shadowing.
This effect occurs mainly in animals that present a gradual transition of colors [28], and should be properly named “self-shadow concealment” [29]. (ii) Countershading coloration would work via background
matching; that is, when seen from the top, the dorsum (if cryptic colored) blends
into the background below, which could be a body of water (when the anuran is
swimming or floating) or dry-to-flooded ground (when the anuran is on the floor
or perched in the vegetation). When seen from below, the lighter ventral area
blends into the sun or moonlight (see [29]). This second
explanation generally occurs with an abrupt
transition of colors and seems to
be the more adequate for anurans.
Countershading
could result from selective pressures other than predation avoidance. For
example, the dorsal surface must be protected against the damaging properties
of UV light and/or abrasion Kiltie [30, 31], and the
ventral side does not need to be pigmented, as pigmentation may be costly
[29]. Therefore, the occurrence of countershading may result
from multiple factors.
This
system is so widespread among aquatic and terrestrial fauna that several
authors have stated that it is perhaps the most universal feature of animal
coloration (see [29] and references therein). Likewise, it is
present in several anuran species and might work against terrestrial predators,
for example, which may be on the ground when the anuran is perched on a tree branch.
In aquatic species, such as the pipids (e.g., Pipa spp. and Xenopus spp.), the system may work as described for fishes.(b) Disruptive Coloration
Disruptive
coloration is a color pattern that breaks the appearance of body form. Several anuran
species have dorsal lines and/or blotches that may be considered constitutive
of disruptive coloration, breaking the general outline of the body. Some
species may enhance their camouflage by having high-contrast lines on the edges
of colored patterns (see [32]). In addition to this,
several species present lateral lines that cross the eyes, breaking their
rounded shape (Figure 1(j)). These are the most common forms of disruptive
coloration in anurans.
A
possible variation is the presence of aposematic coloration (see what follows for
an explanation of aposematism) simultaneously with disruptive coloration,
depending on the predator and/or brightness of the night. This may occur
because the colorful stripes and/or blotches of an aposematic anuran (Figure2(a))
may become a disruptive pattern when seen by a color-blind predator, or by a
color vision predator hunting on dark nights (Figure 2(b); see also [33, 34]).
Recently,
it has been suggested and/or demonstrated that disruptive coloration is
advantageous compared to simple eucrypsis (see [35, 36], and references therein).(a) An
aposematicOophaga lehmanni (Dendrobatidae)
(b) may have disruptive coloration on dark nights or when searched for by a
color-blind predator. (c)  An adult and a juvenile Hypsiboas semilineatus (Hylidae),  (d) an amplectant pair of Rhinella icterica (Bufonidae), and ((e)-(f))
two morphs of Physalaemus cuvieri (Leiuperidae)  are examples
of polyphenism. ((g)-(h)) Flash color exhibited by Hypsiboas
caingua (Hylidae), ((i)-(j)) deimatic
behavior by Eupemphix nattereri (Leiuperidae), and ((k)–(l)) thanatosis
by Melanophryniscus moreirae (Bufonidae).(c) Shadow Camouflage
Anurans may rest in areas with combined spots of sunlight
and shade, making it difficult to recognize the animals on the substrate. If
part of the anuran is exposed to sunlight and the other part is in shadow, such
light play may enhance the anuran’s disruptive pattern (e.g., [32]).(d) Wetting
Some individuals may remain in lotic water bodies,
covered by a film of water or by water drops. This situation may enhance an
animal’s crypsis against terrestrial predators, by creating reflected shiny
spots on its dorsum matching the shiny spots in the water or substrate, for
example, rocks (Figures1(g)-1(h)).(e) Integumentary Structures
Some
integumentary structures seem to be associated with disruptive outlines and
thereby aid in concealment. Such structures include small, irregular ridges,
supraciliary processes (e.g., species ofProceratophrys and Ceratophrys), scalloped folds on
the outer edges of limbs (e.g., Cruziohyla
craspedopus), and calcars (e.g., several Hypsiboas spp.). Dorsal glands may also enhance crypsis by
promoting resemblance with lichens (e.g., Bokermannohyla
alvarengai, Itapotihyla langsdorffii, and Scinax
nebulosus) or mosses (e.g., Theloderma
corticale and other Vietnamese mossy frogs) (Figure 1).


### 3.1.2. Homotypy (Assimilation to Another Type)

It acts differently from camouflage: in homotypy animals
can be perceived by the predator. Homotypy involves the mimetic imitation of
another object (which can be the same or another species, an object of the
environment, or an undefined model), being, therefore, included as mimicry.(1) Concrete Homotypy (Actual Model)
The
model is definite or an existing species (or cluster of similar species).(a) Batesian Mimicry
The concept of Batesian mimicry [37] involves
the success of a specific coloration against a predator’s experience; that is,
predators learn to avoid unpalatable species, which are identified by their
aposematic coloration (which does not always mean bright colors: e.g., [11, 38]), odor, sound, or another signal. Thus, a mimic could
obtain protection by resembling the unpalatable or less palatable model. For
anurans, there are few cases described wherein some palatable frogs may mimic some
poison frogs (Table 2).
Batesian mimicry involves the predator’s ability to learn
or have innate knowledge. Several predators, such as invertebrates in general,
are not as well-endowed in terms of sight and memory as are mammals, and,
therefore, may not have been the promoters of selective pressures for the evolution
and persistence of Batesian mimicry (see also [11]).
A
Batesian mimic does not necessarily need to be identical to its model.
Sometimes, it may exhibit intermediate resemblances to two (or more) models. In
this manner, the mimic may escape from some predators that avoid one model and from
others that avoid the other model. This dual mimicry system has been proposed for
coral snake mimics [39] and may be present in anurans.
An intriguing situation is the Batesian mimicry
proposed for theLeptodactylus lineatus and Allobates femoralis complex. This
complex would actually represent a case of Müllerian mimicry (where both
species are unpalatable; see further explanations below), instead of Batesian
mimicry as initially proposed [16], as L. lineatus seems to be a noxious
species as well. Upon handling and fixing individuals of L. lineatus, they exude a great amount of milky, probably noxious
secretions (C. F. B. Haddad, personal observation). However, some tests performed
on A. femoralis indicated that this
species is not toxic (see [40], and references therein). If A. femoralis is not toxic and L. lineatus is, this would be once again
a case of Batesian mimicry where L.
lineatus is the model. If both species are discovered to be nontoxic, it
would be a case of Arithmetic mimicry (where both species are palatable; see further
explanations below). Therefore, the relationship of this complex remains unresolved
and requires further research.Table 2
Occurrence of Batesian and Müllerian mimicry in anurans, and distribution
overlap between species.
MimicModelMimetism typeSympatric speciesSourceAromobatidaeDendrobatidaeAllobates
zaparoAmeerega bilinguisBatesianYes[14]Allobates zaparoAmeerega parvulaBatesianYes[14]BrachycephalidaeDendrobatidaePristimantis gaigeaePhyllobates lugubrisBatesianYes[15]Pristimantis gaigeaePhyllobates aurotaeniaBatesianYes[15]LeptodactylidaeAromobatidaeLeptodactylus
lineatus**Allobates femoralis**BatesianYes[16]DendrobatidaeDendrobatidaeRanitomeya imitatorRanitomeya fantasticusMüllerianYes[9]Ranitomeya imitatorRanitomeya variabilisMüllerianYes[9]Ranitomeya imitatorRanitomeya ventrimaculataMüllerianYes[9]MantellidaeMantellidaeMantella laevigata*Mantella manery*MüllerianYes[17]Mantella baroni*Mantella madagascariensis*MüllerianYes[17]Mantella pulchra*Mantellacowanii*MüllerianYes[18]DendrobatidaeDendrobatidaePhyllobates aurotaenia*Phyllobates lugubris*MüllerianNoPresent studyIn* these cases, definition of the mimic and model is not possible.**Further studies are needed in this case: see text.(b) Browerian Mimicry
When individuals within a species differ in palatability to
predators, the more palatable individuals (mimics) will gain benefits from those
less palatable (models). The models can be of the same or opposite sex to the
mimics. Albeit never reported that this type of mimicry may be present in aromobatids,
bufonids, dendrobatids, mantellids, and myobatrachids, at least. Individuals of
the same noxious species of these families (cited above) acquire the alkaloids contained
in their noxious secretions from dietary arthropods (e.g., [41–43], and references therein). Therefore, if for
any reason a group of individuals within a species either does not feed on arthropods
that carry the alkaloids, feeds on them but at a lower rate/proportion, or does
not sequester these components, they will be less poisonous than the others
(e.g., [44–47]).
Indeed, there are reports that show spatial (geographic)
and temporal (seasonal) variation in the alkaloid profiles of poison frogs [48], which may support the Browerian mimicry theory for
anurans.(2) Abstract Homotypy (Virtual Model)
When the model is not an actual species, homotypy is an abstract.(a) Definable Model
It occurs
when the model looks like a general type of organism, or part or indirect
vestiges of another organism, but is not identifiable at species level. For
example, the deimatic eyespots present on the back of leiuperids, which could
resemble snakes’ eyes (see, e.g., [6]), but not of a
specific species of snake. Other examples are frogs that rest on leaves and
look like bird droppings (e.g., Dendropsophus
marmoratus and Theloderma spp.).
Besides this, the presence of calcars on many species of rainforest tree frogs,
and their absence in other anurans, may suggest that they might serve as points
of water runoff, mimicking drip tips of leaves [49, page 371].(b) Model Not Definable
Occurs
when the model is not identifiable at all, but a frightening or cryptic form is
conjured up. This seems to be the case for the leg interweaving behavior described
elsewhere (see [50]).


### 3.1.3. Nondeceitful Homotypy

This category was created (sensu [11]) basically for the inclusion of Müllerian
mimicry [51, 52] and Arithmetic mimicry [53]. In both
cases, the predator is not deceived, that is, the predator can recognize whether
the anuran is palatable or unpalatable. In this category, both the model and
the mimic are either unpalatable and/or dangerous in some way (Müllerian
mimicry), or palatable (arithmetic mimicry).These mimicry complexes are formed by species with similar
(or even exactly the same) color pattern. However, it is sometimes hard to
distinguish real nondeceitful homotypy from a possible phylogenetic influence; that
is, closely related species, such as two species ofDendrobates, may resemble one another due to a simplesiomorphy
(sharing of an ancestral character) and not because of coloration convergence (homoplasy).
Whether a convergence or a simplesiomorphy, the resemblance would benefit the
two (or more) species involved.(a) Müllerian Mimicry
Müllerian mimicry involves the mutual benefit of two dangerous (e.g., toxic,
noxious, unpalatable, able to harm the aggressor by any means, such as biting
and scratching, etc.) species by sharing similar phenotypes [51, 52]. To our
knowledge, there are only few cases of Müllerian mimicry in anurans (see Table 2);
however, other possible mimicry relationships may be suggested based on the
current reports. We may join two mimicry complexes of Mantella (M. baroni/madagascariensis and M. pulchra/cowanii) into a larger group of mimicry species, as all individuals
are sympatric and exhibit homochromy and homomorphy [17, 18]. Furthermore,
from the evidence of Batesian mimicry by Pristimantis
gaigeae with both Phyllobates aurotaenia and P. lugubris as models, we may
suggest another Müllerian mimicry system. This system would be comprised of P. aurotaenia and P. lugubris. These two species
are not sympatric, however, chronosympatry (presence of model and mimic in the
same time and place) is not a rule for the existence of mimicry [54, 55]; for instance, their past distributions could have overlapped (see also [15]), and/or the present distribution of selective agents
(predators) may overlap with the distribution of both species (including Batesian
mimic P. gaigeae).
Furthermore, it is possible that other Müllerian
mimicry systems exist that are not based on coloration but still comprise visual
mimetism. For example, if two different-colored species, or different morphs of
the same species, present the same toxic substances, they could be chemical
mimics. Therefore, based on properties other than color, such as body shape and
brightness, they could be part of a Müllerian mimicry ring (see also [56]). This would partly explain the several cases of polymorphism
among aposematic species (see below).(b) Arithmetic Mimicry
Similar sympatric edible species share the burden of
predation in proportion to their relative frequencies. In other words, the
higher the abundance of a certain (color) morph in the predator foraging area, the
lower the chances of an individual prey being preyed upon. In this case,
predator learning (ontogenetic or inherited) is irrelevant. To our knowledge,
arithmetic mimicry has never been reported for anurans; however, it may be a
very widespread phenomenon involving several sympatric (or even syntopic) similar
(e.g., in simultaneous homochromy, homomorphy, and homokinemy) species. As
examples of species pairs (or more), there are syntopicLeptodactylus furnarius and L.
jolyi; Dendropsophus nanus, D. sanborni, and D. minutus; Proceratophrys appendiculata, P. boiei, and P. melanopogon; as well as several species of Ischnocnema, all of them found
chronosympatrically in the Neotropical region.
Furthermore, two species with differences in
coloration (for instance), but of similar sizes (for instance), may also be
arithmetic mimics. Both of these edible species sharing a predator foraging
area may be equally nutritive; therefore, provided that the predator can
perceive that they are both nutritive, they will be nutritional arithmetic
mimics, benefited by the saturating theory (see [56]).


## 3.1.1. Camouflage

Camouflage
may be defined as the resemblance of an animal with a part of the
environment [7], especially as viewed by the predator at the time
and place in which the prey is most vulnerable to predation  (Endler [19]).In
post-metamorphic anurans, camouflage may be optical, chemical (e.g., production
of floral, leaf-like, and ammonia odors), or acoustic (may occur, e.g., when
frogs stop calling in the presence of a predator; e.g., [20]). In
what follows, we will give special reference to optical camouflage, which
implies avoidance of detection by possible predators.(1) Eucrypsis
Definition:
homochromy (imitation of reflected light) which is acting alone. The model is
undefined, that is, it is the background.(a) Visible Color Spectrum Mimesis
Many
frogs are cryptic with the substrate they use, and there are a great variety of
backgrounds and mimic frogs. As substrates, anurans may use rocks with lichens,
tree trunks, leaves, forest litter, as well as mossy and rocky fields, for
example. For any such substrates, there are mimic frogs that live there (Figure1). Eucrypsis may be strengthened or weakened by a predator's angle of vision; that
is, the anuran may be more cryptic from a lateral view than from a dorsal view
(Figures 1(f) and 1(e), resp.).
The
more distant predator is from the site occupied by an anuran, the higher may be
the crypsis benefits. For instance, it is easy to find aDendropsophus nanus in its reproductive site when we are close to it.
However, from a certain distance, the colors and shape of this hylid get mixed
with the general view of the area. The size and colors of D. nanus are generally similar to part of the foliage, and it is
hard to distinguish them from yellowish leaves (Figures 1(k), 1(l)).Different
situations of cryptic mimicry in anurans: (a)Dendropsophus
acreanus (Hylidae) on a tree trunk, (b) Bokermannohyla
alvarengai (Hylidae) on a rock with lichens,
(c) Ischnocnema guentheri (Brachycephalidae) on litter,  (d) green morph
of Hypsiboas prasinus (Hylidae)
perched on a leaf, ((e)-(f), resp.) dorsal and lateral views of Theloderma horridum (Rhacophoridae) on a tree, (g) Lankanectes corrugatus (Nyctibatrachidae) in a lotic
water body,  (h) Hylodes asper (Hylodidae) on a wet rock, (i) Proceratophrys
boiei (Cycloramphidae) on litter,  (j) Scythrophrys
sawayae (Leptodactylidae) on a dead leaf, (k) an adult male of Dendropsophus nanus (Hylidae) of
practically the same size and shape as the leaves  and (l) its reproductive site.(b) Nonvisible Color Spectrum Mimesis
Some studies
have shown that several anuran species, from different families, may show a
pronounced rise in reflectance in the infrared part of the spectrum (e.g., [21–23]). Furthermore, some predators of anurans, such as pit
vipers, may be able to perceive infrared wavebands [24]. Others, such
as rodents, other amphibians, lizards, and mainly birds, have tetrachromatic
color vision (including ultraviolet cones), and may, therefore, perceive ultraviolet
wavelengths (e.g., [25]). Therefore, it is possible that infrared reflectance
may have evolved for anurans to remain cryptic in the foliage (which also has the
same infrared reflectance property), even against those predators who are able
to detect infrared or ultraviolet spectra (e.g., [22, 26]).(2) Mimesis
Definition: it is homomorphy (imitation of morphology)
and/or homokinemy (imitation of movements), in addition to homochromy (defined before).
The model is defined, that is, it is an object.(a) Cryptic Mimesis
It holds when the model
is a dominant element of the mimic's environment, such as green or brown
leaves, sticks, rocks, lichens, and mosses. Many examples may be cited, but to mention
some, we may refer to species of generaProceratophrys and Scythrophrys which resemble fallen leaves (Figures 1(i), 1(j),
resp.), as well as some species of Theloderma and Bokermannohyla that resemble mosses
and lichens, respectively (Figure 1(b)).
The
phyllomedusines of genusPhasmahyla,
when walking, sway slightly as if caught by the movement of the wind (=
homokinemy). Indeed, their genus name Phasmahyla was coined in allusion to the similarity of their moving style with the walking-sticks of order Phasmatodea [27]. The illusion
created by this behavior is increased with the leaf-like color pattern of this
species.(b) Phaneric Mimesis
It holds when the
model is an isolated and conspicuous inanimate element of the mimic’s
environment, such as animal droppings or rocks (when there are few rocks in the
environment). As examples, we may cite someTheloderma spp. and Dendropsophus marmoratus,
which resemble bird droppings, and many species of Rhinella and Bufo that
resemble stones on the floor.(3) Factors of Camouflage Enhancement
Both eucrypsis
and mimesis imply camouflage, which could be strengthened by (a) countershading,
(b) disruptive coloration, (c) shadow camouflage, (d) wetting, and (e)
integumentary structures.(a) Countershading
Countershading
occurs when the anuran's pigmentation is darker dorsally and lighter ventrally.
This transition may be gradual or abrupt, which could involve different
camouflage strategies (see [28, 29]).
Two
main functions have been attributed to countershading. (i) it is believed to have
the effect of reducing conspicuous shadows cast on the ventral region of an
animal's body. In essence, the distribution of light on objects lit from above
will cause unequal reflection of light by a solid body of uniform color. Such
shadows could provide predators with visual cues to a prey's shape and
projection. Countershading, therefore, reduces the ease with which prey is
detected by potential predators by counterbalancing the effects of shadowing.
This effect occurs mainly in animals that present a gradual transition of colors [28], and should be properly named “self-shadow concealment” [29]. (ii) Countershading coloration would work via background
matching; that is, when seen from the top, the dorsum (if cryptic colored) blends
into the background below, which could be a body of water (when the anuran is
swimming or floating) or dry-to-flooded ground (when the anuran is on the floor
or perched in the vegetation). When seen from below, the lighter ventral area
blends into the sun or moonlight (see [29]). This second
explanation generally occurs with an abrupt
transition of colors and seems to
be the more adequate for anurans.
Countershading
could result from selective pressures other than predation avoidance. For
example, the dorsal surface must be protected against the damaging properties
of UV light and/or abrasion Kiltie [30, 31], and the
ventral side does not need to be pigmented, as pigmentation may be costly
[29]. Therefore, the occurrence of countershading may result
from multiple factors.
This
system is so widespread among aquatic and terrestrial fauna that several
authors have stated that it is perhaps the most universal feature of animal
coloration (see [29] and references therein). Likewise, it is
present in several anuran species and might work against terrestrial predators,
for example, which may be on the ground when the anuran is perched on a tree branch.
In aquatic species, such as the pipids (e.g., Pipa spp. and Xenopus spp.), the system may work as described for fishes.(b) Disruptive Coloration
Disruptive
coloration is a color pattern that breaks the appearance of body form. Several anuran
species have dorsal lines and/or blotches that may be considered constitutive
of disruptive coloration, breaking the general outline of the body. Some
species may enhance their camouflage by having high-contrast lines on the edges
of colored patterns (see [32]). In addition to this,
several species present lateral lines that cross the eyes, breaking their
rounded shape (Figure 1(j)). These are the most common forms of disruptive
coloration in anurans.
A
possible variation is the presence of aposematic coloration (see what follows for
an explanation of aposematism) simultaneously with disruptive coloration,
depending on the predator and/or brightness of the night. This may occur
because the colorful stripes and/or blotches of an aposematic anuran (Figure2(a))
may become a disruptive pattern when seen by a color-blind predator, or by a
color vision predator hunting on dark nights (Figure 2(b); see also [33, 34]).
Recently,
it has been suggested and/or demonstrated that disruptive coloration is
advantageous compared to simple eucrypsis (see [35, 36], and references therein).(a) An
aposematicOophaga lehmanni (Dendrobatidae)
(b) may have disruptive coloration on dark nights or when searched for by a
color-blind predator. (c)  An adult and a juvenile Hypsiboas semilineatus (Hylidae),  (d) an amplectant pair of Rhinella icterica (Bufonidae), and ((e)-(f))
two morphs of Physalaemus cuvieri (Leiuperidae)  are examples
of polyphenism. ((g)-(h)) Flash color exhibited by Hypsiboas
caingua (Hylidae), ((i)-(j)) deimatic
behavior by Eupemphix nattereri (Leiuperidae), and ((k)–(l)) thanatosis
by Melanophryniscus moreirae (Bufonidae).(c) Shadow Camouflage
Anurans may rest in areas with combined spots of sunlight
and shade, making it difficult to recognize the animals on the substrate. If
part of the anuran is exposed to sunlight and the other part is in shadow, such
light play may enhance the anuran’s disruptive pattern (e.g., [32]).(d) Wetting
Some individuals may remain in lotic water bodies,
covered by a film of water or by water drops. This situation may enhance an
animal’s crypsis against terrestrial predators, by creating reflected shiny
spots on its dorsum matching the shiny spots in the water or substrate, for
example, rocks (Figures1(g)-1(h)).(e) Integumentary Structures
Some
integumentary structures seem to be associated with disruptive outlines and
thereby aid in concealment. Such structures include small, irregular ridges,
supraciliary processes (e.g., species ofProceratophrys and Ceratophrys), scalloped folds on
the outer edges of limbs (e.g., Cruziohyla
craspedopus), and calcars (e.g., several Hypsiboas spp.). Dorsal glands may also enhance crypsis by
promoting resemblance with lichens (e.g., Bokermannohyla
alvarengai, Itapotihyla langsdorffii, and Scinax
nebulosus) or mosses (e.g., Theloderma
corticale and other Vietnamese mossy frogs) (Figure 1).


## 3.1.2. Homotypy (Assimilation to Another Type)

It acts differently from camouflage: in homotypy animals
can be perceived by the predator. Homotypy involves the mimetic imitation of
another object (which can be the same or another species, an object of the
environment, or an undefined model), being, therefore, included as mimicry.(1) Concrete Homotypy (Actual Model)
The
model is definite or an existing species (or cluster of similar species).(a) Batesian Mimicry
The concept of Batesian mimicry [37] involves
the success of a specific coloration against a predator’s experience; that is,
predators learn to avoid unpalatable species, which are identified by their
aposematic coloration (which does not always mean bright colors: e.g., [11, 38]), odor, sound, or another signal. Thus, a mimic could
obtain protection by resembling the unpalatable or less palatable model. For
anurans, there are few cases described wherein some palatable frogs may mimic some
poison frogs (Table 2).
Batesian mimicry involves the predator’s ability to learn
or have innate knowledge. Several predators, such as invertebrates in general,
are not as well-endowed in terms of sight and memory as are mammals, and,
therefore, may not have been the promoters of selective pressures for the evolution
and persistence of Batesian mimicry (see also [11]).
A
Batesian mimic does not necessarily need to be identical to its model.
Sometimes, it may exhibit intermediate resemblances to two (or more) models. In
this manner, the mimic may escape from some predators that avoid one model and from
others that avoid the other model. This dual mimicry system has been proposed for
coral snake mimics [39] and may be present in anurans.
An intriguing situation is the Batesian mimicry
proposed for theLeptodactylus lineatus and Allobates femoralis complex. This
complex would actually represent a case of Müllerian mimicry (where both
species are unpalatable; see further explanations below), instead of Batesian
mimicry as initially proposed [16], as L. lineatus seems to be a noxious
species as well. Upon handling and fixing individuals of L. lineatus, they exude a great amount of milky, probably noxious
secretions (C. F. B. Haddad, personal observation). However, some tests performed
on A. femoralis indicated that this
species is not toxic (see [40], and references therein). If A. femoralis is not toxic and L. lineatus is, this would be once again
a case of Batesian mimicry where L.
lineatus is the model. If both species are discovered to be nontoxic, it
would be a case of Arithmetic mimicry (where both species are palatable; see further
explanations below). Therefore, the relationship of this complex remains unresolved
and requires further research.Table 2
Occurrence of Batesian and Müllerian mimicry in anurans, and distribution
overlap between species.
MimicModelMimetism typeSympatric speciesSourceAromobatidaeDendrobatidaeAllobates
zaparoAmeerega bilinguisBatesianYes[14]Allobates zaparoAmeerega parvulaBatesianYes[14]BrachycephalidaeDendrobatidaePristimantis gaigeaePhyllobates lugubrisBatesianYes[15]Pristimantis gaigeaePhyllobates aurotaeniaBatesianYes[15]LeptodactylidaeAromobatidaeLeptodactylus
lineatus**Allobates femoralis**BatesianYes[16]DendrobatidaeDendrobatidaeRanitomeya imitatorRanitomeya fantasticusMüllerianYes[9]Ranitomeya imitatorRanitomeya variabilisMüllerianYes[9]Ranitomeya imitatorRanitomeya ventrimaculataMüllerianYes[9]MantellidaeMantellidaeMantella laevigata*Mantella manery*MüllerianYes[17]Mantella baroni*Mantella madagascariensis*MüllerianYes[17]Mantella pulchra*Mantellacowanii*MüllerianYes[18]DendrobatidaeDendrobatidaePhyllobates aurotaenia*Phyllobates lugubris*MüllerianNoPresent studyIn* these cases, definition of the mimic and model is not possible.**Further studies are needed in this case: see text.(b) Browerian Mimicry
When individuals within a species differ in palatability to
predators, the more palatable individuals (mimics) will gain benefits from those
less palatable (models). The models can be of the same or opposite sex to the
mimics. Albeit never reported that this type of mimicry may be present in aromobatids,
bufonids, dendrobatids, mantellids, and myobatrachids, at least. Individuals of
the same noxious species of these families (cited above) acquire the alkaloids contained
in their noxious secretions from dietary arthropods (e.g., [41–43], and references therein). Therefore, if for
any reason a group of individuals within a species either does not feed on arthropods
that carry the alkaloids, feeds on them but at a lower rate/proportion, or does
not sequester these components, they will be less poisonous than the others
(e.g., [44–47]).
Indeed, there are reports that show spatial (geographic)
and temporal (seasonal) variation in the alkaloid profiles of poison frogs [48], which may support the Browerian mimicry theory for
anurans.(2) Abstract Homotypy (Virtual Model)
When the model is not an actual species, homotypy is an abstract.(a) Definable Model
It occurs
when the model looks like a general type of organism, or part or indirect
vestiges of another organism, but is not identifiable at species level. For
example, the deimatic eyespots present on the back of leiuperids, which could
resemble snakes’ eyes (see, e.g., [6]), but not of a
specific species of snake. Other examples are frogs that rest on leaves and
look like bird droppings (e.g., Dendropsophus
marmoratus and Theloderma spp.).
Besides this, the presence of calcars on many species of rainforest tree frogs,
and their absence in other anurans, may suggest that they might serve as points
of water runoff, mimicking drip tips of leaves [49, page 371].(b) Model Not Definable
Occurs
when the model is not identifiable at all, but a frightening or cryptic form is
conjured up. This seems to be the case for the leg interweaving behavior described
elsewhere (see [50]).


## 3.1.3. Nondeceitful Homotypy

This category was created (sensu [11]) basically for the inclusion of Müllerian
mimicry [51, 52] and Arithmetic mimicry [53]. In both
cases, the predator is not deceived, that is, the predator can recognize whether
the anuran is palatable or unpalatable. In this category, both the model and
the mimic are either unpalatable and/or dangerous in some way (Müllerian
mimicry), or palatable (arithmetic mimicry).These mimicry complexes are formed by species with similar
(or even exactly the same) color pattern. However, it is sometimes hard to
distinguish real nondeceitful homotypy from a possible phylogenetic influence; that
is, closely related species, such as two species ofDendrobates, may resemble one another due to a simplesiomorphy
(sharing of an ancestral character) and not because of coloration convergence (homoplasy).
Whether a convergence or a simplesiomorphy, the resemblance would benefit the
two (or more) species involved.(a) Müllerian Mimicry
Müllerian mimicry involves the mutual benefit of two dangerous (e.g., toxic,
noxious, unpalatable, able to harm the aggressor by any means, such as biting
and scratching, etc.) species by sharing similar phenotypes [51, 52]. To our
knowledge, there are only few cases of Müllerian mimicry in anurans (see Table 2);
however, other possible mimicry relationships may be suggested based on the
current reports. We may join two mimicry complexes of Mantella (M. baroni/madagascariensis and M. pulchra/cowanii) into a larger group of mimicry species, as all individuals
are sympatric and exhibit homochromy and homomorphy [17, 18]. Furthermore,
from the evidence of Batesian mimicry by Pristimantis
gaigeae with both Phyllobates aurotaenia and P. lugubris as models, we may
suggest another Müllerian mimicry system. This system would be comprised of P. aurotaenia and P. lugubris. These two species
are not sympatric, however, chronosympatry (presence of model and mimic in the
same time and place) is not a rule for the existence of mimicry [54, 55]; for instance, their past distributions could have overlapped (see also [15]), and/or the present distribution of selective agents
(predators) may overlap with the distribution of both species (including Batesian
mimic P. gaigeae).
Furthermore, it is possible that other Müllerian
mimicry systems exist that are not based on coloration but still comprise visual
mimetism. For example, if two different-colored species, or different morphs of
the same species, present the same toxic substances, they could be chemical
mimics. Therefore, based on properties other than color, such as body shape and
brightness, they could be part of a Müllerian mimicry ring (see also [56]). This would partly explain the several cases of polymorphism
among aposematic species (see below).(b) Arithmetic Mimicry
Similar sympatric edible species share the burden of
predation in proportion to their relative frequencies. In other words, the
higher the abundance of a certain (color) morph in the predator foraging area, the
lower the chances of an individual prey being preyed upon. In this case,
predator learning (ontogenetic or inherited) is irrelevant. To our knowledge,
arithmetic mimicry has never been reported for anurans; however, it may be a
very widespread phenomenon involving several sympatric (or even syntopic) similar
(e.g., in simultaneous homochromy, homomorphy, and homokinemy) species. As
examples of species pairs (or more), there are syntopicLeptodactylus furnarius and L.
jolyi; Dendropsophus nanus, D. sanborni, and D. minutus; Proceratophrys appendiculata, P. boiei, and P. melanopogon; as well as several species of Ischnocnema, all of them found
chronosympatrically in the Neotropical region.
Furthermore, two species with differences in
coloration (for instance), but of similar sizes (for instance), may also be
arithmetic mimics. Both of these edible species sharing a predator foraging
area may be equally nutritive; therefore, provided that the predator can
perceive that they are both nutritive, they will be nutritional arithmetic
mimics, benefited by the saturating theory (see [56]).


## 3.2. Deceptive Coloration

### 3.2.1. Behavioral Display of Colors

Many
anurans may exhibit deceptive coloration, either intentionally or not, by
performing movements (e.g., flash color behavior) or by adopting specific
postures (e.g., body raising).A
fleeing anuran may escape from predators by displaying a flash of aposematic
color(s), generally followed by remaining motionless. This is known as flash
color behavior. This coloration is only visible when the anuran is moving
(generally while jumping), and concealed during resting posture (Figures2(g)-2(h)). Flash color
is widespread among anurans, occurring in several species and families. In the
Neotropics, it is very common in species of genera Scinax and Hypsiboas (Hylidae).Flash
color behavior may serve to disorientate and confuse an attacking predator [7] and/or warn predators of the presence of toxins [57]. These two distinct functions, and the implied predator responses, may
vary among individuals or species of predator. In other words, some predators
may be warned, while some may get confused. In this latter case, the predator
may lose the anuran: the flash behavior may precede the motionless behavior,
creating a prey search image that quickly disappears [7, 58]. Also, flash color behavior may halt the predator’s attack for an
instant and, thus, provide extra time for the frog to escape [59].Another
possibility of color display is body raising. For example, in some leiuperids
(e.g.,Eupemphix nattereri, Physalaemus deimaticus, and Pleurodema brachyops), when individuals
lift their hindparts, they exhibit a pair of black eyespots (Figures 2(i)-2(j)). Similarly to
flash color behavior, this exhibition may be viewed as an aposematic signal (as
these species have large poison glands below the eye-spots) or may be a deceptive
signal. In this latter case, the predator may have the illusion of facing a
different (and larger) animal. Therefore, it would be better classified as an abstract
homotypy where the model is definable (see above).


### 3.2.2. Polymorphism

Polymorphism
in anurans is characterized by the presence of fixed chromatic phenotypes
within or between populations. The individuals seem unable to change their
color, so there must be genetic control involved. Polymorphism may benefit the
anuran in such a way that one or more of the phenotypes are not included in the
predator’s search image. Several species are known to present different
chromatic morphotypes, and such polymorphism may occur in three ways as
follows.(a) between Individuals, Independent of Sex and Life Stage
Two
morphotypes: for example, some adult individuals ofPhysalaemus cuvieri (Leiuperidae) and Paratelmatobius spp. (Leptodactylidae) are green, while others are
brown (Figures 2(e)-2(f)). Another type
of color dimorphism is exhibited by individuals of Leptodactylus fuscus (Leptodactylidae), which may or may not have a
dorso-vertebral white line.
More
than two morphotypes: several species of cryptic generaEleutherodactylus and Ischnocnema (Brachycephalidae) exhibit many different color morphotypes [60]. Even in aposematic species, this sort of
polymorphism can also be observed; for example, in Anomaloglossus
beebei (Aromobatidae), there are five color morphotypes [61], and in Oophaga pumilio (Dendrobatidae), there are at least 15 color
morphotypes (see, e.g., [5, 23]).
Multiple aposematic phenotypes are also observed in other dendrobatids [62] and African mantellids (see, e.g., [63]). Multiple
aposematic phenotypes may add the benefits of aposematism to the benefit
regarding predator search image (see before).(b) between Life Stages: Juveniles Different from Adults
This is
the case ofHypsiboas geographicus, H. semilineatus, H. lundii, H. pardalis, and H. raniceps (Hylidae), for instance, where juveniles have a totally
different coloration from adults, independent of sex (Figure 2(c)).(c) between Sexes: Males Different from Females
As
examples, we may citeRhinella icterica (Bufonidae),
where males are light yellowish and females are black and white (Figure 2(d)); Leptopelis vermiculatus (Arthroleptidae), where males are green and females are brown; and most
contrasting is Incilius periglenes (Bufonidae),
where males are bright orange and females are black, red, and yellow.


### 3.2.3. Polyphenism

Polyphenism is the ability to
generate different phenotypes, by color changing in this case, by the same
individual. Polyphenism may be a better term to describe this phenomenon than
polymorphism, which generally implies a stronger genetic element for each
particular appearance [64].Many anurans can change their dorsal
coloration by rearranging their chromatophores, which involves sophisticated
physiological control of skin structures. There
is a continuous gradient of color change timing in anurans: the change may
occur instantaneously, or may take a few minutes, hours, days, or even weeks to
occur.Some
species may change their color very quickly. We placed one individual ofBokermannohyla circumdata (Hylidae) in a
dark place (under tree bark) and left another individual exposed to the
laboratory light. After 15 minutes, they were completely different from their
initial, dark reddish-brownish coloration. The first individual (kept in the
dark) was much darker, almost black, whereas the second individual (exposed)
was almost white. A similar polyphenism was described for Bokermannohyla alvarengai, but in this case, the color change was
studied with regard to physiological adjustments for temperature and water loss
control [4].The
dorsal coloration ofScinax
fuscomarginatus (Hylidae) males is yellowish during the night (during reproductive
activity) and grayish or brownish during the day. This may be related to the
specific site they use: during the night, they remain perched on yellowish
grass vegetation [65], while during the day they can be
found in dark sites, such as tree holes, under tree bark, and in the middle of
clumps of grass. Conversely, this color change may be due to testosterone
amount during reproductive activity (calling), as the yellowish males also have
an odor which is distinct from the one they have during the daytime resting period.
Additionally, individuals killed while still yellowish left a yellow tinge in
the preservative liquid (formalin, alcohol). We recorded the same phenomenon
for Scinax fuscovarius and S. hayii. Furthermore, some
phyllomedusines can change from purplish during night activity to greenish
during daytime resting. Such polyphenism was observed in Phasmahyla cochranae, P.
guttata, and P. jandaia. This
phenomenon can occasionally be observed in Phyllomedusa
azurea, P. megacephala, and P. rohdei (see colored pictures in [66]).We observed a seasonal
polyphenism inHypsiboas prasinus (Hylidae), in which a higher presence of green individuals occurred mainly in
the hot, rainy season of the year, whereas a higher presence of brown
individuals occurred in the cold, dry season of the year. This pattern overlaps
with the frequency of green and brown leaves in the Mesophytic Semideciduos Forest where this species dwells [67]: the peak of leaf fall precedes the peak of brown
morphs and the peak of leaf flushing precedes the peak of green morphs (Figure 3). Seasonal color changing has also been observed in Pseudacris regilla (Hylidae), and has been considered a response to divergent selection for crypsis in
a heterogeneous, seasonally variable environment [68]. This is likely to be an explanation for the
polymorphism of H. prasinus as well.Seasonal
variation (March 1988 to May 1989) in the dorsal coloration of reproductive
males ofHypsiboas prasinus (Hylidae),
and number of plants that exhibited leaf fall (brown lines) and leaf flushing
(green lines), in Serra do Japi, Jundiaí, São Paulo, Brazil. Brown bars
represent brown morphs (upper picture), green bars represent green morphs
(lower picture), and olive bars represent intermediate (olive) coloration
morphs. Plant phenology data were obtained from Morellato et al. [67].Polyphenism may be
advantageous over polymorphism because the anuran may select a substrate and then
adjust its color pattern. Polymorphic anurans may find adequate substrates to
fit their general coloration, and such are not necessarily hard to find, but
polyphenic species may have a wider range of substrates that they can use.


## 3.2.1. Behavioral Display of Colors

Many
anurans may exhibit deceptive coloration, either intentionally or not, by
performing movements (e.g., flash color behavior) or by adopting specific
postures (e.g., body raising).A
fleeing anuran may escape from predators by displaying a flash of aposematic
color(s), generally followed by remaining motionless. This is known as flash
color behavior. This coloration is only visible when the anuran is moving
(generally while jumping), and concealed during resting posture (Figures2(g)-2(h)). Flash color
is widespread among anurans, occurring in several species and families. In the
Neotropics, it is very common in species of genera Scinax and Hypsiboas (Hylidae).Flash
color behavior may serve to disorientate and confuse an attacking predator [7] and/or warn predators of the presence of toxins [57]. These two distinct functions, and the implied predator responses, may
vary among individuals or species of predator. In other words, some predators
may be warned, while some may get confused. In this latter case, the predator
may lose the anuran: the flash behavior may precede the motionless behavior,
creating a prey search image that quickly disappears [7, 58]. Also, flash color behavior may halt the predator’s attack for an
instant and, thus, provide extra time for the frog to escape [59].Another
possibility of color display is body raising. For example, in some leiuperids
(e.g.,Eupemphix nattereri, Physalaemus deimaticus, and Pleurodema brachyops), when individuals
lift their hindparts, they exhibit a pair of black eyespots (Figures 2(i)-2(j)). Similarly to
flash color behavior, this exhibition may be viewed as an aposematic signal (as
these species have large poison glands below the eye-spots) or may be a deceptive
signal. In this latter case, the predator may have the illusion of facing a
different (and larger) animal. Therefore, it would be better classified as an abstract
homotypy where the model is definable (see above).


## 3.2.2. Polymorphism

Polymorphism
in anurans is characterized by the presence of fixed chromatic phenotypes
within or between populations. The individuals seem unable to change their
color, so there must be genetic control involved. Polymorphism may benefit the
anuran in such a way that one or more of the phenotypes are not included in the
predator’s search image. Several species are known to present different
chromatic morphotypes, and such polymorphism may occur in three ways as
follows.(a) between Individuals, Independent of Sex and Life Stage
Two
morphotypes: for example, some adult individuals ofPhysalaemus cuvieri (Leiuperidae) and Paratelmatobius spp. (Leptodactylidae) are green, while others are
brown (Figures 2(e)-2(f)). Another type
of color dimorphism is exhibited by individuals of Leptodactylus fuscus (Leptodactylidae), which may or may not have a
dorso-vertebral white line.
More
than two morphotypes: several species of cryptic generaEleutherodactylus and Ischnocnema (Brachycephalidae) exhibit many different color morphotypes [60]. Even in aposematic species, this sort of
polymorphism can also be observed; for example, in Anomaloglossus
beebei (Aromobatidae), there are five color morphotypes [61], and in Oophaga pumilio (Dendrobatidae), there are at least 15 color
morphotypes (see, e.g., [5, 23]).
Multiple aposematic phenotypes are also observed in other dendrobatids [62] and African mantellids (see, e.g., [63]). Multiple
aposematic phenotypes may add the benefits of aposematism to the benefit
regarding predator search image (see before).(b) between Life Stages: Juveniles Different from Adults
This is
the case ofHypsiboas geographicus, H. semilineatus, H. lundii, H. pardalis, and H. raniceps (Hylidae), for instance, where juveniles have a totally
different coloration from adults, independent of sex (Figure 2(c)).(c) between Sexes: Males Different from Females
As
examples, we may citeRhinella icterica (Bufonidae),
where males are light yellowish and females are black and white (Figure 2(d)); Leptopelis vermiculatus (Arthroleptidae), where males are green and females are brown; and most
contrasting is Incilius periglenes (Bufonidae),
where males are bright orange and females are black, red, and yellow.


## 3.2.3. Polyphenism

Polyphenism is the ability to
generate different phenotypes, by color changing in this case, by the same
individual. Polyphenism may be a better term to describe this phenomenon than
polymorphism, which generally implies a stronger genetic element for each
particular appearance [64].Many anurans can change their dorsal
coloration by rearranging their chromatophores, which involves sophisticated
physiological control of skin structures. There
is a continuous gradient of color change timing in anurans: the change may
occur instantaneously, or may take a few minutes, hours, days, or even weeks to
occur.Some
species may change their color very quickly. We placed one individual ofBokermannohyla circumdata (Hylidae) in a
dark place (under tree bark) and left another individual exposed to the
laboratory light. After 15 minutes, they were completely different from their
initial, dark reddish-brownish coloration. The first individual (kept in the
dark) was much darker, almost black, whereas the second individual (exposed)
was almost white. A similar polyphenism was described for Bokermannohyla alvarengai, but in this case, the color change was
studied with regard to physiological adjustments for temperature and water loss
control [4].The
dorsal coloration ofScinax
fuscomarginatus (Hylidae) males is yellowish during the night (during reproductive
activity) and grayish or brownish during the day. This may be related to the
specific site they use: during the night, they remain perched on yellowish
grass vegetation [65], while during the day they can be
found in dark sites, such as tree holes, under tree bark, and in the middle of
clumps of grass. Conversely, this color change may be due to testosterone
amount during reproductive activity (calling), as the yellowish males also have
an odor which is distinct from the one they have during the daytime resting period.
Additionally, individuals killed while still yellowish left a yellow tinge in
the preservative liquid (formalin, alcohol). We recorded the same phenomenon
for Scinax fuscovarius and S. hayii. Furthermore, some
phyllomedusines can change from purplish during night activity to greenish
during daytime resting. Such polyphenism was observed in Phasmahyla cochranae, P.
guttata, and P. jandaia. This
phenomenon can occasionally be observed in Phyllomedusa
azurea, P. megacephala, and P. rohdei (see colored pictures in [66]).We observed a seasonal
polyphenism inHypsiboas prasinus (Hylidae), in which a higher presence of green individuals occurred mainly in
the hot, rainy season of the year, whereas a higher presence of brown
individuals occurred in the cold, dry season of the year. This pattern overlaps
with the frequency of green and brown leaves in the Mesophytic Semideciduos Forest where this species dwells [67]: the peak of leaf fall precedes the peak of brown
morphs and the peak of leaf flushing precedes the peak of green morphs (Figure 3). Seasonal color changing has also been observed in Pseudacris regilla (Hylidae), and has been considered a response to divergent selection for crypsis in
a heterogeneous, seasonally variable environment [68]. This is likely to be an explanation for the
polymorphism of H. prasinus as well.Seasonal
variation (March 1988 to May 1989) in the dorsal coloration of reproductive
males ofHypsiboas prasinus (Hylidae),
and number of plants that exhibited leaf fall (brown lines) and leaf flushing
(green lines), in Serra do Japi, Jundiaí, São Paulo, Brazil. Brown bars
represent brown morphs (upper picture), green bars represent green morphs
(lower picture), and olive bars represent intermediate (olive) coloration
morphs. Plant phenology data were obtained from Morellato et al. [67].Polyphenism may be
advantageous over polymorphism because the anuran may select a substrate and then
adjust its color pattern. Polymorphic anurans may find adequate substrates to
fit their general coloration, and such are not necessarily hard to find, but
polyphenic species may have a wider range of substrates that they can use.


## 3.3. Aposematism

Aposematic
coloration has also been referred to as sematic, conspicuous, or warning
coloration. Aposematism is the presence of contrasting and conspicuous coloration
that is generally related to the presence of skin toxins in the individuals [7, 58]. Furthermore, it may also signalize that the
anuran is dangerous or unpleasant in any other way. For example, aposematic
anurans may bite, exhibit spine aggression, and/or produce loud defensive
screams.Aposematic
coloration is generally bright red, orange, yellow, and/or blue on a dark
(generally black), contrasting background. This aposematic coloration is most
commonly widespread over the entire body, such as in species ofAllobates (Aromobatidae), Ameerega and Dendrobates (Dendrobatidae), Mantella (Mantellidae), Atelopus (Bufonidae), and Brachycephalus (Brachycephalidae).Aposematic
coloration is often confined to parts that are usually concealed when the frog
is in its resting posture (e.g., some leiuperids (Eupemphix nattereri and Physalaemus spp.), bombinatorids (Bombina spp.), hylids (Phyllomedusa spp. and Hypsiboas of the marmoratus group), bufonids (Melanophryniscus spp.), and leptodactylids (Leptodactylus of the pentadactylus group)). In
this case, the bright coloration is generally present on the back of the
thighs, the underside of the body, the limbs, feet, and hands, and is displayed
by specific posturing such as the unken reflex [69] or body raising [65].In
species ofCeratoprhys and Hemiphractus, aposematic coloration may
be present on the lips or on the tongue, respectively, which are displayed when
the individuals perform the mouth-gapping display or emit defensive screams. In Phyllomedusa spp., the bright, contrasting
coloration may be displayed intentionally (e.g., during foot flagging) or when
the individuals walk on tree branches. The foot signaling of Atelopus zeteki, in addition to being an
intraspecific communication, may be a visual display, including aposematic
coloration (bright yellow contrasting with black stripes) for potential
predators [70]. In Ameerega flavopicta, there
seems to be a relationship between parental care and body raising [71]. Several species have a conspicuously colored belly (or other
underside parts; e.g., Paratelmatobius spp., Leptodactylus pustulatus, or Melanophryniscus spp.). When facing a
predator, they might not present any specific behavior to display these colors.
However, they may display thanatosis (a widespread behavior in frogs) and,
during handling by the predator, the anurans may be turned upside down and
would thus display the aposematic coloration (Figures 2(k)-2(l)). Species of Oreophrynella, after displaying “balling
behavior" while fleeing, may stop belly-side-up, exposing their bright,
contrasting ventral coloration [72].Several factors are involved in the evolution of
aposematism, such as unpalatability, honest signals, relative predator-prey
abundance-dependence, and kin selection (review in [73]). In
anurans, aposematism has evolved multiple times (e.g., [74–76]). However, some of these authors have based
their results on the hypothesis of evolutionary relationships that have been
recently modified or complemented [40, 77].
Therefore, a new overview of these evolutionary approaches to defense is
needed, because their assumptions may be modified. For example, Summers and
Clough [74] did their study based on the assumption that family Dendrobatidae
(as considered at that time) was monophyletic, and that the toxic aposematic
dendrobatids clade was also monophyletic. However, this apparent monophyly has been
rejected [75, 76], the former dendrobatid
family has been divided into two sister families (Dendrobatidae and
Aromobatidae), and the toxic species are divided into several genera (e.g., Adelphobates,
Allobates, Ameerega, Dendrobates, Epipedobates, Hyloxalus, Myniobates, and Oophaga) in both families [40].Although
there may be changes to the phylogenetic hypotheses, it is still possible that aposematic
coloration has evolved in tandem with toxicity in anurans of the Bufonidae,
Dendrobatidae, Aromobatidae, and Mantellidae families, as previously proposed (e.g., [43, 74]). “If differences among species in
dietary preferences or predatory capabilities are heritable, then natural
selection could act to favor brighter coloration in species that consistently
have preferences for or access to prey with more or more potent toxins”
[74]. Speculations apart, the most evident fact is that
anuran aposematism has evolved by means of multiple convergent radiations,
within the order, its families, and/or its genera (e.g., [43, 75, 76, 78]).


## 4. Discussion

As we
observed above, anuran coloration may provide protection against predators by
providing concealment (e.g., camouflage, homotypy, and arithmetic mimicry) by
alerting the predator about a possible hidden danger or unpleasant
characteristic (aposematism), or by deceiving predators (deceptive coloration
and some cases of mimicry). These strategies may act on the two first stages of
predation as reviewed by Endler [79]: detection and identification.The
different types of defensive coloration presented in this study may have been
selected differently throughout anuran evolution (see Table3). Cryptic
coloration (e.g., camouflage) may have been selected for by predation pressures
imposed by predators upon anurans (defensive strategies), by the predatory
behavior of anurans upon their prey (feeding strategies), or by both. All
deceptive coloration categories (polyphenism, polymorphism, and behavioral
display of colors) are directly related with predator search image. Therefore,
the pressures that may have promoted them are tightly associated with the
predator’s vision and cerebral capability. Aposematic coloration may have multiple
factors involved in its evolution. It may have evolved by means of sexual
selection and/or after the acquisition of any dangerous or unpleasant defensive
strategy. In the former case, in anurans, such strategies can be biting, spine
aggression, defensive screams, unpalatability (in terms of bad taste), or, most
commonly, noxious skin secretions. Therefore, we would not expect to find a harmless
aposematic anuran, except for those involved in mimicry rings (mainly Batesian
and Browerian). Indeed, as far as we know, every aposematic anuran (except for some
mimics) produces harmful defenses, such as poison (e.g., some species of Mantellidae,
Dendrobatidae, and Brachycephalidae: [40, 43, 80]), or aggressive defenses (e.g., some
species of Ceratophryidae and Leptodactylidae: L. F. Toledo, I. Sazima, and C. F.
B. Haddad, unpublished data). Therefore, multiple selection factors may be
synergistically involved in the origin and evolution of anuran coloration.Table 3
Characteristics,
benefits acquired, and constraints involved in the evolution of different
classes of anuran coloration.
Coloration classesMain characteristicBenefits acquiredEvolutionary constraints involvedCryptic colorationBackground matchingDetection avoidance
(by prey and predators)Predator and prey search imageAposematic colorationBackground contrastingPredator avoidancePredator learning, presence of harmful defenses*,
sexual selectionReproductive successDeceptive colorationDissuasive colorationPredator avoidancePredator search image, sexual selectionReproductive successMay* be an exception in cases of Browerian and
Batesian mimicry.Use of colors by anurans as a defensive strategy is a very
large field of knowledge, and quite unexplored up to the present moment. Now, with
this review, we attempt to organize part of our knowledge, generating at least
a standardization of the nomenclature that may be applied to anuran coloration as
regarding defensive strategy. Also, we added some information and insights on the
relationships between predation and the defensive mechanisms of
post-metamorphic anurans. From this point forward, we recommend some lines of
research which may (i) complement this and other recent reviews with more
observational information (which is truly lacking at present), (ii) focus on
specific defensive strategies against predators and reports of predator-prey
interactions, (iii) complete a broader, meta-analysis of predator-prey interactions,
and (iv) advance further in the understanding of the evolution (including
phylogenetic approaches) of defensive strategies and their relationships with
present and past predators.



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