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.
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., [
Anurans are remarkable for their
color patterns, which may range from a uniform black dorsum, as in
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.
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 [
The use of colors can be divided into three major
categories: mimicry, deceptive coloration, and aposematism (Table
Major categories and subcategories of colors used as defensive strategies in post-metamorphic anurans.
Major | 2nd major | 3rd major | Subcategories |
---|---|---|---|
Eucrypsis | Visible color spectrum mimesis | ||
Camouflage | Nonvisible color spectrum mimesis | ||
Mimesis | Cryptic mimesis | ||
Phaneric mimesis | |||
Mimicry | Concrete homotypy | Batesian mimicry* | |
Homotypy | Browerian mimicry* | ||
Abstract homotypy | Definable model | ||
Model not definable* | |||
Nondeceitful homotypy | Müllerian mimicry* | ||
Arithmetic mimicry | |||
Deceptive coloration | Behavioral display of colors* | ||
Polymorphism* | |||
Polyphenism | |||
Aposematism* |
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
Table
Camouflage
may be defined as the resemblance of an animal with a part of the
environment [
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., [
Definition: homochromy (imitation of reflected light) which is acting alone. The model is undefined, that is, it is the background.
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 (Figure
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 a
Different
situations of cryptic mimicry in anurans: (a)
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., [
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.
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 genera
The
phyllomedusines of genus
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 some
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.
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 [
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 [
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 [
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 [
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 [
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 (Figure
Recently,
it has been suggested and/or demonstrated that disruptive coloration is
advantageous compared to simple eucrypsis (see [
(a) An
aposematic
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., [
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 (Figures
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 of
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.
The model is definite or an existing species (or cluster of similar species).
The concept of Batesian mimicry [
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 [
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 [
An intriguing situation is the Batesian mimicry
proposed for the
Occurrence of Batesian and Müllerian mimicry in anurans, and distribution overlap between species.
Mimic | Model | Mimetism type | Sympatric species | Source |
---|---|---|---|---|
Aromobatidae | Dendrobatidae | |||
Batesian | Yes | [ | ||
Batesian | Yes | [ | ||
Brachycephalidae | Dendrobatidae | |||
Batesian | Yes | [ | ||
Batesian | Yes | [ | ||
Leptodactylidae | Aromobatidae | |||
Batesian | Yes | [ | ||
Dendrobatidae | Dendrobatidae | |||
Müllerian | Yes | [ | ||
Müllerian | Yes | [ | ||
Müllerian | Yes | [ | ||
Mantellidae | Mantellidae | |||
Müllerian | Yes | [ | ||
Müllerian | Yes | [ | ||
Müllerian | Yes | [ | ||
Dendrobatidae | Dendrobatidae | |||
Müllerian | No | Present study |
**Further studies are needed in this case: see text.
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., [
Indeed, there are reports that show spatial (geographic)
and temporal (seasonal) variation in the alkaloid profiles of poison frogs [
When the model is not an actual species, homotypy is an abstract.
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., [
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 [
This category was created (
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 of
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 [
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 [
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 syntopic
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 [
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 (Figures
Flash
color behavior may serve to disorientate and confuse an attacking predator [
Another
possibility of color display is body raising. For example, in some leiuperids
(e.g.,
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.
Two
morphotypes: for example, some adult individuals of
More
than two morphotypes: several species of cryptic genera
This is
the case of
As
examples, we may cite
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 [
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 of
The
dorsal coloration of
We observed a seasonal
polyphenism in
Seasonal
variation (March 1988 to May 1989) in the dorsal coloration of reproductive
males of
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.
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 [
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 of
Aposematic
coloration is often confined to parts that are usually concealed when the frog
is in its resting posture (e.g., some leiuperids (
In
species of
Several factors are involved in the evolution of
aposematism, such as unpalatability, honest signals, relative predator-prey
abundance-dependence, and kin selection (review in [
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., [
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 [
The
different types of defensive coloration presented in this study may have been
selected differently throughout anuran evolution (see Table
Characteristics, benefits acquired, and constraints involved in the evolution of different classes of anuran coloration.
Coloration classes | Main characteristic | Benefits acquired | Evolutionary constraints involved |
---|---|---|---|
Cryptic coloration | Background matching | Detection avoidance (by prey and predators) | Predator and prey search image |
Aposematic coloration | Background contrasting | Predator avoidance | Predator learning, presence of harmful defenses*, sexual selection |
Reproductive success | |||
Deceptive coloration | Dissuasive coloration | Predator avoidance | Predator search image, sexual selection |
Reproductive success |
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.
Ivan Sazima, Anne D'Heursel, Itamar Martins, Ricardo
Sawaya, Rogério Bastos, and two anonymous referees made valuable comments
during early versions of the manuscript. André Antunes, Cynthia Prado, Daniel
Loebmann, Juliana Zina, José Pombal Jr., Luís Giasson, Olívia Araújo, and
Rodrigo Lingnau helped during field expeditions. Julián Faivovich and Patrícia
Morellato helped with some references. Peter Janzen, Glenn Tattersall, André
Antunes, Ricardo Sawaya, Zoltan Takacs, and Jeet
Sukumaran provided the pictures of