Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio
1 Department of Biological Sciences, University of Maryland Baltimore
County, Baltimore, MD 21250, USA
2 Department of Biomedical Sciences, Cornell University, Ithaca, NY 14853,
USA
3 Vision Touch and Hearing Research Centre, University of Queensland,
Brisbane, Queensland 4072, Australia
4 Department of Biology, East Carolina University, Greenville, NC 27858,
USA
* Author for correspondence (e-mail: cronin{at}umbc.edu)
Accepted 21 April 2004
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Summary |
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Key words: visual ecology, aposematism, poison frog, Dendrobates pumilio, color vision, color signal
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Introduction |
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The species Dendrobates pumilio Schmidt 1858, commonly called the
`strawberry poison frog', offers an excellent case study of how color and,
therefore, aposematic signaling may vary within a single species. D.
pumilio is a toxic species, generally about 1 to 2 cm in size, that
inhabits the forest floor throughout Central America. A group of islands in
Panama's Bocas del Toro Archipelago is populated with these poison frogs (see
Summers et al., 2003). Here,
D. pumilio has evolved to become chromatically distinct between
islands, and single populations of D. pumilio on the adjacent
mainland of Panama may also have striking color variations
(Myers and Daly, 1983
).
Fig. 1 depicts typical D.
pumilio color morphs, all of which have been classified into one species
based on call parameters, toxicity and mitochondrial DNA sequence comparisons
(Summers et al., 1997
).
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Warning coloration in poison frogs seems to be very effective, as predation
is rarely observed. Unlike most frogs, poison frogs are active during the
daytime when predators can easily see them. The toxins that are released from
their skin are some of the most potent animal poisons known, and the bright
daylight environment favors advertisement based on color
(Myers and Daly, 1983). The
polymorphic appearance of D. pumilio is not obviously deleterious to
the species in terms of predation. The divergence is a recent phenomenon.
Today's color morphs have apparently arisen within the last 6000 years, as the
geography of the archipelago has altered with the rise of sea level
(Summers et al., 1997
).
Notably, other monomorphic species of dendrobatid frogs are sympatric with
D. pumilio (Summers et al.,
1997
). D. pumilio's variability is not explained by
Mullerian mimicry, where natural selection should favor convergence of color
and pattern in unpalatable species
(Summers et al., 1997
;
Mallet and Joron, 1999
).
Instead, it is apparently driven by mate selection by females. Unlike other
dendrobatid species, where males and females have equal parental roles,
parental investment in D. pumilio is higher in females, and gives
them a strong role in sexual selection
(Summers et al., 1997
). Female
choice can be an important factor in the divergence of populations. Fisher
theorized that a preference and the preferred trait may coevolve, resulting in
an exaggeration of the trait in a positive-feedback cycle known as the runaway
process (reviewed by Pomiankowski,
1988
).
If mate choice explains D. pumilio color diversity, then signals
are not only important for signaling to potential predators they also
effect communication between conspecifics. Summers et al.
(1999) explored the role of
vision in mate choice in D. pumilio. When individual D.
pumilio females were given a choice between frogs having different color
morphs, they preferentially chose their own type. Under light conditions where
frogs were unable to tell the difference in color between the color morphs,
they expressed no preference. Thus, female D. pumilio use visual cues
to assess possible mates. The relatively lengthy courtship behavior of D.
pumilio potentially gives a female ample opportunity to observe and
examine the coloration and patterning of a possible mate
(Limerick, 1980
).
D. pumilio shares its range with other dendrobatid species;
consequently, species recognition is vital for successful reproduction.
Acoustic signals are species-specific and aid in the recognition of possible
mates and conspecifics, but (as just noted) visual cues are also important in
this task (Summers et al.,
1999). The color signals expressed by D. pumilio should
be discriminable between color morphs by conspecifics. Frogs should also be
detected easily against backgrounds such as foliage or tree bark. This is
important for finding mates and for facilitating social interactions between
conspecifics.
Since D. pumilio colors also serve as aposematic color signals,
potential predators should recognize them as indicators of unpalatability and
move on without an attempted attack. Therefore, the signals should be well
tuned to the vision of predators. The polymorphic character of D.
pumilio motivates the question of how potential predators perceive these
differences in coloration. For instance, are color morphs that are seemingly
cryptic (see examples of green frogs in
Fig. 1) easily discriminated
from backgrounds by visual systems of predators? Here we investigate the
question of how the signals of many D. pumilio color morphs are
perceived and discrimated by conspecifics and by a potential predator. Since
birds are predators on many anurans (Myers
and Daly, 1983; Poulin et al.,
2001
), and avian visual systems are well studied
(Hart, 2001
), we use a typical
passerine bird as a model predator on D. pumilio.
This study thus addresses the effectiveness of color signals used by D. pumilio as perceived both by conspecifics and by a potential predator. The effectiveness is assessed by determining how discriminable colors are to each viewer, quantifying the viewer's ability to discriminate frog colors from each other and from background colors. Our study of the frogs' color signals will help to comprehend the effectiveness of the polymorphic nature of D. pumilio in Panama.
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Materials and methods |
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The selection criteria used for data inclusion into the
max analysis pool were the same as those used by Loew
(1994
). Each acceptable
spectrum was smoothed prior to normalization using a digital filter routine
(`smooft'; Press et al.,
1987
). The smoothed spectrum was overlaid on the unsmoothed one
and checked by eye to make sure that over-filtering or spurious data points
had not shifted the apparent maximum. The peak absorbance used for
normalization prior to template fitting was the calculated maximum of the
best-fit Gaussian to the data points 20 nm either side of the estimated-by-eye
absorbance maximum of the alpha band and is referred to as
Xmax. For those curves meeting the selection criteria, the
max (the wavelength at maximum absorbance for a
template-derived visual pigment best fitting the experimental data) of the
smoothed, normalized (using Xmax) visual pigment
absorbance spectrum was obtained using the method of Mansfield as presented by
MacNichol (1986
). The
templates used were those of Lipetz and Cronin
(1988
). In some cases the data
were not of sufficient quality for template matching, but were usable for
qualitative estimation of
max.
Reflectance measurements
Summers et al. (2003)
measured reflectances in the field in Panama from various D. pumilio
color morphs. Some colors, generally those of small or insignificant body
parts, were not measured in the field or did not produce good quality data. To
include the colors not represented in the data from Panama (invariably black
or dark brown patches), reflectance measurements were taken from similar
patches on dendrobatid frogs at NAIB. Altogether, 47 reflectance spectra were
used, representing 15 color morphs.
To measure background spectra, tropical plants were acquired from the University of Maryland, Baltimore County's greenhouse. These included aglonema (Aglaonema commutatum), bromeliads (including Neoreglia carolinae), rubber plant (Ficus elastica), maranta (Maranta leuconeure), monstera (Monstera deliciosa), and Zebrina pendula (see examples in Fig. 2). Dry leaves, rocks, dirt, sand, sticks, and moss were also collected on campus for measurements of background reflectance.
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Reflectance spectra were taken using an Ocean Optics (Dunedin, FL, USA) S2000 spectrometer, connected to a portable computer. A Labsphere (North Sutton, NH, USA) certified WS-1 Diffuse Reflectance Standard was used as a reference. A WILD Heerbrugg (Leica Microsystems, Wetzlar, Germany) photomicroscope connected to the spectrometer was used to isolate specific locations on the surface of the sample to be measured. A fiber optic light source illuminated samples, providing a measurable spectral range of about 350750 nm. Various areas of plants were measured to ensure that dark, bright, and colored spots were included.
Irradiance spectra
To define lighting conditions where D. pumilio are found, four
irradiance spectra were used (Fig.
3A): standard D55, D65 and D75 irradiance spectra
(Wyszecki and Stiles, 1982),
and a forest shade green light measured in D. pumilio habitat by
Summers et al. (2003
). The
spectrum labeled D65 is the `standard daylight', D55 is illumination dominated
by sunlight, D75 is `north' light dominated by sky, and Green is taken in
shade, under the forest canopy.
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Quantitative model
To analyze the perception of signals, we used the model developed by
Vorobyev et al. (2001), which
assumes that receptor noise limits discrimination (see
Vorobyev and Osorio, 1998
).
Noise in frog photoreceptors was estimated using behavioral data from birds
and humans, as no appropriate measurements exist for amphibians.
Signal-to-noise estimates are used to estimate the visual Weber fractions, the
ratio of intensity between two lights that is just perceived by a visual
system (i.e. at threshold). The Weber fraction estimated in bird
long-wavelength sensitive class (LWS) cone is 0.1
(Vorobyev et al., 1998
),
calculated from behavioral experiments. In frogs, we assume that the Weber
fraction of 0.05 (at threshold) for the LWS mechanism, which is an
intermediate value between the Weber fraction of human LWS cones (0.02;
Wyszecki and Stiles, 1982
) and
birds (0.1; Vorobyev et al.,
1998
). Since absolute values of Weber fractions are not known, we
perform calculations for several values of the signal-to-noise ratio (or the
jnd, see below). Noise decreases with the number of receptors in a given type,
because more individual receptors provide a signal to the system. Thus, the
signal-to-noise ratio (Equation
5) takes into account both the visual Weber fraction
(
i) and the number of cone per type (ni).
The ratios of cones between classes were estimated from MSP preparations,
assuming that the relative encounter rates in these preparations are similar
to the actual proportions of cone types found in the eye. The bird ratios were
refined by accurately matching behavioral spectral sensitivities (see
Maier and Bowmaker, 1993
;
Vorobyev et al., 1998
),
providing ratios of cone types as follows: LWS 4: MWS 2: SWS 2: UVS 1 (MWS,
middle-wavelength-sensitive class; SWS, short-wavelength-sensitive class; UVS,
ultraviolet-sensitive class). Using data from our MSP results, receptor ratios
in D. pumilio were taken as: LWS 4: MWS 3: SWS 1.
The model was run using a program written in Mathematica (Version 4.0,
Wolfram Research). The program requires the photopic sensitivity functions of
the frog (Fig. 3B) and bird
(Fig. 3C,D) visual systems,
using templates fitted to MSP data in D. pumilio and taken directly
from avian templates generously provided by Nathan Hart. It also requires the
selection of one of the irradiance spectra
(Fig. 3A) and of a pair of
reflection spectra measured from frog skin or background. First, we calculate
the quantum catch Qi of each receptor class, denoted by
the subscript i, over the wavelength range 350750 nm, as the integrated
product of the receptor sensitivity spectrum (Ri),
reflectance spectrum (S), and illumination spectrum (I):
![]() | (1) |
Equation 2 accounts for the
adaptation of a receptor to its light environment, using the von Kries
transformation. This assumes that receptors adapt their sensitivities in
proportion to the light they absorb from the illuminant, a property that
contributes to color constancy (Foster and
Nascimento, 1994), thus:
![]() | (2) |
![]() | (3) |
Equation 4 is then applied to
find the contrast between two spectra, as the logarithm of the quotient of
quantum catches from spectrum 1 and spectrum 2. The result of this calculation
is the contrast f for each receptor type i:
![]() | (4) |
For quantum catches that differ only slightly, the contrast is equal to the
relative difference between these catches,
qi/qi, where
qi=qi(spec1)qi(spec2),
because
fi=ln[qi(spec1)/qi(spec2)]=ln(1+
qi/qi(spec2)]=
qi/qi(spec2)
(Vorobyev et al., 2001
). Note
that this relation holds only if the natural logarithms are used.
The contrast, so defined, does not depend on the adaptation of receptors to
their light environment, ki, because
fi depends on the ratio of quantum catches.
Nevertheless, it is convenient to use adapted receptor responses to compare
the quantum catches from different spectral types of cones.
To quantify discrimination using all receptor types in a given
visual system, each receptor class is first assigned a noise value
based on its individual Weber fraction (
) and on the receptor proportion
(n); see also Vorobyev et al.
(2001
):
![]() | (5) |
Then, we calculate discrimination values for trichromatic and
tetrachromatic visual systems. The subscript number of each variable in
Equations 6i,
ii is again the value given for a
particular receptor class (1 to 3 for frogs,
6i; 1 to 4 for birds,
6ii): Trichromat:
![]() | (6i) |
![]() | (6ii) |
Results of calculations using Equations
6i,
ii provide the chromatic distance
(S) separating the perceptual values of two spectra in
receptor space. The units for
S are jnds (just noticeable
differences), where 1 jnd is at the threshold of discrimination, values <1
jnd indicate that the two colors are indistinguishable, and values above 1 jnd
indicate how much above threshold a pair of spectra is discriminated. The
higher the value, the more `distance' in color space there is between the two
spectra and the more distinguishable the two colors are, providing
increasingly rapid discrimination under difficult conditions.
We also performed an achromatic (brightness contrast) analysis similar to
the chromatic analysis, where comparisons are based on brightness differences
alone.
![]() | (7) |
In birds, it is assumed that the double cone class (which contains LWS
pigment; Fig. 3D) is
responsible for achromatic tasks (Maier
and Bowmaker, 1993;
Campenhausen and Kirschfeld,
1998
; Hart et al.,
1998
; Vorobyev et al.,
1998
; Osorio et al.,
1999b
). The double cone's principal member contains an oil droplet
that absorbs at short wavelengths, but does not displace the
max of the visual pigment
(Hart, 2001
). In frogs, the
LWS class is again assumed to be responsible for the achromatic task, based on
evidence from birds, bees and turtles that the LWS receptor is the most
numerous type and is commonly used in achromatic tasks
(Srinivasan, 1985
;
Campenhausen and Kirschfeld,
1998
). As before, the quantum catches and contrasts are calculated
using Equations 1,
2,
3,
4, and the separation in receptor
space of the two spectra is determined using
Equation 7. We estimated the
Weber fraction as 0.05 (at threshold) for the double cone in birds and for the
LWS cone in frogs.
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Results |
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Rod
The average max of all individual rod cells measured in
D. pumilio was 491±2 nm (mean ± S.D.,
N=16). The average spectrum can be seen in
Fig. 4A, together with the
template fit to the curve (
max=491±1 nm (mean
± S.D.). Amphibians typically have two distinct rod types,
`red' rods (with
max near or above 500 nm) and `green' rods
(
max in the mid 400 nm range). Our measurements provided no
evidence for the presence of `green' rods in this species.
SWS cone
The shortest-wavelength-absorbing cone class was found to absorb maximally
at a mean of 466±5 nm (mean ± S.D., N=5).
Measurements were noisier for cones of this class, and template fits had
larger standard deviations than for other receptor types. In individual fits,
max ranged from 457 nm to 471 nm.
Fig. 4B shows the average
absorbance curve of the measured receptors and the best-fit template spectrum
(
max=467±3 nm, mean ± S.D.).
MWS cones
The second type of cone had an average max of
489±8 nm (mean ± S.D., N=14). The average
spectrum and its best template fit, seen in
Fig. 4C, had a
max of 488±1 nm (mean ± S.D.).
LWS cones
This was the most frequently encountered cone type, and it had an average
max of 561±3 nm (mean ± S.D.,
N=14). The average absorbance curve, shown in
Fig. 4D, had its best template
fit with a
max of 563±1 nm (mean ±
S.D.).
Oil droplets
Oil droplets were associated with some cones. The absorbance spectrum of
one such droplet, from an LWS cone, is displayed in
Fig. 4E and shows very low
absorbance from 350 nm to 750 nm. All oil droplets that were observed looked
similar to the one that was measured, and we assume that these droplets have
no significant influence on light absorption by the underlying visual
pigment.
Reflectance spectra
Most reflectance spectra from frogs that were used (a total of 47 spectra)
came from work published by Summers et al.
(2003) and can be seen in the
figures of that paper. Fig. 2
shows some representative spectra (of a total of 15 background spectra) from
several leaf backgrounds against which individuals of D. pumilio
might be viewed by predators or conspecifics.
Frog colors discriminated
Using our model, color signals were quantified pairwise for their contrast
as viewed by conspecifics or by a typical passerine bird. Forty-seven spectra
were compared to each other resulting in 1081 [(47x46)/2] comparisons.
The results are displayed as histograms showing the number of cases occurring
at each jnd (just-noticeable-difference) level (Figs
5,
6,
7,
8,
9). In general, when jnd=1, the
spectral pair is barely discriminable under ideal conditions, and as jnd
becomes greater, discrimination can be made more rapidly and under
increasingly unfavorable viewing conditions.
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Frogs are able to discriminate many frog colors well, but about 27% of color pairs are relatively poorly discriminable, producing values that are <4 jnds (Fig. 5A, Table 1). About 5% of pairs have a value of 0 jnds, and are thus never discriminable by frogs. Birds discriminate frog colors even better: only about 18% of frog color pairs are separated by <4 jnds, and less than 1% have a value of 0 jnds (Fig. 5C, Table 1). Overall, then, it appears that birds discriminate similar frog colors better than frogs, but both appear to discriminate many dissimilar colors equally well.
In an attempt to discover whether the colors within each color morph contrast well, perhaps for pattern displays (see Fig. 1), we compared them pairwise. Results are presented in Table 2 and in Fig. 6A (frog vision) and Fig. 6C (bird vision). Again, results were generally similar among the different light regimes tested. Table 2 contains the extreme values from this analysis and lists the color morphs expressing them (see also Fig. 1). Frogs of most morphotypes have color pairs with very low visual contrast, often just above 0 jnd. The Uyama type generally has the very least internal color contrast between two of its colors, but for bird vision in the green illuminant, the San Cristobal type has the color pair with the lowest value. Both frog and bird vision see the greatest color contrast in the Almirante type. In general, both frogs and birds have similar discrimination abilities within a frog coloration scheme, and all color morphs of frogs contain at least one color pair that is easily discriminated.
Frogs compared to backgrounds
Contrasts of frog colors against backgrounds involved analysis of all 47
frog reflectance spectra against 15 background spectra, yielding 705
(47x15) comparisons. Each test was conducted for both model visual
systems under the four illuminants; results were similar under all lighting
conditions (Table 1).
Analytical results using the green illuminant for frog and bird vision are
displayed in Fig. 5B and
Fig. 5D, respectively. In the
case of the frog visual system, most discrimination values are found at
relatively low jnd values (Fig.
5B). For frogs, about 28% of frog/background comparisons are
discriminable at <4 jnd, and 5% of the pairs are never discriminable
(Table 1). Birds are better
than frogs at this discrimination task, as there are very few comparisons that
give a value less than 1 jnd (<1%) and only about 15% of spectral pairs are
barely discriminable (less than 4 jnd) (Tables
1 and
2). While birds generally
outperform frogs in this discrimination task, the highest discrimination value
(24 jnd) occurred with the frog visual system.
For a frog to contrast well with its background, only one of the colors it displays need be very different from the background spectrum. Thus, we analyzed the visual contrast of colors within each of the 13 color morphs of Fig. 1 in turn to background colors. Such an approach suggests which color morphs are always highly detectable and which may always be difficult to see. The results are seen in Fig. 6B (frog vision) and Fig. 6D (bird vision). Each color morph has at least one color that is discriminable from any background color with a value of at least 8 jnd for frogs and at least 10 jnd for birds. The Shepherd Island type was generally the most difficult to detect against background, while the most detectable was the Solarte type (for frogs) or the Almirante type (for birds, Table 2). Both frogs and birds can discriminate each color morph from any background quite well, but birds are able to discriminate better overall. Interestingly, the most discriminable of the color morphs that were tested differs for the two visual systems.
Many of the non-discriminable frog colors (as viewed by frogs) may be dark colors, present on the body to produce patterns. We therefore compared only the `bright' colors found in the frogs, disregarding `patterning' colors. `Patterning' colors were identified by eye, and included black, brown or other generally dark colors that form stripes or spots and visually break the uniform coloration of the animal. All other colors were classified as `bright' colors and compared both to each other and to backgrounds, pairwise. This analysis reduced the number of spectra compared to 24, resulting in 276 ((24x23)/2) comparisons of frog colors. Results for frog and bird visual systems are tabulated in Table 3 and displayed in Fig. 7A and Fig. 7C, respectively. Comparing Fig. 7A to Fig. 5A, a small shift to the right is observed, but still 4% of colors remain indiscriminable (0 jnd). The number of poorly discriminable spectra (<4 jnd) is reduced to 17%. Therefore, disregarding `patterning' colors and only considering those that are `bright' only slightly increases discriminability, at least to frogs. The bird visual system analysis, Fig. 7C compared to Fig. 5C, also shows a shift to the right when only `bright' colors are analyzed, but still some spectra can hardly be discriminated. About 13% of all spectral pairs are discriminable at <4 jnd, while less than 1% are completely indiscriminable (Table 3). Thus, birds better discriminate `bright' colors compared to `patterning' colors, and birds remain better at discriminating frog colors than are frogs (compare Table 3 to Table 1).
The analysis of `bright' frog colors compared to backgrounds is given in Fig. 7B and Fig. 7D, where the pairing of 24 frog colors with 15 background colors results in 360 comparisons. In frogs, comparing Fig. 7B to Fig. 5B shows that `bright' colors are discriminated better, but many spectral pairs remain indistinguishable; about 19% fall in the 03 jnds range and about 3.5% are not discriminable at all (Table 3). The analysis for bird vision (Fig. 7D compared to Fig. 5D) also shows a slight improvement in discriminability. Birds can discriminate all `bright' spectra from backgrounds, and only about 8% of spectral pairs fall in the 13 jnd range (Table 3).
Dorsal vs. ventral colors
The color signals received by conspecifics and predators may come from
different body regions. Birds normally view frogs from above, so they would
see aposematic signals on the dorsal parts of the frog. However, interactions
among frogs occur mainly at eye level, while facing each other. Therefore,
signals to conspecifics are commonly produced by ventral body parts. For
example, during courtship, males will distend the throat pouch while calling
to females (Wells, 1978;
Limerick, 1980
). D.
pumilio has often been observed on elevated perches
(Graves, 1999
), where the
ventral parts would be particularly prominent. Similarly, territorial
behaviors of males include vocalization, postural changes and fighting
(Donnelly, 1989
), making
ventral body parts potentially influential in malemale interactions as
well. To assess how such signals may differ, dorsal and ventral colors were
separated for analysis, comparing them to background spectra. The results are
plotted in Fig. 8, where dorsal
colors are represented by white bars and ventral colors by dark bars. To both
frog (Fig. 8A) and bird
(Fig. 8B) systems, ventral
colors are more discriminable from backgrounds overall. This may aid frogs in
finding conspecifics in their environment. Birds may not view these ventral
colors very often; nevertheless, for birds the dorsal colors are still quite
discriminable from the background colors
(Fig. 8B).
Achromatic analysis
Discriminations among frogs, or between frogs and backgrounds, may also be
based on brightness (achromatic) cues alone.
Fig. 9A (frog vision) and
Fig. 9C (bird vision) represent
frog colors compared to each other using only achromatic cues. In both frog
and bird vision, many spectral pairs have low discrimination values; about 14%
of the frogfrog pairs are barely discriminable (03 jnd) to frogs
and birds (Table 4). Frog
colors compared to background colors are represented in
Fig. 9B (frog vision) and
Fig. 9D (bird vision). Here,
approximately 12% of the spectra compared are barely discriminable to frogs
and about 15% are barely discriminable to birds
(Table 4). Surprisingly, in
both frog and bird vision fewer spectral pairs generally have jnd values <4
in the achromatic quantification than in the chromatic, with the exception of
birds viewing frogs against backgrounds (both 15%). Some pairs of frog
and background spectra are perceptually very different, with high values
reaching 56 jnds for frog vision and 53 jnds for bird vision. Such high
contrasts may be useful for both frogs and birds, particularly for spotting
D. pumilio frogs against their backgrounds.
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Discussion |
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Like most amphibians (Liebman and
Entine, 1968), poison frogs have three cone classes, but
unusually, they have only one type of rod receptor. Many frogs are active
during twilight and some are nocturnal
(Duellman and Trueb, 1986
), so
having two types of rods may be useful to them. With the exception of one
species in the genus Colostethus, dendrobatid frogs are diurnal
animals (Graves, 1999
).
Therefore, the presence of two rod receptor classes, specialized for use in
scotopic conditions, may have been lost over evolutionary time.
Most poison frogs are active in the early morning and again in the late
afternoon (Poulin et al.,
2001). D. pumilio become active at dawn and peak in
activity early in the morning (07:45 h to 09:15 h); then activity gradually
decreases to midday, after which a moderate level of activity is observed
until dusk (Graves, 1999
).
Avian foraging also peaks in the early morning and late afternoon
(Poulin et al., 2001
). Thus,
while poison frogs are rarely preyed upon by birds, the likelihood of birds
viewing frogs is high.
This study focuses on photopic conditions, when frogs and birds are active
and color vision is utilized. The results from color comparisons indicate that
birds (potential predators) readily discriminate colors within the species
D. pumilio, and are particularly adept at discriminating the frogs
from their backgrounds. While it is important for a potential predator to
recognize an aposematic signal, the ability to differentiate between toxic
frogs has little relevance unless there are differences between frogs, such as
toxin levels, that a predator profits from knowing. Such differences do occur
in D. pumilio (Daly and Myers,
1967), but it is not known whether they affect predation rates.
The use of color signals in D. pumilio seemingly flies in the face of
the theory of Mullerian mimicry, where natural selection favors sharing of
color and pattern in unpalatable species
(Summers et al., 1997
;
Mallet and Joron, 1999
).
Predators often have little time to make the decision of whether or not to
attack a potential prey item once it is seen. Therefore, unpalatable prey
should be as visible as possible to deter incorrect decisions by predators
(Guilford, 1986). The
advantage of increased conspicuousness has been demonstrated with chicks
(Gallus gallus domesticus) feeding on aposematic insect larvae
(Tropidothorax leucopters)
(Gamberale and Tullberg, 1996
).
Naïve chicks attacked larger (presumably more conspicuous) prey less
frequently than the smaller larvae.
The uniquely unusual feature of the various populations of D. pumilio is that the aposematic signals have diverged into a variety of conspicuous signals. In this species, conspicuousness expressed by bright coloration may in itself be enough to ward off predation. If so, the aposematic signal does not arise from a specific color or pattern. Instead, all conspicuous, colored signals would be interpreted by potential predators as warnings. Other poison frog species are diverse in coloration and pattern, although to a much lesser extent than what is observed in D. pumilio, and the poison frogs as an ensemble of species exhibit great diversity. All of these diverse signals are evidently effective, and the frogs are successful throughout the neotropics.
Nevertheless, the basis of the diversity demands explanation. Coloration
can be an important signal in mate selection in birds and fish, where specific
colors enhance success for mating
(Withgott, 2000;
Ryan, 2001
;
Arnold et al., 2002
). As noted
above, D. pumilio females discriminate among potential mates using
visual cues (Summers et al.,
1999
), and it is female choice that best accounts for the
diversity seen in Panama today. Our analytical results suggest that in
general, color morphs should be effectively distinguished by conspecifics, a
factor that may be important in maintaining the identities of the various
populations (Table 5).
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Ventral colors were better discriminated against backgrounds than dorsal
colors, both by conspecifics and predators. These ventral colors may be
particularly important as signals in frog-to-frog interactions. For birds,
normally viewing the frog from overhead, the ventral signals probably play
little role in communication. However, it is interesting to note that the
dorsal colors tend to be far more saturated than ventral shades (see
photographs of Fig. 1).
Reflectance spectra from the dorsal regions almost always have steep changes
in spectral height in a particular spectral region, and tend to have strong
spectral contrast, but those from the ventral regions are often spectrally
flatter (Summers et al.,
2003). Saturation of the color is likely to be an important
component of its signal quality.
Achromatic aspects of colors and patterns are important in spatial vision,
texture, shape and movement detection
(Maier and Bowmaker, 1993;
Hart et al., 1998
; Osorio et
al.,
1999a
,b
).
Our analysis indicates that achromatic aspects of D. pumilio signal
colors permit the differentiation of D. pumilio from backgrounds both
by birds and frogs, even in the absence of color vision. Birds do not
outperform frogs in achromatic discrimination, as only one spectral channel
contributes. On the other hand, the superb chromatic discrimination ability of
birds is probably owed to the extra receptor type found in bird eyes compared
to frog eyes (i.e. tetrachromatic vision vs. trichromatic vision) and
to the narrow sensitivity curves produced by filtering by oil droplets in
birds (Vorobyev et al., 1998
).
Thus, while elevated values of achromatic discrimination aid in the detection
of D. pumilio in its environment, chromatic discrimination remains
important for recognizing signals and color morphs.
This study indicates that the signal colors used throughout the complex of color morphs of Dendrobates pumilio are easily seen and potentially easily recognized, both by conspecifics and by a model predator. Bright, often unsaturated ventral colors seem to be particularly important in frogfrog interactions and may play important roles in female choice, driving the divergence of color morphs between isolated populations. A diversity of saturated dorsal colors effectively signal prey toxicity to avian predators and contrast well to typical forest backgrounds under the typical range of natural illuminants. Aposematic signaling in poison frogs is particularly interesting for its diversity, both within and between species. It appears that predators recognize their toxic prey not through the perception of particular colors, but instead simply because they are brightly colored objects in a world of green and brown.
List of Abbreviations
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Acknowledgments |
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