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First published online March 28, 2008
Journal of Experimental Biology 211, 1203-1210 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.012963
Visual sensitivity to a conspicuous male cue varies by reproductive state in Physalaemus pustulosus females
1 Section of Integrative Biology, University of Texas, Austin, TX 78712,
USA
2 Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Panama
* Author for correspondence (e-mail: mcummings{at}mail.utexas.edu)
Accepted 4 February 2008
 |
Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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Key words: visual sensitivity, reproductive status, visual cue, túngara frog, nocturnal vision, vocal sac
|
INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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;
Martin, 1972;
Gans, 1973;
Dudley and Rand, 1991;
Pauly et al., 2006). Although
diurnal species typically call, mounting evidence shows that many use both
body coloration and vocal sac pulsation to attract mates or repel rivals
(Lüddecke, 1999;
Summers et al., 1999;
Hödl and Amézquita,
2001; Narins et al.,
2003; Hirschmann and
Hödl, 2006). Less expected is that in at least one species of
nocturnal frog, the túngara frog (Physalaemus pustulosus),
vocal sac inflation serves as a dynamic visual cue used by females when
choosing mates (Rosenthal et al.,
2004; Taylor et al.,
2008). There is, however, relatively little understanding of how
visual communication in this frog can take place `in the dark'. Here we
explored the conspicuousness and detectability of this visual cue in a
nocturnal animal that has a well-developed auditory communication system.
Túngara frogs breed during the rainy season in Panama, from about
May to December. Males join in choruses that range in size from a few animals
to over a hundred. These breeding sites can be under the forest canopy or in
open fields. The frogs breed under a range of light intensities. From an
anthropocentric perspective `it is too dark to see your hand in front of your
face is the literal truth in the middle of the jungle on a cloudy night' (p.
166 of Ryan, 1985) while on a
cloudless night with a full moon you could read a newspaper. Jaeger and
Hailman (Jaeger and Hailman,
1981) reported that most activity of túngara frogs on Barro
Colorado Island, Panama, occurred under 0.01 lx
(
1.5x10–9 W cm–2), the lowest
light level they could measure. These frogs are prey for a number of
predators, some of which find them by orienting to the frogs' vocalization
while others seem to rely on visual cues
(Ryan, 1985).
The vocal sac of túngara frogs is a rather conspicuous feature to
the human observer. It differs in color from the surrounding area in being
generally lighter than the rest of the dark-bodied frog. Through buccal
pumping a male túngara frog can force pulmonary air into this
distensible cavity, and this enlarged feature can increase the male's size by
nearly 100% (Savitzky et al.,
1999; Dudley and Rand,
1991). This extension of the vocal cavity clearly serves a
vocalization role – allowing the males to attract females through a
higher calling rate via recycling of air
(Pauly et al., 2006) and thus
reducing the cost of re-inflation (Bucher
et al., 1982), and, as in all frogs, enhancing the coupling of
sound to the environment (Ryan,
1985). Yet the light coloration, coupled with the large size, may
serve as a visual cue for females trying to assess males under night-time
skies. Hence, the objectives of our study were threefold: (1) to characterize
the spectral properties of the putative `vocal sac' visual cue, (2) to
determine whether túngara frogs can detect this cue under nocturnal
light conditions, and (3) to determine whether sensitivity to visual cues
varies by reproductive state or sex.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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)
were collected from the field and measured for spectral reflectance within 6 h
of capture. Head, ventral surface, dorsal surface and non-inflated vocal sac
regions were measured on hand-held, non-anesthetized frogs with an Ocean
Optics S2000 spectrometer and reflectance probe (Ocean Optics R400-7 UV/VIS,
Dunedin, FL, USA) with an Analytical Instrument Systems
deuterium–halogen light source (AIS model DT 1000, Flemington, NJ, USA).
Directly following these measurements, males were killed by an overdose of
MS222 for spectral reflectance measurements of inflated vocal sacs. The nares
and mouth were sealed with Krazy Glue (Columbus, OH, USA), and a syringe was
inserted into the posterior of the vocal sac; air was blown into the frog
until the vocal sac was fully inflated (no wrinkles present). Four to six
spots were measured per region (head, dorsum, ventrum, non-inflated vocal sac
and inflated vocal sac) and each spot was measured at least 3 times
(N=12–18 reflectance spectra collected per body region per
male). Background substrate (mud, stone, dead leaves), where male frogs were
collected, was also brought back to the lab for immediate reflectance
measurements.
The visual system operates by color-blind rod photoreceptors at night, and
consequently visual targets are assessed in terms of lightness and darkness
rather than color, which in daylight would be processed by comparing the
output of different cone photoreceptors. The conspicuousness of nocturnal
visual signals is therefore a function of how much light a target can produce
relative to background, as opposed to the specific color contrast. To assess
the conspicuousness of a given body part of a túngara frog, we
calculated the total reflectance flux for each region:
 | (1) |
Nocturnal irradiance measurements were collected in Gamboa, Panama, in different areas along the edge of a secondary forest with túngara frogs present, using an International Light (Peabody, MA, USA) IL1700 Research Radiometer and calibrated PM271C photomultiplier detector with a 200–675 nm sensitivity range. Measurements were made by pointing the photomultiplier detector directly up in the sky (90° zenith angle) and towards background vegetation (horizontal to Earth's surface, 0° zenith angle) in June 2007 near midnight on three evenings: June 13th (00:06 h, light overcast sky, 1 day from new moon), June 23rd (23:02 h, light overcast sky, 1 day greater than quarter moon) and June 28th (22:00 h, light overcast sky, 2 days prior to full moon; Table 1).
|
Optomotor device
An optomotor device estimates visual sensitivity by measuring the
optokinetic response of an animal, and this response is exhibited by a wide
range of taxa, from fish (Lyon,
1904; Schaerer and Neumeyer,
1996), to insects (Hassenstein
and Reichardt, 1956; McCann
and MacGinitie, 1965), to frogs
(Cronly-Dillon and Muntz,
1965). The optokinetic response is eye orientation followed by
head and body movements coincident with vertical features in a moving
environment. An optomotor device usually involves a rotatable striped drum
with an interior stationary chamber that houses the focal animal and a means
to monitor the animal's movement with the movement of the stripes. The
intensity of the illuminating light can be modified to determine threshold
sensitivity levels (the minimal intensity at which the animal follows the
movement of the drum).
Typical optomotor devices incorporate a black and white striped drum that
is monochromatically illuminated to test sensitivity functions across a span
of wavelengths (e.g. Maan et al.,
2006). Our question, however, was at what light intensities can
túngara frogs see the inflated vocal sac? Thus we replaced the white
stripes with a color that matched the reflectance spectrum of the inflated
vocal sac. To do so, we placed a combination of spectral filters (Lee 185, Lee
Filters, Burbank, CA, USA; GamColor 305, GamColor 1516 Gamproducts Inc., Los
Angeles, CA, USA) above a white background for the `vocal sac' colored
stripes, and used electrical tape for the black stripes. All stripes were 2 cm
in width. Fig. 1B shows the
approximate matching between the reflectance of a male's inflated vocal sac
and that of the `vocal sac' drum stripe. Instead of using monochromatic light,
we employed a light source with a spectrum mimicking that of moonlight (see
Fig. 1B). Reflectance
measurements of both of the optomotor stripes (black tape and the combination
of spectral filters) were made to calculate the contrast of the visual task.
The Michelson contrast
(Imax–Imin)/(Imax+Imin),
where I is the estimated radiant flux, between the black
(Imin) and `vocal sac colored' (Imax)
stripes is 0.74. This level of contrast is of the same order estimated between
inflated vocal sac and different natural backgrounds (from
Fig. 2; contrast of vocal sac
to stone, 0.73; to mud, 0.59; and to dead leaves, 0.67).
|
|
1 cm at the edge of the cylinder) for each movement the frog
made during the 2 min trials.
Frog selection
From July 2003 to November 2004, 25 male and 40 female túngara frogs
were selected from our colony population (in Austin, TX, USA) to be tested for
visual sensitivity. Prior to testing, all individuals were measured
(snout-to-vent length, SVL) and their reproductive state recorded. All males
were of unknown reproductive readiness, although none had recently mated.
Females were classified into two categories: reproductive (having oviposited
within 48 h preceding test) or non-reproductive (no oviposition within 5 days
of testing). After an initial optomotor test, females were isolated in
containers or small colony tanks to monitor reproductive state. They were then
retested in the alternative state. If females were first tested in a
non-reproductive state, they were then placed in a chamber with a male and
monitored daily for reproductive activity. Most females that were initially
tested while reproductive were then retested 2 weeks later for their
non-reproductive state measurement.
|
). Females were injected with HCG and then placed with a
male for 24 h; if a female oviposited she was tested in the optomotor chamber
within 24 h of injection.
Optomotor procedure
Frogs were dark adapted for 60 min and then placed in a moistened optomotor
inner chamber and allowed to acclimate for 5 min. After acclimation, a trial
began by rotating the outer striped drum for 2 min at 3.3 r.p.m. in either the
clockwise or counterclockwise direction while the frog's movements relative to
the motion of the drum were monitored with an infrared video system. Angular
movement of the frog was characterized by placing a transparency with 360°
marked in 5° degree partitions above the inner chamber image on the
monitor. Observers recorded the angle of the frog's initial position and then
cataloged the direction (clockwise or counterclockwise) and the ultimate
position (in degrees) for each movement the frog made during the 2 min
observation period. Full 360° revolutions and jumping behavior were also
noted. After 2 min, the drum rotation was reversed and frog movements and
orientations were quantified for the opposite direction. After the frog
completed a 2 min observation period in each direction, the light intensity
level was increased to the next level and the frog was given another 5 min
acclimation time before the testing process was repeated. All frogs were
initially exposed to the lowest light intensity level
(1.16x10–13 W cm–2) and subsequently
tested with incremental increases in light intensity (level 1, 2, 3, etc.) and
all frogs were exposed to all six light levels. The sequence of tests was not
randomized, which was necessary to maintain dark adaptation.
A pilot study was conducted to determine whether movements in the optomotor
drum were random, by including a control trial prior to each optomotor trial.
A control trial involved observing the total movements of the frog for 2 min
with no motion of the drum. Comparison between control trials and optomotor
trials indicated that movement in the optomotor trial was significantly
greater than movement in the control trial (mean ± s.e.m. total degrees
moved in 2 min for control, 72.5±11.9°; total degrees moved in 2
min optomotor trial period, 210.0±15.3°; d.f.=225, paired
t=7.88, P=1.4x10–13); with 38% of the
control trials exhibiting no movements over the 2 min observation period.
Given the great variation in response across individuals, we employed a
criterion response similar to that employed with other highly mobile taxa,
e.g. zebrafish (Krauss and Neumeyer,
2003). A positive optomotor response was scored only if two
criteria were met: (1) the frog showed a net positive movement in both 2 min
trials in the same direction as the drum rotation, and (2) the proportion of
all movements made by each frog in the 4 min observation (distance in angles
where 5°1 cm at the outer edge of the optomotor cylinder) was >65%
in the direction of the drum's rotation. This latter criterion was more
stringent than some other studies that evaluated all movements of a subject
during optomotor trials [e.g. 60% of all movement in the drum's direction
(Krauss and Neumeyer, 2003)].
If an animal did not meet both criteria in any of the six light-intensity
levels, they were not used in further analyses. An individual frog's threshold
response was defined as the lowest trial setting in which a positive optomotor
response was recorded. Each individual's `threshold response' was used for all
statistical analyses.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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Optomotor responses
Eighty-seven trials using vocal sac-specific optomotor stimuli (see
Fig. 1) were conducted with 25
males and 40 females including numerous repeated measurements from the same
individual in different reproductive states. Of the initial 65 individuals,
only 23 males and 33 females that showed a complete optomotor response (i.e.
met the criteria for an optomotor response in one of the six intensity levels)
were included in further analyses. Optomotor responses were quite strong among
individuals, with movement in the direction of the rotating drum significantly
greater than movements in the opposite direction [Student's paired
t-test, mean ± s.e.m. distance (in degrees) moved with the
direction of the rotating drum, 204.4±21.5°; mean degrees moved
against the direction of the rotating drum, 24.0±7.2°;
t=9.49, d.f.=54, P=4.1x10–13]. The
mean ± s.e.m. per cent movement with the optomotor rotation was
93±2.5% of all movements across the 4 min observation period.
Of the 33 female túngara frogs, only 14 were tested successfully in both the reproductive and non-reproductive state. Of these 14 repeat females, eight were initially tested in the reproductive state and six were initially tested in the non-reproductive state. Mean optomotor threshold responses between reproductive and non-reproductive state among females were different (mean ± s.e.m. reproductive female threshold response, 1.86±0.23; mean non-reproductive female threshold response, 2.64±0.40); however, there was a significant order effect (ANOVA model on 14 repeat females with threshold response as the dependent variable, reproductive state as a factor, and trial order as covariate: reproductive state F=2.214, P=0.149; trial order F=7.17, P=0.013). Females showed greater sensitivity (lower threshold response) in their first optomotor test than in their second (Fig. 3; mean ± s.e.m. first optomotor threshold response, 1.64±0.17; mean second optomotor threshold response, 2.86±0.39; Wilcoxon signed-rank test, z=2.579, P=0.01).
|
Given the significant order effect, we compared only the initial testing
trial between females first tested in the reproductive state (N=12)
and those first tested in the non-reproductive state (N=20). The
majority of the 12 reproductive females were tested within 24 h of laying foam
nests (five tested on the same day as laying a foam nest; four on the next
day; two on the second day, and one on the third day). We observed a
significant difference in optomotor threshold response between females in the
reproductive and non-reproductive states (mean ± s.e.m. reproductive
state optomotor threshold response, 2.25±0.35; median, 2; mean
non-reproductive state optomotor threshold response, 3.6±0.28; median,
4; Kruskal–Wallis, U=51, 
2=7.535,
P=0.006). Comparing responses between equivalent sample sizes yielded
an even stronger difference (first 12 non-reproductive females' mean optomotor
threshold response, 3.92±0.35).
Three of the 12 reproductive females had been injected with HCG to induce oviposition. Whether females oviposited naturally or with a 100–500 i.u. injection of HCG did not significantly affect their visual sensitivity (mean ± s.e.m. optomotor threshold for natural egg-laying females, 2.33±0.44; for HCG-injected females, 2.0±0.58; Kruskal–Wallis, U=15, P=0.77). Given the lack of significant differences between HCG and naturally ovipositing females, we pooled all reproductive females for comparison across groups (non-reproductive females and males). Reproductive females showed the greatest visual sensitivity across all three groups (Fig. 4; Kruskal–Wallis test, 10.74, P=0.005) and post hoc comparisons showed that the only significant difference was between non-reproductive and reproductive females (Tukey HSD probabilities: male versus non-reproductive females, P=0.43; male versus reproductive females, P=0.19; reproductive versus non-reproductive females, P=0.02).
Comparing visual sensitivities to nocturnal irradiance measurements, all three groups exhibited visual sensitivities at intensities that were below the near new moon vertical measurement as well as quarter moon horizontal measurements (Table 1). This result suggests that all groups have visual thresholds allowing detection of the inflated vocal sac under nearly all nocturnal sky conditions in an open environment.
Size differences
Body size was also a significant covariate in accounting for variation in
optomotor responses among individuals [ANOVA model on all tested individuals
(N=53) with threshold response as the dependent variable, group ID
(N=3, male, reproductive female or non-reproductive female) as a
factor, and body size (SVL) as covariate: group ID F=8.011,
P=0.001; body size F=4.5, P=0.039]. Across all
groups, body size did not explain a significant amount of the variation in
optomotor response [Fig. 5A,
r2=0.009, N=53 (note two individuals were not
measured), t=0.665; P=0.509]. Within each group, however,
the relationship between size and response varied. Both males and reproductive
females showed no significant relationship between SVL and visual sensitivity
(males r2=0.105, t=1.53, P=0.14;
reproductive females r2=0.035, t=0.573,
P=0.58), whereas non-reproductive females showed a significant
relationship between size and optomotor threshold response (non-reproductive
females r2=0.212, t=2.2, P=0.04), with
larger females showing a decrease in visual sensitivity. Importantly,
reproductive females were slightly larger than non-reproductive females (mean
± s.e.m. SVL of reproductive females, 29.5±0.62 mm,
N=12; non-reproductive females, 27.3±0.63 mm, N=20;
t=2.25, P=0.03). Thus, differences in visual sensitivity due
to size alone would suggest that the reproductive group of females should have
lower visual sensitivity (higher optomotor thresholds). Of note, the initial
12 females tested in each condition showed no difference in mean size (mean
± s.e.m. SVL of reproductive females, 29.5±0.62 mm; first 12
non-reproductive females, 29.2±0.46 mm; t=0.437,
P=0.67). Mean male SVL was 28.4±0.28 mm, which was not
significantly larger than that of the non-reproductive females
(t=1.64, P=0.11) nor smaller than that of the reproductive
females (t=1.82, P=0.08).
|
Seasonal differences
Overall, there was no significant relationship between season (month of
testing) and optomotor threshold response (r2=0.019,
N=55, t=1.012; P=0.316;
Fig. 5B). There was also no
significant relationship between threshold response and month with either
males or reproductive females (reproductive females:
r2=0.111, N=12, t=1.117,
P=0.29; males: r2<0.001, N=23,
t=0.064, P=0.95). There was, however, a significant
relationship between optomotor threshold and season within the
non-reproductive females (r2=0.286, N=20,
t=2.687, P=0.015), with non-reproductive females showing the
greatest sensitivity in the early spring months (February–April).
|
DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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;
Taylor et al., 2008) can also
function in the wild.
We suggest that the vocal sac initially evolved under selection for
acoustic function and has been co-opted in túngara frogs, and probably
many other frogs, as a visual cue. Although this was known in diurnal frogs
(Lüddecke, 1999;
Summers et al., 1999;
Hödl and Amézquita,
2001; Narins et al.,
2003; Hirschmann and
Hödl, 2006), we have now shown it is true in at least one
nocturnal species. There are other instances in which dynamic structures
associated with acoustic signaling serve as additional cues for communication.
One example is the McGurk effect (McGurk
and McDonald, 1976), in which the movements of the lips associated
with speech contribute to speech recognition in humans. A challenge in any
form of communication is to produce signals that can be distinguished from
background noise (Maynard Smith and
Harper, 2003; Ryan and
Cummings, 2005). Thus it comes as no surprise that such a
conspicuous and dynamic structure as the frog's vocal sac, which is so
intricately associated with vocalization, would come to serve a communication
function. We refer to the vocal sac in this context as a visual cue rather
than a visual signal since it is an aspect of the phenotype that provides
information to the receiver but did not evolve under selection for signaling
(e.g. Hauser, 1996). We do
suggest, however, that the colors and patterns that sometimes adorn vocal sacs
probably have, in many circumstances, evolved for a communication function and
thus might be considered visual signals rather than visual cues. The striking
variation in vocal sacs among frogs offers a rich, untapped resource for
studies of visual and multimodal communication.
We also suggest that the particular coloration of the inflated vocal sacs
of túngara frogs appears to have been selected for detectability by
frog viewers. When the vocal sac of male túngara frogs is inflated it
has higher reflectance, and therefore is likely to be more conspicuous,
against the dark background than any other body region measured
(Fig. 2). This increase in
reflected light is predominantly in the middle wavelength region
(450–550 nm), which corresponds to the visual sensitivity of most anuran
rods (reported 
max values, 498–529 nm)
(Liebman and Entine, 1968;
Hárosi, 1975;
Donner et al., 1990;
Fyhrquist et al., 1998;
Palma et al., 2001), and
consequently the increase in reflected light is likely to be detectable by
conspecifics.
Dimorphic response
We found that reproductive females exhibited a visual response at lower
light intensities than did males or non-reproductive females
(Fig. 4). Reproductive females,
on average, exhibited a 1 log unit increase in sensitivity over
non-reproductive females, and a 0.5 log unit increase in sensitivity over
males. If the vocal sac is a component of the male calling signal, it is
relevant that reproductive females showed a mean response to the vocal sac
coloration under the darkest of night sky conditions. Rand et al.
(Rand et al., 1997) showed
that female mate choice behavior is affected by light intensity, with
significantly more female túngara frogs exhibiting phonotaxis toward
male calls under darker light conditions (mimicking moonless nights). Their
interpretation was that females are more likely to make mate choice decisions
when there is a lower risk of predation from visually orienting predators,
which are quite common (Ryan,
1985). We have found that females are capable of seeing a male
vocal sac under these conditions where mate choice seems to be most
common.
While reproductive females exhibited the greatest visual sensitivity of all
three groups studied, there was no significant difference in visual
sensitivity between non-reproductive females and males
(Fig. 4). If the inflated vocal
sac serves as a function in antagonistic interactions as it does in the
diurnal frogs with conspicuous vocal sacs, such as Phrynobatrachus
krefftii (Hirschmann and Hödl,
2006) or Epipedobates femoralis
(Narins et al., 2003), then we
would expect both males and females interested in mating to exhibit abilities
to detect this cue under relevant conditions. Males, however, usually remain
in the same place while calling, whereas females are coming to the breeding
site to find a mate. It is possible that the vocal sac acts as a long-distance
beacon to females for mate localization, a function that might be less
important to males.
Our results suggest that the inflated vocal sac would be detected by all
females and males on most, if not all, nights in a month. It is also worth
mentioning that this vocal sac could possibly be detected in even darker
environments (deep canopied forests) given that the inflated vocal sac can
expand beyond the 2 cm width tested in our optomotor device
(Dudley and Rand, 1991). Since
scotopic (rod-based) vision operates by spatially pooling photoreceptor
signals, a larger, reflective object such as an inflated vocal sac is more
likely to be seen than a smaller object of equal reflectivity.
Reproductive state and sensitivity
Perhaps the most intriguing result of our optomotor experiment is that
visual sensitivity differed significantly by reproductive state among females.
This is interesting as neuroendocrinology studies in túngara frogs have
shown that two female reproductive behavior decisions, discrimination
(preference for one stimulus over another) and permissiveness (tolerance for
unattractive signals), vary with reproductive cycle. Lynch and Wilczynski
(Lynch and Wilczynski, 2005)
showed that reproductive hormones varied across three reproductive states in
female túngara frogs. Plasma concentrations of estrogen and
progesterone in unamplexed and post-mated (non-reproductive) females were
significantly lower than in amplexed (reproductive) females. Their study
showed significant changes in the levels of plasma gonadal steroids despite
the túngara frogs showing asynchronous oogenesis (constant production
of oocytes), suggesting that the hormonal increase has roles beyond gamete
production. Lynch and colleagues have also shown that female choice behavior
varies across these same reproductive states with female túngaras
showing the maximal receptivity and permissiveness during the amplexed stage
or when estrogen levels are increased
(Lynch et al., 2005;
Lynch et al., 2006). Taken
together, their studies suggest that surges in estrogen and progesterone
change reproductive behavior in female túngara frogs.
Our findings, though only correlational, suggest that the surge in
reproductive hormones may be having physiological effects on the sensory
system that may contribute to surges in specific reproductive behaviors. A
similar result was found in sticklebacks whereby optomotor tests of visual
sensitivity showed that female sticklebacks were more sensitive to red
wavelengths than were males during the reproductive season; yet there was no
sexual dimorphism in visual sensitivity outside of the breeding season
(Cronly-Dillon and Sharma,
1968). The similarity between our results and those of the
stickleback study is that red wavelengths correspond to the nuptial coloration
that male sticklebacks use to attract females during the breeding season. More
recent work on estrogens and the human retina suggests that steroid hormones
increase the transmission speed in the optical pathway by augmenting the
effect of glutamate and dopamine (Drouva et
al., 1988), and are argued to be responsible for the shorter
latency values and higher amplitudes of evoked potentials in women
(Celesia et al., 1987;
Yilmaz et al., 1998;
Yilmaz et al., 2000).
Steroid hormones have recently been shown to play a role in sensory tuning
of the auditory system. Estrogen- or testosterone-treated midshipman
(Porichthys notatus) females become more precisely tuned to the
temporal cues of the male courtship song than control females
(Sisneros et al., 2004a).
Similar to túngara frogs and other vertebrates, the onset of
reproductive behavior is associated with circulating levels of both estrogen
and testosterone (Sisneros et al.,
2004b). This group identified an estrogen receptor
(ER
) in the midshipman's saccular epithelium that is
suspected to directly control the action of steroids on the sensory neurons.
In humans, estrogen fluctuations during the menstrual cycle influence evoked
neural responses to sound (Elkind-Hirsch
et al., 1992). Estrogen receptors have been found in the inner ear
of mammals as well (Stenberg et al.,
1999) and are suspected to influence hearing. There have been few
investigations of hormonal effects on the auditory system in frogs, but it
seems that overall auditory sensitivity is increased, but not frequency
shifted, in the breeding season (Yovanof
and Feng, 1983; Penna et al.,
1992).
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CONCLUSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONReferences |
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Bucher, T. L., Ryan, M. J. and Bartholomew, G. W. (1982). Oxygen consumption during resting, calling and nest building in the frog Physalaemus pustulosus. Physiol. Zool. 55,10 -22.
Cannatella, D. C. and Duellman, W. E. (1984). Leptodactylid frogs of the Phyasalaemus pustulosus group. Copeia 1984,902 -921.[CrossRef]
Celesia, G. G., Kaufman, D. and Cone, S. (1987). Effects of age and sex on pattern electroretino grams and visual evoked potentials. Electroencephalogr. Clin. Neurophysiol. 68,161 -171.[CrossRef][Medline]
Cronly-Dillon, J. R. and Muntz, W. R. A.
(1965). The spectral sensitivity of the goldfish and the clawed
toad tadole under photopic conditions. J. Exp. Biol.
42,481
-492.
Cronly-Dillon, J. and Sharma, S. C. (1968).
Effect of season and sex on the photopic spectral sensitivity of the
three-spined stickleback. J. Exp. Biol.
49,679
-687.
de Jongh, H. J. and Gans, C. (1969). On the mechanisms of respiration in the bullfrog, Rana catesbeiana: a reassessment. J. Morphol. 127,259 -290.[CrossRef]
Donner, K., Firsov, M. L. and Govardovskii, V. I.
(1990). The frequency of isomerization-like `dark' events in
rhodopsin an porphyropsin rods of the bullfrog retina. J.
Physiol. 428,673
-692.
Drouva, S. V., Rerat, E., Bihoreau, C., Laplante, E.,
Rasolonjanahary, E., Clauser, H. and Kordon, C. (1988).
Dihydropyridine sensitive calcium channel activity related to prolactin,
growth hormone and luteinising hormone release from anterior pituitary cells
in culture: interactions with somatostatin, dopamine and estrogens.
Endocrinology 123,2762
-2773.
Dudley, R. and Rand, A. S. (1991). Sound production and vocal sac inflation in the tungara frog, Physalaemus pustulosus (Leptodactylidae). Copeia 1991,460 -470.[CrossRef]
Elkind-Hirsch, K. E., Stoner, W. R., Stach, B. A. and Jerger, J. F. (1992). Estrogen influences auditory brainstem responses during the normal menstrual cycle. Hear. Res. 60,143 -148.[CrossRef][Medline]
Fyhrquist, N. F., Govardovskii, V. I., Leibrock, C. and Reuter, T. (1998). Rod pigment and rod noise in the European toad Bufo bufo. Vis. Res. 38,483 -486.[CrossRef][Medline]
Gans, C. (1973). Sound production in the Salientia: mechanism and evolution of the emitter. Am. Zool. 13,1179 -1194.
Hárosi, F. I. (1975). Absorption spectra
and linear dichroism of some amphibian photoreceptors. J. Gen.
Physiol. 66,357
-382.
Hassenstein, B. and Reichardt, W. (1956). Systemtheroretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswetung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus.Zeit. Naturforsch. B 11,513 -524.
Hauser, M. D. (1996). The Evolution of Communication. Cambridge, MA: MIT Press.
Hirschmann, W. and Hödl, W. (2006). Visual signaling in Phrynobatrachus krefftii Boulenger, 1909 (Anura: Ranidae). Herpetologica 62, 18-27.[CrossRef]
Hödl, W. and Amézquita, A. (2001). Visual signaling in anuran amphibians. In Anuran Communication (ed. M. J. Ryan), pp.121 -141. Washington, DC: Smithsonian Institution.
Jaeger, R. C. and Hailman, J. P. (1981). Activity of Neotropical frogs in relation to ambient light. Biotropica 13,59 -65.
Krauss, A. and Neumeyer, C. (2003). Wavelength dependence of the optomotor response in zebrafish (Danio rerio). Vis. Res. 43,1273 -1282.[Medline]
Liebman, P. A. and Entine, G. (1968). Visual pigments of frog and tadpole (Rana pipiens). Vis. Res. 8,761 -775.[CrossRef][Medline]
Lüddecke, H. (1999). Behavioral aspects of the reproductive biology of the Andean frog Colostethus palmatus (Amphibia: Dendrobatidae). Rev. Acad. Colomb. Cienc. Exact. Fís. Nat. 23 (Suplemento Especial), 303-316.
Lynch, K. S. and Wilczynski, W. (2005). Gonadal steroids vary with reproductive stage in a tropically breeding female anuran. Gen. Comp. Endocrinol. 143, 51-56.[CrossRef][Medline]
Lynch, K. S., Rand, A. S., Ryan, M. J. and Wilczynski, W. (2005). Plasticity in female mate choice associated with changing reproductive states. Anim. Behav. 69,689 -699.[CrossRef]
Lynch, K. S., Crews, D., Ryan, M. J. and Wilczynski, W. (2006). Hormonal state influences aspects of female mate choice in the Túngara Frog (Physalaemus pustulosus). Horm. Behav. 49,450 -457.[CrossRef][Medline]
Lyon, E. P. (1904). On rheotropism. I. Rheotropism in fishes. Am. J. Phys. 12,149 -161.
Maan, M. E., Hofker, K. D., van Alphen, J. J. M. and Seehausen, O. (2006). Sensory drive in cichlid speciation. Am. Nat. 167,947 -954.[CrossRef]
Martin, W. R. (1972). Evolution of vocalization in the genus Bufo. In Evolution in the Genus Bufo (ed. W. F. Blair), pp. 279-308. Austin: University of Texas Press.
McCann, G. D. and MacGinitie, G. F. (1965). Optomotor response studies of insect vision. Proc. R. Soc. Lond. B Biol. Sci. 163,369 -401.[Medline]
McFarland, W. N. (1991). The visual world of coral reef fishes. In The Ecology of Fishes on Coral Reefs (ed. P. F. Sale), pp. 16-38. San Diego: Academic Press.
McGurk, H. and McDonald, J. (1976). Hearing lips and seeing voices. Nature 264,746 -748.[CrossRef][Medline]
Maynard Smith, J. and Harper, D. (2003). Animal Signals. Oxford: Oxford University Press.
Narins, P. M., Hödl, W. and Grabul, D. S.
(2003). Bimodal signal requisite for agonistic behavior in a
dart-poison frog. Proc. Natl. Acad. Sci. USA
100,577
-580.
Palma, F., Roncagliolo, P., Bacigalupo, J. and Palacios, A. G. (2001). Membrane current of retinal rods of Caudiverbera caudiverbera (Amphibia: Leptodactylidae): dark noise, spectral and absolute light sensitivity. Vis. Neurosci. 18,663 -673.[CrossRef][Medline]
Pauly, G., Bernal, X. E., Rand, A. and Ryan, M. J. (2006). The vocal sac increases call rate in the túngara frog Physalaemus pustulosus. Physiol. Biochem. Zool. 79,708 -719.[CrossRef][Medline]
Penna, M., Capranica, R. R. and Somers, J. (1992). Hormone-induced vocal behavior and midbrain auditory sensitivity in the green treefrog, Hyla cinerea. J. Comp. Physiol. A 170,73 -82.[Medline]
Rand, A. S., Bridarolli, M. E., Dries, L. and Ryan, M. J. (1997). Light levels influence female choice in tungara frogs: predation risk assessment? Copeia 1997,447 -450.[CrossRef]
Rosenthal, G. G., Rand, A. S. and Ryan, M. J. (2004). The vocal sac as a visual cue in anuran communication: an experimental analysis using video playback. Anim. Behav. 68,55 -58.[CrossRef]
Ryan, M. J. (1985). Energetic efficiency of
vocalization by the frog Physalaemus pustulosus. J. Exp.
Biol. 116,47
-52.
Ryan, M. J. and Cummings, M. E. (2005). Animal signals and the overlooked costs of efficacy. Evolution 59,1160 -1161.
Savitzky, A. H., Roberts, K. A. and Rand, A. S. (1999). Organization of elastic fibers in the vocal sacs of frogs. Am. Zool. 39,98A .
Schaerer, S. and Neumeyer, C. (1996). Motion detection in goldfish investigated with the optomotor response is "color blind". Vis. Res. 36,4025 -4034.[CrossRef][Medline]
Sisneros, J. A., Forlano, P. M., Deitcher, D. L. and Bass, A.
H. (2004a). Steroid-dependent auditory plasticity leads to
adaptive coupling of sender and receiver. Science
305,404
-407.
Sisneros, J. A., Forlano, P. M., Knapp, R. and Bass, A. H. (2004b). Seasonal variation of steroid hormone levels in an intertidal-nesting fish, the vocal plainfin midshipman. Gen. Comp. Endocrinol. 136,101 -116.[CrossRef][Medline]
Stenberg, A. E., Wang, H., Sahlin, L. and Hultcrantz, M.
(1999). Mapping of estrogen receptors and β in the
inner ear of the mouse and rat. Hear. Res.
136, 29-34.[CrossRef][Medline]
Summers, K., Symula, R., Clough, M. and Cronin, T. (1999). Visual mate choice in poison frogs. Proc. Roy. Soc. Lond. B 266,2141 -2145.[Medline]
Taylor, R. C., Klein, G., Stein, J. and Ryan, M. J. (2008). Multicomponent cue assessment in the túngara frog: a test using a robotic frog. Anim. Behav. In press.
Yilmaz, H., Erkin, E. E., Mavioglu, H. and Sungurtekin, U. (1998). Changes in pattern reversal evoked potentials during menstrual cycle. Int. Ophthalmol. 22, 27-30.[CrossRef][Medline]
Yilmaz, H., Erkin, E. E., Mavioglu, H. and Laçin, S. (2000). Effects of estrogen replacement therapy on pattern reversal visual evoked potentials. Eur. J. Neurol. 7, 217-221.[CrossRef][Medline]
Yovanof, S. and Feng, A. S. (1983). Effects of estradiol on auditory evoked responses from the frog's midbrain. Neurosci. Lett. 36,291 -297.[CrossRef][Medline]
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), ventral (
), non-inflated
vocal sac (•) and inflated vocal sac (
). Average background material
spectral reflectance is also shown (broken lines) including mud (•),
stone (
) and dead leaves (
). (B) Average spectral reflectance of
the vocal sac of a representative male túngara frog in non-inflated
(•) and inflated (
