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First published online February 29, 2008
Journal of Experimental Biology 211, 1012-1020 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.014795
Sex differences in energetic costs explain sexual dimorphism in the circadian rhythm modulation of the electrocommunication signal of the gymnotiform fish Brachyhypopomus pinnicaudatus
Department of Biological Sciences, Florida International University, University Park, Miami, FL 33199, USA
* Author for correspondence (e-mail: vsalaz01{at}fiu.edu)
Accepted 12 January 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: gymnotiform, sexual dimorphism, circadian rhythm, electric fish, electric organ discharge, energetic cost, communication signal
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Endler, 1978;
Endler, 1980;
Endler, 1983;
Frischknecht, 1993;
Houde, 1988;
Kodric-Brown, 1993;
Moodie, 1972;
Pomiankowski, 1987;
Prestwich, 1994;
Ryan, 1988;
Ryan et al., 1982;
Searcy and Andersson, 1986).
Electrocommunication signals, such as those displayed by weakly electric fish,
likewise may have evolved in response to a similar suite of opposing selective
pressures. Growing evidence suggests that hostile eavesdropping by predators
has driven the evolution of electric signals
(Hanika and Kramer, 1999;
Hanika and Kramer, 2000;
Reid, 1983;
Stoddard, 1999) while
exaggeration of male-typical electric signal traits may enhance reproductive
opportunities (Curtis and Stoddard,
2003). Less well understood, however, is whether and how the
energetic cost of electrogenesis has influenced the evolution and regulation
of electric fish signals.
To date, no study has measured the energetic cost of electrogenesis
relative to a fish's total energy budget and natural behaviors. Indeed, the
few studies to address the cost of electric signals either have suggested that
the costs are negligible (Hopkins,
1999; Julian et al.,
2003) or have focused on estimating absolute costs of
bioelectrogenesis with no reference to the overall energy budget
(Aubert et al., 1961;
Aubert and Keynes, 1968;
Bell et al., 1976;
Keynes, 1968). We undertook
the first direct measurement of the energetic cost of electric signal
production in weakly electric fish and examined this cost with respect to the
overall energy budget and circadian rhythm in signal expression of this
fish.
The nocturnal gymnotiform fish Brachyhypopomus pinnicaudatus
(Hopkins, 1991) generates
electric organ discharges (EODs) to electrolocate and communicate in the dark.
During the breeding season, B. pinnicaudatus males display EODs of
greater magnitude and duration than females
(Franchina and Stoddard, 1998;
Hopkins et al., 1990), and
further exaggerate their EODs during the night-time hours of courtship and
spawning (Franchina and Stoddard,
1998; Silva et al.,
1999) (Fig. 1). In
addition, various parameters of the EOD (amplitude, duration and repetition
rate) oscillate with true circadian rhythms, the magnitudes of which are
greater in males than in females (Silva et
al., 2007; Stoddard et al.,
2007). Therefore, heightened expression of circadian rhythmicity
in the signals of males could have partially resolved the conflict between
sexual selection for conspicuous signals and the attendant costs of predation
and energetic expense. In a polygynous species, males should produce costly
signals only at those times in the diel cycle when benefits are greatest (e.g.
when females are receptive or males are competing), and females should strive
to minimize signal costs at all times.
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). Furthermore, in males, body size correlates positively with
the magnitude of the circadian rhythms in the EOD waveform's amplitude and
duration (Franchina and Stoddard,
1998). Also, circadian rhythmicity of the EOD is affected by
social interactions. The enhanced EOD circadian rhythms observed in B.
pinnicaudatus males attenuate gradually under social isolation and
recover during social stimulation, and although social interactions with both
sexes restore a socially isolated male's EOD circadian rhythm enhancement,
male social stimuli induce a bigger and faster effect
(Franchina et al., 2001).
Furthermore, social interaction enhances the EOD discharge rate during the
night (Silva et al., 2007).
The EOD reduction observed during social isolation suggests that the nocturnal
signal enhancements could be energetically costly, perhaps too costly to keep
when no social benefit is to be gained
(Terleph and Moller,
2003).
Therefore, we asked whether the daytime reductions in the electric signal
waveform and repetition rate might save sufficient energy to confer selective
advantage upon the male signaler and thus help to explain the existence of the
well-documented sexually dimorphic circadian rhythms in the EOD waveforms and
discharge rates of Brachyhypopomus
(Franchina et al., 2001;
Franchina and Stoddard, 1998;
Hagedorn, 1995;
Silva et al., 2007;
Silva et al., 1999;
Stoddard et al., 2003). To
this end, we used respirometry and pharmacological manipulations to obtain
direct measurements of the relative energy expended in electric signals.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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O2) while we
applied successively two pharmacological agents that suppressed different
energetic components: the GABAA binding enhancer (+)metomidate HCl
suppressed locomotion, and the curare analog flaxedil blocked motor synapses
on myogenic tissue including the electric organ, thus silencing the electric
signal (details below). The body length of the tested males ranged from 19.0
to 27.0 cm and their body mass ranged from 11.8 to 17.3 g. Females' body
length ranged from 13.9 to 18.4 cm and their body mass ranged from 6.6 to 13.6
g. Fish were fasted 24 h prior to the experiments, sufficient time for gut
clearance. We measured and partitioned costs of activity, standard metabolic
rate (SMR, minimum energy required to sustain basal physiological processes
under a specified set of standard experimental conditions) and electrogenesis
by day for both sexes.
EOD measurements
Fish were transported from the outdoor colony to an indoor aquarium (280 l,
122 cmx46 cmx50 cm lengthxwidthxheight, filled with
air-saturated water at a conductivity of 100 µS cm–1)
inside a temperature-controlled room (25°C) on a 12 h:12 h light:dark
cycle. The EODs were detected by a pair of carbon rod electrodes (23 cm long,
6 mm diameter) located at opposite ends of the tank
(Fig. 2A) and amplified by an
AC-coupled differential amplifier (Charles Ward Electronics BMA-200, Ardmore,
PA, USA), 1 Hz high-pass filter, 10 kHz low-pass filter, x200 gain for
males and x500 gain for females. Online analysis was used to locate all
the EODs in a 1 s train and calculate the mean values for the discharge rate,
peak-to-peak amplitude (mV cm–1 at 10 cm) and duration (ms).
The duration of the EOD waveform was measured at 10% of the peak-to-peak
amplitude to minimize sampling artifacts
(Franchina et al., 2001;
Franchina and Stoddard, 1998;
Hopkins et al., 1990).
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Power output (energy per EOD waveform x EOD repetition rate) of the
electric organ (EOD power) could be calculated as the product of voltage and
current. But EOD power cannot be measured directly or modeled simply in
gymnotiform fish because the electric field is spatially complex
(Stoddard et al., 1999).
Fortunately, we can obtain repeatable measures of electric field strength
distant from the fish (Franchina and
Stoddard, 1998). From Ohm's Law, I=V/r,
so current (I) varies directly with the electric field (V).
Resistance (r) can be treated as a constant if water conductivity is
constant (held at 100 µS cm–1) and we assume tissue
resistance is similar across individuals. With r constant,
V2 is proportional to power (VI), thus the time
integral of V2 is a valid and useful proxy of EOD power
that lets us compare power output between individuals. This assumption is
explored further in the Discussion. To obtain a representative proxy for
electric field strength, we digitized head-minus-tail EOD waveforms of each
fish across a 1.2 m length, using a calibrated and repeatable geometry
(Franchina and Stoddard,
1998).
Daytime respirometry
We estimated the entire energy budget of active fish using oxygen
consumption as a proxy for energy expenditure. To avoid adverse effects of
social isolation on the fish's EOD
(Franchina et al., 2001), a
small male and a female were housed together with the test fish during the 24
h fasting period. An unglazed ceramic tube (3.2 cm i.d., 28.5 cm long, 223 ml)
was used as the respirometry chamber because its interference with the fish's
electric field is negligible. The respirometry apparatus consisted of a
peristaltic pump (Masterflex L/S, Model 77200-62, Cole-Parmer Instrument Co.,
Vernon Hills, IL, USA), a pair of O2-recording chambers with a
temperature-compensated Clarke oxygen electrode (Analytical Sensors, Inc.,
model D012, Sugar Land, TX, USA) inside each one, and the respirometry
chamber, all connected with Tygon® flexible plastic tubing
(Fig. 2A). The gills of
anesthetized fish (see below for procedure) were irrigated continuously with
air-saturated water pumped into the mouth.
We measured the oxygen concentration in the water as the peristaltic pump drove air-saturated tank water through the entire apparatus at an average flow rate of 30 ml min–1. A two-channel polarographic oxygen and temperature meter (Cameron Instruments Co., model OM200, Port Aransas, TX, USA) recorded readings from oxygen electrodes on the intake and outflow of the chamber (Fig. 2A). The oxygen electrode's zero end was calibrated once at the start of an experiment with a fresh solution of 100 mg of sodium sulfite per 5 ml of 0.1 mol l–1 sodium borate, while the high end (saturation level) was re-calibrated with air-saturated water. Data from the polarographic meter were simultaneously conveyed to the computer as it sampled and analyzed the electric signal data.
Pharmacological partition of the energy budget
After collecting control data from a resting fish
(O2,total) using
the respirometry apparatus, we induced the fish for 10 min with a 15 p.p.m.
solution of (+)metomidate HCl, a GABAA binding enhancer that
inhibits motor activity but not the EOD. Then the fish's gills were irrigated
with a 5 p.p.m. maintenance solution of metomidate at a flow rate of 30 ml
min–1 (Hattingh et al.,
1975). We measured O2 consumption rate
(O2,metomidate)
until it stabilized, typically 30 min after induction. At the concentration we
used, metomidate increases EOD amplitude by 10% over 2 h (M. R. Markham,
personal communication), but our measurements were completed in 30 min, over
which time metomidate has no measurable effect on the EOD. Next we completely
silenced the EOD by injecting the fish intramuscularly with 3 µg
g–1 fish of the curare analog flaxedil (gallamine
triethiodide; Sigma, St Louis, MO, USA), a nicotinic acetylcholine receptor
blocker. Again we recorded O2 consumption
(O2,metomidate&flaxedil).
At the end of a pharmacological experimental set, the test fish's gills were
irrigated with air-saturated water until it recovered from the drug
effects.
By subtracting oxygen consumption rates
(O2) across the
different pharmacological manipulations, we calculated the rates associated
with the different energy budget components
(Fig. 2B), standard metabolic
rate
(O2,SMR=O2,metomidate&flaxedil),
electric signal production
(O2,EOD=O2,metomidate–O2,metomidate&flaxedil),
and everything else such as activity, muscle tone and ventilation
(O2,other=O2,total–O2,SMR–O2,EOD).
We used regression analysis to evaluate the relationship between EOD power and
the dependent variable
O2,EOD, during
daytime. In addition, to assess the ancillary effects of the drugs we used, we
reversed the order of drug treatment in five additional males.
Night-time methods
We measured oxygen consumption during normal nocturnal activity by sealing
two fish of the same sex and size in a large tank. The fish were separated by
a plastic screen to allow electrical interaction but to prevent fighting,
which might suppress the loser's EOD. The tank was sealed with an acrylic lid
that covered the entire water surface. One O2 electrode was mounted
in the lid so that oxygen concentration in the chamber could be recorded
continuously for 9 h. The difference between the final and initial oxygen
concentrations equaled the total oxygen consumed by the two fish. We assumed
that fish in a pair consumed O2 at a similar rate since they were
matched by weight and length. Thus we divided the total O2 of the
fish pair by two to calculate the mean O2 consumption rate for each
fish during the night. We could not perform the daytime pharmacological
manipulations at night because the night-time changes in EOD values are
altered by light and handling, and diminish in the absence of social
stimulation (Franchina et al.,
2001). Instead, we used two alternative models to estimate the
relationship between
O2,EOD and EOD
power at night.
Models and data analyses
Model 1 assumes an individual's
O2,EOD increases
linearly with the measured increase in EOD power at night. Model 2 assumes
that the within-individual day-to-night changes follow the regression
equations derived from the between-individual (same sex) data collected during
the day (see Results, Fig. 3).
For females, the two models produced indistinguishable values for modeled
night-time
O2,EOD, but for
males, model 2 estimated mean night-time costs of electrogenesis to be about
twice as high as those estimated by model 1. Both models assume that
O2,EOD varies
linearly with discharge rate, an assumption we justify on theoretical and
empirical grounds. EOD waveforms are not affected by discharge rate across the
normal range of rates (Franchina and
Stoddard, 1998) so the energetic cost of the EOD should be
determined by the ATP required to actively transport the charge-carrying ions
(Na+ and K+) back across excitable membranes following
the action potentials. Empirically,
O2,EOD
consumption varied linearly with EOD rate across males
(Fig. 3C), though the data from
females, with their low EOD power, were too noisy to establish a strong
relationship (Fig. 3C). Even
tighter relationships were obtained within individuals; however, these
relationships are methodologically problematic because sufficiently variable
EOD rates were only evident in untranquilized fish, in which locomotor
activity is likely to covary with EOD rate. Because EOD rates were altered
significantly by our handling and drug treatments, we rescaled the day and
night values for
O2,EOD to comply
with mean day and night rates recorded in our lab from resting and courting
pairs of fish. We divided
O2,EOD values by
obtained discharge rates then multiplied by the sex-typical mean discharge
rates (day 23.0 Hz for both sexes, night 75.6 Hz for males, 61.0 Hz for
females, at 27°C).
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All analyses and models were written in Matlab 7 with the Statistics
Toolbox (script available upon request). Statistical analyses were all
2-tailed with 
set to 0.05. All values are expressed as means and 95%
confidence intervals.
O2,EOD values
for females were normally distributed but those for males were not, thus we
log transformed the male data to eliminate heteroscedasticity and used the
transformed values in our analyses.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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O2 differed
across the sexes (two-way ANOVA, dependent variable
O2 and fixed
factors sex and time of day: F1,37=11.60,
P=0.002) and total
O2 differed
significantly between day and night (F1,37=20.71,
P=0.0001). Although absolute costs of activity
(O2,other) did
not differ significantly between the two sexes (Wilcoxon rank-sum test,
P=0.36), the cost of electrogenesis
(O2,EOD) was
much higher for males than for females (P=0.028), as was the standard
metabolic rate
(O2,SMR;
P<0.0001; Fig.
3A).
Oxygen consumed per EOD
(O2,EOD/rate in
µl O2 EOD–1) varied tightly with measured EOD
power (mV2 cm–1) in both sexes
(Fig. 3B), confirming that the
cost of electric signal production can be isolated accurately and measured
with the methods we used. Oxygen consumed per EOD by males was best described
by a power function of EOD power
(y=3.32e–05x1.80–1.03e–05,
R2=0.99, F>200, P<0.0001, where
x is EOD power and y is oxygen consumed per EOD). For
females, oxygen consumed per EOD was best described as a linear function of
EOD power after log transformation (logy=1.06
logx–2.64, R2=0.79, F=26.0,
P=0.001). Controlling for EOD power,
O2,EOD varied
linearly with EOD rate in males (R2=0.56,
F=10.02, P=0.013, Fig.
3C). This relationship was weak in females
(R2=0.15, F=1.26, P=0.3,
Fig. 3C), perhaps because their
values were closer to the noise floor of the measurement system.
The male EOD as a condition-dependent signal
Body condition is commonly estimated as mass adjusted for body length
(Jakob et al., 1996;
Kotiaho, 1999;
Marshall et al., 1999). While
neither the male's body mass nor length alone was a good predictor of male
O2,EOD (mass:
R2=0.34, F=4.16, P=0.08; length:
R2=0.05, F=0.43, P=0.53), male body mass
robustly predicted
O2,EOD after
partialing out body length with stepwise linear regression
(R2=0.75, F=10.29, P=0.008,
Fig. 4). The strong
relationship between residuals of male body mass and O2 consumed in
electrogenesis suggests that the EOD is a condition-dependent signal, one for
which males pay a premium incremental cost for increased signal power
(exponent 1.8). Among females, by contrast, body mass was sufficiently
correlated with body length that either factor alone predicted
O2,EOD (mass:
R2=0.76, F=9.52, P=0.014; length:
R2=0.76, F=21.59, P=0.002).
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Based on model 1, the EOD as a mean percentage of the males' total energy
budget increased from 8.3% by day (where daytime
O2,EOD was
0.0038, 0.0244 and 0.1814 µl O2 s–1 minimum,
median and maximum, respectively) to 12–26% at night (night-time
O2,EOD was
0.0131, 0.1095 and 0.3442 µl O2 s–1 minimum,
median and maximum, respectively). For females, the relative expense of the
EOD remained unchanged between day and night, being 3.4% for both (daytime
O2,EOD was
0.0024, 0.0042 and 0.0145 µl O2 s–1 minimum,
median and maximum, respectively; and night-time
O2,EOD was
0.0053, 0.0125 and 0.0642 µl O2 s–1 minimum,
median and maximum, respectively). Across 24 h, bioelectrogenesis consumed
11–22.5% of the males' total energy budget (where 24 h
O2,EOD in males
was 0.0169, 0.1339 and 0.5256 µl O2 s–1
minimum, median and maximum, respectively) but only 3.4% of the females' (24 h
O2,EOD in
females was 0.0077, 0.0167 and 0.0787 µl O2 s–1
minimum, median and maximum, respectively). Taken in the context of the entire
energy budget, diurnal reduction of EOD pulse rate and waveform conferred a
total daily energy saving of 7–16% for males and 2% for females
(Fig. 3A and
Fig. 5B).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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O2,SMR of males
(0.138 µl O2 s–1) was over an order of
magnitude higher than that of females (0.0085 µl O2
s–1). We were not surprised to find that males have higher
SMR than females because of the high energetic demands of reproductive
competition among males. But even after adjustment for differences in body
mass, this difference is still larger than we expected from a sex difference
in global cellular metabolism alone. The sex difference in SMR could also
result from a substantially higher cost of maintaining the male's electric
organ. Thus our calculated
O2,SMR values
may include some maintenance components of the electric organ beyond costs per
discharge and we may have underestimated both the overall cost and sex
difference in the cost of electrogenesis. Other sources of error probably
include the differences in size, night-time activity levels, and signal
strengths and rates between captive-reared and wild fish, as well as the
proportionally higher measurement error for females due to their smaller EODs
and lower metabolic rates. Curare analogs such as flaxedil probably quiet some
cell groups in the brain and, as mentioned before, (+)metomidate HCl enhances
the EOD waveform by 5–10% over 2 h. Any of these errors would change our
numbers by a few per cent, but none of these is large enough to alter the
general conclusions of our analysis.
Adaptive significance of the sex difference in the energetic cost of the different EOD components
Sex differences in the energetic costs of different EOD components may
reflect the relative adaptive importance of each component in the life
histories of the two sexes. In the sexually dimorphic species B.
pinnicaudatus, EOD waveforms of females are very much like those of
sexually undifferentiated juveniles. So, if one assumes that the female EOD
has not been altered significantly by sexual selection, it follows that the
energetic costs of the female EOD are primarily those needed for
electrolocation. Costing only 3.5% of her total energy budget, the female's
electric signal appears relatively inexpensive, as postulated previously for
weakly electric fish in general (Bell et
al., 1976; Julian et al.,
2003). This logic also suggests that the female's nightly increase
of EOD rate facilitates electrolocation, an assumption strongly supported by
experimental data demonstrating enhanced sensory acuity with increased
discharge rate (Caputi et al.,
2003; Heiligenberg,
1980; Lissmann and Machin,
1958). Because mature male and female B. pinnicaudatus
show similar electrolocation thresholds
(Stoddard et al., 2006), we
believe that sex differences in electric signals, and the higher energetic
costs for males, are a sole consequence of sexual selection for
communication.
The nightly increases in amplitude and duration of the EOD waveform may be
adaptations to advertise the social and sexual status of males and to a lesser
extent of females. In other gymnotiform species, both sexes display dominance
hierarchies (Black-Cleworth,
1970; Hagedorn,
1986; Hagedorn and
Heiligenberg, 1985; Hopkins
and Westby, 1986; Westby,
1975). For instance, female B. occidentalis (a congener
of B. pinnicaudatus) are known to be highly territorial
(Hagedorn, 1988) and captive
males compete for refuge sites (Hagedorn
and Zelick, 1989). In B. pinnicaudatus, dominance
interactions are common within both sexes, but we suspect they play a bigger
role in the reproductive success of males, which appear to advertise their
social status through their EOD waveforms. For instance, B.
pinnicaudatus males increase their EOD waveform more when presented with
another male than when presented with a female
(Franchina et al., 2001) and
the magnitude of the changes depends on the relative sizes of their respective
waveforms at the onset of the interaction (V.L.S., unpublished data).
Sexual selection appears to have left multiple signatures on the electric
signal production of males. Assuming the validity of our estimated
O2,EOD at night,
EODs of males are not only more energetically expensive than those of females,
but also make the males more conspicuous to electroreceptive predators by
diverting significant signal energy into the spectral sensitivity range of
electrosensory predators (Hanika and
Kramer, 1999; Hanika and
Kramer, 2000; Stoddard,
1999; Stoddard,
2002). It follows that the enhanced night-time EODs of males may
provide honest indicators of male quality since those males that display
nocturnal enhancement of the EOD incur the greatest energetic costs and
predation risks. Another indicator of honest sexual signaling is that the
energetic cost of the males' EODs is positively related to their body
condition. Studies using experimental manipulations of the condition of males
are needed to characterize the role of the nightly EOD enhancement in B.
pinnicaudatus males as a condition-dependent signal.
Our use of the time integral of V2 as a proxy of EOD
power depends on the assumption that resistance (r) is constant
across individuals. In fact, we believe that resistance is likely to be
similar among members of each sex but to be systematically higher in females
than males. Male Brachyhypopomus pinnicaudatus have longer and
broader caudal filaments (tails) with flared tips, the `feather-tails' for
which they were named (Hopkins,
1991). These traits are thought to lower impedance between the
electric organ and the surrounding water in male B. pinnicaudatus
(Stoddard et al., 1999).
Likewise, electrocytes of male B. pinnicaudatus have a lower membrane
resistance than do those of females (M. R. Markham and P.K.S., unpublished
data). Thus resistance is possibly an order of magnitude higher for females
than for males. The effect of this difference can be seen in
Fig. 3B as a rightward shift of
female estimated EOD power towards the male values. For example, if
rfemale=10rmale, we would shift
females 10 times to the right, causing females to overlap the low-end cluster
of males in estimated EOD power. At the same time, because body plans and
membrane resistances are similar among members of each sex, uncertainty about
sex differences in resistance does not affect our figures or conclusions about
the relationship between EOD waveform and energy consumption within each sex.
Further, resistance has no bearing on our analysis of sex differences in
energy allocation.
Adaptive significance of circadian rhythms in electric signal production
Male electric fish may enhance their EOD waveforms to advertise quality and
may increase their EOD repetition rates both as signals of quality and to
improve the acuity of electrolocation. But having improved the efficacy of a
signal for its various functions, why reduce these parameters during the day?
Both predation risk and metabolic energetic costs may account for the daytime
signal reduction in males. Diurnal reductions in signal output
(Franchina and Stoddard, 1998;
Silva et al., 1999) confer
significant energetic savings, especially in males as determined by our
estimated night-time
O2,EOD values, a
probable selective advantage of circadian rhythms in the different signal
parameters. The males' EODs are not only more energetically expensive on
average than those of females, but the low frequency spectral shifts,
characteristic of the EOD waveform at night, render the signaler more
conspicuous to electroreceptive predators
(Hanika and Kramer, 1999;
Hanika and Kramer, 2000;
Stoddard, 1999), a common cost
of sexual signals (Zuk and Kolluru,
1998). Nevertheless, if circadian rhythms in male EODs are solely
adaptations to predation pressure, one might expect to find an inverse
relationship between predation intensity and the sexually selected trait, in
this case EOD circadian rhythms, similar to the signal trait variation seen in
other fish such as guppies and sticklebacks
(Candolin, 1997;
Endler, 1978;
Endler, 1980;
Endler and Houde, 1995;
Moodie, 1972). Males in
populations subjected to strong predation pressure should display smaller EOD
circadian rhythms on average (the EOD waveform should be less exaggerated at
night to reduce conspicuousness, and the EOD repetition rate should be higher
during the day to detect incoming predators), while those under low predation
intensity should display more pronounced EOD circadian rhythms. Different
geographical populations under different predation regimes often display rapid
evolution, where predation pressure intensity leads to alternative life
histories (Schoener et al.,
2005; Yoshida et al.,
2003). Perhaps such a pattern may be present across
Brachyhypopomus populations. Alternatively, if the magnitudes of
circadian rhythms in the EODs remain unchanged across populations, regardless
of differences in predation pressure, one would conclude that other selective
pressures (i.e. energy conservation) sustain circadian oscillation of the
sexually selected signal traits. Given that male B. pinnicaudatus
from Uruguay and male B. occidentalis from Panama both display marked
EOD circadian rhythms (Hagedorn,
1995; Silva et al.,
1999), yet occupy habitats free of large electroreceptive
predators (Eigenmann and Ward,
1905; Hagedorn,
1988; Silva et al.,
2003), we suggest that the energetic cost of the enhanced
night-time EOD is sufficient to sustain the persistence of strong circadian
rhythms in the EODs of Brachyhypopomus.
How does the energetic cost of electric signals compare with the energetic cost of acoustic signals?
We assume that the EOD has been subjected to selective forces similarly
documented in other communication models, such as insects, frog and birds, to
mention a few (Andersson,
1994). We compared the energetic cost of electric signals to the
well-characterized acoustic signals across different organisms to gain an
understanding of where electric signals fall in reference to the energetic
cost of communication signals in general. For the purposes of this comparison,
we used `signaling' factorial scope, the organism's
O2,signal
divided by its
O2,resting,
where O2,signal
is the oxygen consumption when the animal is signaling and
O2,resting is
the oxygen consumption when the animal is silent. During both conditions the
animals are stationary. The signaling factorial scope is a good metric for
comparative studies because it standardizes the energetic allocation across
the effective metabolic demand of the organism by measuring the factor by
which communication exceeds the metabolic cost at resting level. Analysis of
the signaling factorial scopes across acoustic signalers compared with
electric fish in this study indicates that the energetic cost of electric
signals falls within the high end of the orthopteran range, within the lower
end of the anuran range, approximately five times the energetic cost of
crowing in a non-passerine bird, and twice the energetic cost of singing in a
passerine bird (Table 1).
|
In contrast to acoustic signals, electric signals spread locally but do not
propagate through the environment
(Hopkins, 1986). The fish's
electric organ creates an electrostatic field, the strength of which decreases
by three orders of magnitude just 10 cm from the fish
(Assad et al., 1999;
Assad et al., 1998;
Stoddard et al., 1999). An
electric fish needs to increase its EOD field strength by a factor of eight to
double the range of its electric field
(Hopkins, 1986). Differences
between the physical transmission properties of acoustic and electric signals
may increase the relative cost of EODs over acoustic signals when they are
used for sexual advertisement. Because electric signals enable electrolocation
as well as communication, electric fish need to generate their EODs
continuously to monitor changes in their surroundings. This dual function of
electric signals increases selective pressure for low cost signals because
turning off the electric signal for prolonged periods of time eliminates the
active electric sense, increasing the risk of predation from all aquatic
piscivores.
|
Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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