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First published online June 15, 2007
Journal of Experimental Biology 210, 2244-2252 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.003509
Electrical and behavioral courtship displays in the mormyrid fish Brienomyrus brachyistius
Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA
* Author for correspondence (e-mail: ryan.wong{at}mail.utexas.edu)
Accepted 19 April 2007
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Summary |
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Here we describe nine common motor displays and 11 SPIs. Analysis of frequency of occurrences suggests that some SPI patterns are sex and season specific. We also observed electrical duetting called `rasp matching' during courtship signaling among pairs; males and females exchange `rasps' and `bursts', respectively, in alternation. Our study employs new techniques to separate and document SPIs in the context of courtship. We show that some SPIs correlate with specific behavioral acts around the time of spawning.
Key words: Mormyridae, Brienomyrus, courtship, reproduction, electrocommunication, electric organ discharge
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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) (for reviews,
see Kramer, 1990;
Ladich et al., 2006;
Moller, 1995;
von der Emde, 1999). The
waveform of the electric organ discharge (EOD) is highly stereotyped and
contains information about species, sex and social status (reviewed by
Carlson, 2002). The sequence of
pulse intervals (SPIs) varies according to the behavioral state and motivation
for aggression and courtship (reviewed by
Carlson, 2002). This paper
seeks to add to the limited knowledge of SPIs and behavioral motor acts
involved in the context of courtship in mormyrids.
The behavioral work that has been done on mormyrid signaling has focused
mostly on agonistic interactions because of their territorial behavior and the
ease of observing their chasing and fighting. Some studies used mixed species
interactions in which individuals could be distinguished by their divergent
waveforms (Kramer, 1974;
Kramer and Bauer, 1976). Other
studies tethered an individual to a wire as a way of uniquely identifying its
pulses in a mix (Bell et al.,
1974; Graff, 1987;
Hopkins and Westby, 1986).
Still others controlled the location of an interacting pair
(Moller et al., 1989;
Terleph and Moller, 2003). As
a result of these studies, we know about correlations between overt behaviors
and associated stereotypic SPIs (reviewed by
Hopkins, 1986a)
In spite of this work, little is known about SPIs during courtship behavior
of mormyrid fish. Hopkins and Bass
(Hopkins and Bass, 1981) first
described an SPI during courtship, termed `rasp', during their field study on
Brienomyrus sp. from Gabon. However, because these experiments were
conducted in the field where visibility was poor, the signals could not be
correlated with behavior. Kirschbaum and Westby
(Kirschbaum and Westby, 1975)
reported the first successful breeding of mormyrids under laboratory
conditions but did not describe any motor behavior. Crawford et al.
(Crawford et al., 1986)
documented courtship behavior of lab-bred Pollimyrus isidori, but
concluded that courtship communication was largely acoustic-based and not
through electric discharges as electrical signaling was suppressed during the
male's acoustical courtship calls. The few SPIs that did occur during
courtship in P. isidori were limited to changes from random
discharges to a regularized discharge rate or cessations
(Bratton and Kramer, 1989).
Kirschbaum and Schugardt (Kirschbaum and
Schugardt, 2002) reported success in breeding five additional
different species of mormyrids, but did not report on courtship signaling.
Although our laboratory in the past has successfully bred B.
brachyistius in captivity, courtship behavior was not documented.
Recently, Werneyer and Kramer (Werneyer
and Kramer, 2005) described electric signaling and behavior during
courtship in one pair of Marcusenius macrolepidotus. M.
macrolepidotus showed no courtship behavior and produced only one
putative courtship specific SPI (Werneyer
and Kramer, 2005).
Although Kirschbaum and Schugardt
(Kirschbaum and Schugardt,
2002) found that lowering the conductivity, rising water levels
and the sprinkling of water over the surface induces reproductive behavior,
successful spawning is difficult to achieve for some species. Each has
different requirements for induction of spawning. Although we succeeded in
breeding Brienomyrus brachyistius, an even greater challenge was to
separate the EODs from more than one fish so that we could reconstruct each
individual's patterns of discharge. Previous methods were too invasive to
allow studies of courtship. However, with available technology, custom-written
computer programs allowed for EOD discrimination by sex in freely behaving
mormyrids. A similar method has recently been used
(Werneyer and Kramer,
2005).
In this study, we reliably induced courtship while separating the EOD pulses in four pairs of B. brachyistius. We used two new methods to simultaneously record and view electrical and behavioral motor displays and automatically separated pulses based on sex-specific EOD waveforms. Video editing software allowed the merging of high quality EOD recordings with video recordings so that behavior and SPI patterns could simultaneously be viewed.
To separate a mixed signal, we used cross correlation analysis via
a custom written program that was originally developed by Carlson (see
Arnegard and Carlson, 2005).
Briefly, a single EOD from each individual was digitized at 30 kHz sampling
frequency and stored as a template for that individual. The combined signals
from both fish were cross correlated, first with one and then the other
individual's template. We reliably identified the two EOD types and assigned
each to one individual or the other by comparing the two cross correlations.
This method is accurate when there are clear differences in the duration of
EOD waveforms. Because EODs in B. brachyistius are sexually dimorphic
and the male's EOD is even more divergent from female's during breeding
seasons, we were able to assign the sex to each EOD. Collectively, nine
behavioral categories and 11 SPI patterns are described for B.
brachyistius, some of which show sex and season specificity.
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Materials and methods |
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) is found naturally in western Africa with a patchy
distribution ranging from Southern Senegal to coastal Gabon and Congo.
Although no information is available about the breeding season for B.
brachyistius, other mormyrids breed with the onset of the rainy seasons
(Hopkins and Bass, 1981;
Kirschbaum, 1995). Decreasing
water conductivity, increasing water levels, and artificial rainfall on the
surface all promote gonad growth in this and other species
(Kirschbaum, 1979;
Kirschbaum, 1987;
Kirschbaum and Schugardt,
2002; Schugardt and
Kirschbaum, 2004). The fish used in this study were wild-caught
sexually mature males (N=4) and females (N=4) with a
standard length greater than 110 mm. The fish originated from Nigeria, Africa
via a commercial dealer. The two sexes were distinguished based on
the presence of an anal fin notch on the male and absence of one on the female
(Brown et al., 1996).
Stimulated breeding
In preparation for the study, each pair of fish was acclimated for 3 weeks
in a 190 l aquarium kept at 25°C and on a 12 h:12 h light:dark cycle. The
tank contained plastic tubes, driftwood, plants (Vesicularia dubyana)
and cotton filter material. At the outset, water conductivity was maintained
at high levels at 300–350 µS cm-1 to inhibit breeding. The
conductivity was then gradually lowered over a 3-week period to 20–40
µS cm-1 by addition of deionized water. With the drop in
conductivity, we observed the onset of courtship activity. The addition of
water raised the water level in the tank approximately 2 cm per day until the
tank was filled.
Behavioral and electrical recordings
We recorded electrical and behavioral activity during 30 min sessions on 10
different days equally divided into two phases: one at the end of the
acclimation period (non-breeding) and one during the low conductivity periods
after courtship commenced (breeding). We recorded B. brachyistius
behavioral activity at night using infrared light illumination and a Sony
Digital Video Camera Recorder (Model DCR-PC100). All recordings were done 2 h
after the onset of darkness. Two chlorided silver wire dipole electrodes were
placed on opposite sides of the tank to capture all electrical activity even
as the fish swam around the tank. The signal was amplified 100x with a
differential AC amplifier (A-M Systems, Inc., Everett, Washington, USA; model
1700) and band-pass-filtered from 0.1 Hz to 10 kHz. These signals were
recorded on the two-channel audio track of the digital video recorder and
simultaneously on a desktop computer using Cool Edit 2000 (Syntrillium 2000).
The recording of the latter provided a clean low-noise recording. To minimize
electrical noise during the recordings, all motors, pumps and unnecessary
electronic equipment were shut off for the duration of the trial.
Each video recording was digitized using the video-editing software, Adobe Premier Pro (Adobe Systems 2003). We replaced the low quality audio track recording of the EODs with the high quality stereo recording from the computer after ensuring accurate alignment of the two signals. Realignment of video with digital audio tracks were accurate to 0.5 ms.
Signal separation
We used a custom software written in Matlab 6.1 (MathWorks 2000) by Carlson
(see Arnegard and Carlson,
2005) to separate a mixed signal based on sex. The
cross-correlation analysis is most effective when there is a distinct
difference in EOD duration between male and female. The sexually dimorphic EOD
waveforms of B. brachyistius, which become further divergent in the
breeding season, allow us to use cross correlation to identify the sex of the
fish that emitted a particular EOD. From a 30-s recording of a mixed signal
recording, we selected one EOD from a male and one from a female as templates
for cross correlation analysis (Fig.
1A). We then computed the cross correlation between the signals
and each EOD template (30-s segments) (Fig.
1B,C). We calculated the square at each point to eliminate
polarity of the original waveforms. We then compared the heights of the two
resulting peaks and sex was assigned based on which one had a higher value
(see Fig. 1B,C). As a final
check, we inspected by eye to correct errors in mis-assigned EODs. We had
incorrect assignments only when two EODs were similar in duration or when a
pulse from each individual occurred almost at the same time. When correcting
errors, we noted the patterns of amplitude changes in the original record, as
well as the recent firing patterns. A plot of the SPI for each sex was made so
that we could view any stereotyped temporal patterns
(Fig. 1D,E).
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Behavioral and sequence of pulse interval analysis
For each of the four pairs of fish, we observed and video-taped 30 min of
behavioral and electrical activity on five different nights during both high
and low conductivity conditions. From these 30-minute segments, we randomly
selected three consecutive minutes of activity for detailed analysis, totaling
15 min per pair for non-breeding conductivities. We identified SPI displays
and occurrences for stereotyped motor acts for each fish and tallied their
frequencies (Fig. 2). During
the stimulated breeding period, we selected to analyze records surrounding
courtship events that included at least one `spawning' motor act using the
same methods described above (see Table
1 for motor act description). A courtship event started when the
male and female were behaviorally interacting (excluding `hovering') within
approximately 7 cm of each other for at least 30 s and ended when that
interaction stopped for at least 30 s. We included here analysis of 64.5 min
of courtship activity (129x30-s segments) for all pairs. The results
were then expressed as events per 15 min to be compared to rates of activities
during the high conductivity period. We defined electrical and motor acts
using subjective cues from the video and the patterns in the SPI. We used
Carlson (Carlson, 2002)
terminology for electrical displays. `Scallops' were defined according to
Serrier and Moller (Serrier and Moller,
1989). We distinguished `creaks' from `scallops' by the longer
minimal interval lengths and the cessation periods preceding and following the
`creak'. `Gradual increases' were distinguished from `scallops' by the long
duration of returning to original interval lengths following the burst of
pulses (2–6 s) and the greater number of EODs (>30).
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There were both seasonal and sex differences in motor acts and SPIs. Tables S1 and S2 in the supplementary material show the frequency of behavioral motor acts and SPIs (events per 15 min), respectively, listed by sex and season. For seasonal behavioral differences, males `HTC', `spawned' and `followed' more in the breeding season than the non-breeding season (Mann–Whitney U-test, P<0.05). Females showed increased behavioral activity for `HTC', `spawning' and `probing' in the breeding period (Mann–Whitney U-test, P<0.05). `Spawning' and `HTC' were exclusively seen during courtship bouts. For SPIs, males and females both increased the number of `fast bursts' (Mann–Whitney U-test, P<0.05) during courtship. Males increased the number of `creaks', `rasps', `fast bursts' and `short cessations' (Mann–Whitney U-test, P<0.01). Females had significantly more `fast bursts' and `gradual increases' (Mann–Whitney U-test, P<0.05) in the breeding period while `long cessations' were seen more during the non-breeding period (Mann–Whitney U-test, P<0.05). `Creaks', `rasps' and `gradual increases' were only seen during courtship, whereas `scallops' and `slow bursts' were non-breeding season specific.
Within a season, there were sex-typical behaviors and SPIs. In the non-breeding season, males `probed' more than females. A male was also seen to have `no activity' during the breeding season while the females were always active. `Lunges' were male specific and `fleeing' was female specific in both seasons. The remaining behaviors were not preferentially displayed by either sex in the two seasons. For SPIs, aside from `medium bursts', which were produced more by males, on average no other SPIs were emitted more by a sex during the non-breeding season. As for breeding season, `rasps' and `creaks' were male specific. Males also emitted more `medium bursts' and `short and long cessations' (Mann–Whitney U-test, P<0.05) in this season. The many cessations indicated the periods of time between other SPIs such as `rasps' and `medium bursts'. There were also many more `fast bursts' by the female (Mann–Whitney U-test, P<0.05). The only female sex-specific SPI pattern was the `gradual increase'.
Quantitative analysis of simultaneous electrical and motor patterns
With the ability to use video editing software in conjunction with SPI
graphs based on sex, we could view the corresponding SPI patterns emitted
during a particular behavior. Table S3 and Table S4 in the supplementary
material show the number and types of SPIs emitted for a respective behavior,
by sex for 60 and 64.5 min of analyzed non-breeding and breeding recordings,
respectively. Although there were few behavioral patterns with a single
associated SPI pattern (e.g. `fast or medium bursts' with `lunging' in males
and `fast bursting' with `fleeing' in females), there were many behaviors
associated with more than one SPI pattern. Similarly, there were few SPI
patterns with a single associated behavior; females only `regularized' and
`scalloped' when `hovering' during non-breeding conditions and males only
`creaked' while `spawning' during breeding conditions.
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;
Kramer, 1974;
Moller et al., 1989). Males in
this study were larger than females, were always dominant to the female and
freely swam around the tank. While the male was patrolling, the submissive
female tended to avoid the male by either hovering in a head-up posture or
move toward the opposite side of the tank. While exhibiting either of these
behaviors, some females were electrically silent for long periods indicating
submissive behavior (Bell et al.,
1974; Kramer,
1974; Moller et al.,
1989). This strongly contrasted with the male as he frequently
discharged and had higher numbers of `short cessations'. During the relatively
infrequent encounters with the female, he would `lunge' and chase the female
while emitting a `fast or medium burst'. This behavior and electrical
discharge frequency was also seen in Gnathonemus petersii in a
dominance-subordinate relationship with another mormyrid
(Bauer, 1972). There were also
periods of times where both sexes `hovered' near each other, emitted
`scallops' and ceased when there were behavioral interactions. `Scallop'
production during non-breeding conditions have previously been seen while fish
were resting, and decreased in frequency during social interactions
(Moller et al., 1989).
During courtship there was a marked increase in all motor and electrical
activities. The male became tolerant of the female, which was indicated by
prolonged and increased mutual behavioral interaction. The ritual included
many permutations of initiating contact, `following', `HTC' and `spawning'.
The lack of a rigid behavioral ritual suggests that motor patterns are not
critical in eliciting receptivity of the female. This may also be the case in
M. macrolepidotus as the female began spawning bouts almost
immediately when given access to the male
(Werneyer and Kramer, 2005).
We did not observe any differences in behavior compared to the non-breeding
conditions when the pairs were in breeding conductivities but not engaged in
courtship.
Rather, SPIs more likely constitute honest signals. As seen in Table S3 and
Table S4 in supplementary material, multiple SPIs were associated with a motor
act during courtship, further suggesting that motor acts are not evaluated as
critically as SPIs by each sex. `Rasps' have been previously described during
breeding seasons in the wild for Brienomyrus sp., and B.
brachyistius and are believed to be a courtship signal
(Hopkins and Bass, 1981;
Carlson and Hopkins, 2004).
This study lends support to that idea as `rasps' were only produced by males
during courtship activity. Notably, males produced many more `rasps' and
`medium bursts' than any other SPI found during courtship and those SPIs were
seen in all behaviors involving close proximity to the female. This suggests
that these SPIs play a significant role during courtship as the male's
advertisement signal. It is possible that some aspect of the timing or
characteristic of each SPI conveys fitness information. Furthermore, future
studies should look at possible correlations between characteristics of the
rasp and male quality (e.g. health, size, social status).
As soon as the male initiated courtship by `lunging' or `swimming' near the
female, she continuously emitted EODs. Perhaps more interestingly, the female
rarely had any `cessations' and each SPI pattern merged continuously. The rate
of `fast bursts' increased over five times between seasons. Previously, bursts
had mostly been described in all behavioral contexts besides courtship in
mormyrids; they frequently served to indicate dominance and possibly to
enhance electrolocation (Bell et al.,
1974; Kramer,
1974; Kramer,
1976). While not dominant, the high frequency of discharging `fast
bursts' by females during courtship suggests they may also serve as a
communication response in this species and M. macrolepidotus
(Werneyer and Kramer, 2005).
Hopkins and Bass (Hopkins and Bass,
1981) showed that while playing female EODs in the field to males
during the breeding season, the males responded with `rasps'.
There appeared to be a coordinated communication pattern between the male
and female during courtship (Fig.
5). Although not as complex as the acoustical courtship in P.
isidori, the observed B. brachyistius electrical courtship was
more complex than that described in M. macrolepidotus
(Bratton and Kramer, 1989;
Werneyer and Kramer, 2005).
Male `rasps' or `medium bursts' were followed by female `fast bursts' or
vice versa, which we termed `rasp matching'. This duet was only seen
during breeding conditions and when the sexes were interacting for long
periods of time. Although not focused on in this study, `rasp matching'
contains some possible cues for future research to focus on, which include
timing of each SPI relative to the opposite sex's SPI and the matching of
frequencies. This electrical duetting between the sexes also can serve one of
many possible functions such as a form of evaluation of the fitness of each
sex, maintaining contact with the opposite sex, or indication of mutual
interests as seen in avian acoustic duetting
(Hall, 2004)
The data suggests that some SPI patterns were associated with a motor act
during courtship. As mentioned previously, some SPIs occur in greater
frequency with a particular behavior but `creaks' were only produced by males
during spawning. Although random SPIs were also seen during spawning, `creaks'
were not found with any other behavior. The general pattern of the `creak' was
seen in P. isidori and the one male M. macrolepidotus during
their respective spawning bouts (Bratton
and Kramer, 1989; Werneyer and
Kramer, 2005). Similar to female M. macrolepidotus, B.
brachyistius females predominantly emitted a `medium burst' when spawning
(Werneyer and Kramer, 2005).
There were, however, occasional `random' SPI by the female during this event.
This could be a result of an unsuccessful courtship, either in terms of the
male's failure to elicit receptivity from the female or poor positioning
during `spawning'. However, during successful `spawning' events, in which both
quiver their bodies and it lasts 2–3 s, the male and female emitted
`creaks' and `medium bursts', respectively. The functions of these SPI
patterns are currently unknown but they may facilitate or signal the release
of gametes. Although no eggs were found the following day in this study, eggs
were found in other species exhibiting similar SPIs to the `creak' and `medium
bursts' in the vent-to-vent copulatory behavior
(Bratton and Kramer, 1989;
Werneyer and Kramer,
2005).
This study, and to our knowledge, one other study have successfully
documented courtship in a mormyrid that only possesses the electric modality
for communication (Werneyer and Kramer,
2005). Although this study reports courtship activity from four
different pairs, we are confident that the overt behaviors and SPIs are
characteristic of this species during courtship because of the consistencies
of behavioral and electrical displays seen across the pairs between breeding
and non-breeding conditions. Moreover, we observed a putative male
advertisement signal (`rasp') in the laboratory, which has been seen in the
wild during the breeding season, suggesting that we have induced similar
breeding conditions as in the wild and likely similar communicative and
behavioral responses (Hopkins and Bass,
1981). We acknowledge that our periods of data analyses were
relatively shorter compared to the recorded periods. This may pose as a
limitation to our understanding of the electrical and motor displays during
breeding conditions while not engaged in courtship. However, we analyzed all
the data during courtship and feel we have captured electrical and motor
displays during those events. For periods outside of courtship, in each pair
we observed similar behaviors seen in the non-breeding periods. With regards
to non-breeding conditions, we observed similar behavioral displays throughout
each of the observation periods for all pairs.
The importance of sensory modalities such as the auditory, olfactory, visual and mechanical sensory systems has been explored in many organisms in the context of courtship. In this study we have quantified and categorized overt behavioral and electric displays (SPI patterns) emitted during courtship in B. brachyistius. The variation differences of SPIs between sexes and individuals affect the actual broadcast, and by implication, the transmitted message. Furthermore, from this study and the few other reported studies of mormyrid courtship, we already see a broad range of complexity with respect to behavioral and electrical displays. The extent to which this range could be explained by ecological, evolutionary, physiological or phylogenetic constraints is unknown. Without knowledge of the overt behaviors and associated electrical activity during courtship, we cannot begin to explore issues such as mutual or reciprocal electrical signaling between sexes, sexual selection, honest electrical signals, and the neural mechanisms underlying SPI pattern generation and interpretation.
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Acknowledgments |
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Footnotes |
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References |
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