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On the Diversity of Electric Signals in a Community of Mormyrid Electric Fish in WestAfricaAuthor(s): Carl D. HopkinsSource: American Zoologist, Vol. 21, No. 1 (1981), pp. 211-222Published by: Oxford University PressStable URL: http://www.jstor.org/stable/3882722Accessed: 09/01/2009 15:08

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Amer. Zool., 21:211-222 (1981)

On the Diversity of Electric Signals in a Community of

Mormyrid Electric Fish in West Africa1

Carl D. Hopkins

Department of Ecology and Behavioral Biology, University of Minnesota, Minneapolis, Minnesota 55455, and Laboratoire d'Ecologie Equatoriale (C.N.R.S.), Makokou, Gabon

Synopsis. Communication through electric discharges is a rich and varied modality of social communication among mormyrid fishes of West Africa. Field studies permitted an analysis of the electric signals of over 20 species of Mormyridae living sympatrically in and near the Ivindo River of Gabon. Electric discharges can be classified according to their waveforms and can be shown to be species-specific in many cases. The waveform of the discharge is a signature which is a carrier for social communication signals. The paper asks: "Why is the signature, or carrier, adaptive?" An analysis points to competitive and cooperative forces in the evolution of electrical waveforms, not physical or habitat forces. Competition between species, as well as mutualistic interactions, appear important in ex- plaining how electrical signatures are adaptive for: 1) channel privacy (noise immunity); 2) unique signals for species recognition; and 3) electrolocation signals less vulnerable to jamming.

Introduction

Electric communication, like other bet? ter known communication modalities, is a rich and varied form of social communi? cation which is used by a few groups of freshwater teleost fishes from the new- and old-world tropics. Comparative field stud? ies of African mormyrid fishes, and also South American gymnotoid fishes, have revealed a startling diversity of types of electric signals (Hopkins, 1974). This di?

versity, and the reasons for its evolution, will be the subject of this paper.

Comparative studies of signal diversity from other sensory modalities used in communication have always presented a

challenge, as biologists have attempted to find adaptive patterns in communication

signal structure. Numerous hypotheses have been proposed; a few classic studies should be mentioned: Wilson and Bos- sert's (1963) study of diffusibility of olfac?

tory signals, Marler's (1959) analysis of

convergence in bird alarm calls, and Hail- man's (1977) review of visual signals.

Throughout this paper I will emphasize two important types of selective influences on electric signals in mormyrid fishes: those which I find to be purely ecological?

1 From the Symposium on Social Signals?Compar? ative and Endocrine Aspects presented at the Annual Meeting of the American Society of Zoologists, 27- 30 December 1979, at Tampa, Florida.

that is arising due to some physical con- straint by the habitat within which the

signalling organism is found; and other influences which are cooperative or competi? tive?that is, arising because of the pres? ence of another signaling organism in the same habitat.

Both the Mormyridae and the Gymno- toidei produce Electric Organ Discharges (EODs) in specialized organs, usually in their tails (review in Bennett, 1971), and

perceive electric signals through special? ized, lateral-line-derived electroreceptors in their skin (review in Fessard, 1974). EOD signals are employed in electric com?

munication, in which one fish produces an electric signal which evokes a change in behavior of a second individual (review*in Hopkins, 1977), and in electro-location, where one fish senses distortions in its own electric field caused by electrical inhomo-

geneities in its near vicinity (review in Hei-

ligenberg, 1977). Studies on the evolution of EOD signals will have to address the

adaptive significance of signal structure for these two sometimes competing behav? ioral roles.

Methods

Field site

Field studies were conducted in North- eastern Gabon (0.34?N, 12.52?E) in the Ivindo River drainage system, 10 km south of the village of Makokou. The Ivindo Riv-

211

212 Carl D. Hopkins

er there is approximately 300 m in width, is approximately 10 m deep in the deepest point, and fluctuates over 4 m in depth from minimum to maximum, twice per year, in response to approximately 1,750 mm of rainfall distributed over two sea? sons (Jackson, 1961). From the study site, which is dense primary forest within a protected forest reserve established by the

C.N.R.S., the Ivindo River flows west to? ward the Ogowe River, and then to the Atlantic Coast. Many of the fish are en- demic to this region and north to Camer- oon. Poll (1957) refers to this geographical region as the Cameroon-Gabon ichtio- faunal province; Roberts (1975) calls it the Lower-Guinea Province. Research spanned three seasons: August 1975; August through December 1976; and October

through December 1979.

Fish detection and localization

An audio amplifier served as a fish detector for mormyrids. I used a three Ag/ AgCl-wire electrode probe in which the

ground wire was centered between the

positive and negative wires. The two active electrodes were separated by 20 cm. Wider

spacing increased environmental noise from lightning (see Hopkins, 1973, 19806), without significantly increasing signal am-

plitude from fish. A horizontal orientation of the electrodes gave best results. The electrodes were connected via two-conduc- tor shielded cable to the input of an operational-amplifier-based audio-frequency amplifier. The first stage was a direct input to a pair of Teledyne-Philbrick type 1021 FET operational amplifiers. Low and high pass filters were set to 3 Hz and 30 kHz. A speaker amplifier stage followed two in? termediate amplification stages so that fish could be heard on an audio monitor. Al?

though the sounds of fish discharges were

similar, shorter pulses could be discrimi- nated from the longer ones and rhythmic qualities of pulse trains were discriminat- ed. A portable oscilloscope (Sony-Tektro- nix Type 322) proved essential for field observations of electric organ discharges. Fish could be localized to within centime- ters by slowly moving the electrode probe back and forth while listening on the audio

monitor. Fish sequestered far under the stream banks were less easily localized and the accuracy diminished to tens of centi- meters.

Fish capture and identification Three methods were used to capture

fish: baskets baited with earthworms served as traps when placed at the bottom of the Ivindo River at night; fish detected in small streams with the fish detector, were captured with a 1 m diameter, 3 mm mesh hoop net; and some very small streams were dammed and drained of all water in order to capture fish. Similar methods are used by local fisher per sons, as described in Mathes (1964).

The mormyrids of the Ivindo region are known incompletely. New genera and

species remain to be described, thus some identifications are tentative. Previous collections in this region by Jaques Gery in 1964 and by Armin Heymer in 1975 have resulted in several new species and genera (Taverne and Gery, 1968, 1975; Taverne et al, 1976, 1977). Specimens have been

kindly identified tentatively by Dr. F. E.

Thys van den Audenaerde and Dr. Louis Taverne of the Musee Royal de L'Afrique Centrale in Tervuren, Belgium, and are

deposed there (collection number 77-41-p- 1 to 91).

Recording EODs

Because the waveform of the EOD of

mormyrids is subject to variation as envi? ronmental temperature and conductivity change (Harder et al, 1964; Bell et al, 1976), recording conditions were stan? dardized. Fish were transported to the lab?

oratory for recording as soon after capture as possible. They were maintained in their own home water at 22 to 25?C. The re?

cording chamber was a 7 x 40 cm Plexi-

glas aquarium outfitted with Ag/AgCl electrodes on each end, and with a dark plastic tube for hiding. The signal from the electrodes passed directly into an oscilloscope for photographing or, if too feeble,

through a DC amplifier (Princeton Ap- plied Research 113) and then to an oscil?

loscope. I also used a magnetic tape recorder (Nagra IV SJ) for recording the

Electric Signal Diversity in Mormyrids 213

EOD after amplification. The recorder has a frequency response of 20 Hz to 35 kHz

at 37 cm/sec. The polarity of the EOD was noted with respect to head position.

Electrophysiological methods

I recorded from neurons in the lateral line nerve while applying stimuli to the water around the fish. Electrophysiological techniques are described in Hopkins and

Heiligenberg (1978).

Results and Discussion

Diversity ofEODS Successive EODS from a motionless in?

dividual were indistinguishable on the os-

cilloscope: they superimposed exactly. EODS recorded from different individuals differed. They were compared by: 1) digitizing the tape-recorded EOD at 50 kHz

using a PDP 11/34 computer, 2) scaling the

peak-to-peak amplitude to a standard val?

ue, 3) aligning the time axis of the pulse around a time reference located midway between the positive peak and the negative peak of the waveform, 4) scaling the ver? tical off set to the same value, and 5) plot- ting the EODs on top of one another. The results of superposition of 8 EODs from different individuals of Brienomyrus bra-

chyistius (l bp.f are shown in Figure 1. This

figure illustrates the general observation that EODs show minor variation in wave-

shape, and in duration (in this case dura- tions range from 1.5 msec to 2.0 msec). Variation for other species will be illus? trated using power spectra below.

Representative EODs of 23 species of

mormyrid fishes from the Ivindo River and surrounding streams are shown in

Figure 2. All EODs are plotted on the same time scale, with head-positivity upward,

2 Because the identifications of mormyrids from Gabon are tentative, and because the collections un- doubtedly involve some new species, they are given temporary names here. One group of species resem- bles Brienomyrus brachyistius morphologically, but can be shown to be four distinct species on the basis of the EODs. These four species are called: B. brachyis? tius (mp) for "monophasic EOD"; B. brachyistius (bp) for "biphasic EOD"; B. brachyistius (l. bp.) for "long biphasic"; and B. brachyistius (tp) for "triphasic."

J\

Brienomyrus hrachyistius (1. bp. ) (N=8)

r

Fig. 1. Superimposed oscilloscope tracings of Elec? tric Organ Discharges (EODs) of eight individual mormyrids of the same species. Each EOD is digitized, scaled to the same peak-to-peak amplitude, and positioned on the time axis so that the mid-points between the two peaks superimpose.

with the same peak to peak amplitude. EODs are arranged according to duration. EOD waveforms are remarkably diverse across species. In Gabon, I soon learned to

identify with approximately 80% accuracy the species of mormyrid by observing the waveform of the discharge alone. In some

species, such as Petrocephalus simus, P. stuhl-

mani, and M. paucisquamatus, intra-individual variation in EODs exceeded intra-

species variation. The following features were used as key characteristics in field identification of EODs: total duration of

EOD; number of peaks to the waveform; relative amplitudes of each peak; presence or absence of inflection points in the wave?

form, or sudden changes in slope of the

wave; and the polarity of the wave. Figure 2 show two cases where females and males differed in their EODs (Stomatorhinus corneti and Brienomyrus brachyistius (tp)), and two other cases where juveniles and adults showed a marked change in EOD as adults. One may conclude from Figure 2 that EODS of mormyrids are complex and diverse "signatures" showing considerable

diversity in duration and in wave-shape. We may speculate on the forces that

shape the evolution of EOD signatures for

mormyrids, and it is convenient to consid- er in turn two types of influences: the hab?

itat, and the social environment. In other

words, EODs may be adapted to features of the habitat in which the fish are living or

they may be adapted to cooperative or

competitive roles resulting from habitual associations with other organisms.

Habitat factors The transmission of an electrical signal

may be affected by physical factors in the

214 Carl D. Hopkins

MORMYRIDAE IVINDO RIVER, GABON

t

r

t

t-

1-

f-

\

Stomatorhinus corneti 9

Pollimyrus kingsleyae

Petrocephalus simus

Petrocephalus stuh/mani

Marcusenius paucisquamatus

Ivindomyrus opdenboschi (juv.)

\

Stomatorhinus corneti cf

Hippopotamyrus batesii (r.p.)

Boulengeromyrus knoepffleri

Hippopotamyrus batesii (tp.)

Brienomyrus brachyistius (mp)

Hippopotamyrus batesii (b bp.J

Brienomyrus brachyistius (tp.)y

Brienomyrus brachyistius (bp)

isichthys henryi (juv.)

Ivindomyrus opdenboschi (ad)

Hippopotamyrus castor (bp)

Hippopotamyrus castor (mp)

Mormyrops zanclirostris

Hippopotamyrus sp. (r.p)

Brienomyrus curvifrons

Brienomyrus brachyistius (I. bp.)

Brienomyrus brachyistius (tp.) c

Marcusenius conicephalus

Isichthys henryi (ad.)

Paramormyrops gabonensis

-j-1?"-1-1-h 4 6

time (mseo 8 10


environment such as water depth, conduc-

tivity, presence or absence of vegetation, quality and quantity of obstacles, pH, etc, and signals may be affected differentially. Certain habitats could act as simple filters for electric signals. However, Hopkins and

Heiligenberg (1978) measured the rate of

signal attenuation around constant-cur-

rent, sinusoidal dipole sources at 100 Hz, 1000 Hz, and 10,000 Hz, in a variety of natural habitats. The rate of attenuation of electric fields varied from the inverse 2.8

power of distance, to the inverse 3.3 pow? er, when comparing open water 1 m deep, with water 20 cm deep, with habitats with dense sedge or fanwort mats. However, all sinusoidal frequencies were attenuated equally within each habitat. Thus, to the extent that the electric fish approximates a current

source, in the absence of any specific fil-

tering effect, no EOD should have an ad?

vantage over another in terms of signal attenuation rate.

The presence of background noise in the environment from non-biological sources could influence the evolution of EODs of mormyrids. Some EODs, for ex?

ample, could contrast with the background noise and thus be detectable at lower am-

plitudes and at longer distances; others could blend with the noise and be incon-

spicuous. The analysis of background elec? trical noise from non-biological sources,

principally caused by atmospheric lightning, shows a decided spectral energy peak to noise at about 2 kHz, and a gap at 1.0 to 1.5 kHz (Hopkins, 1973, 1980*). It is not known if different habitats are affect? ed differently by ambient noise, thereby favoring one type of EOD over another, nor is any data available which indicates whether one species is more or less con-

spicuous than another in the presence of natural ambient noise conditions.

Social factors

famming. The EOD of a species may have evolved because it is adaptive in some social or competitive context. One well- documented influence, called jamming, occurs when the EOD of one electric fish contaminates the electrolocation abilities of a second. Heiligenberg (1975) demon? strated that one mormyrid, Brienomyrus niger, performed worse at electrolocation when external electrical pulses repeatedly coincided in time with the fish's EOD. Non-coincident pulses were inconsequen- tial. Therefore, for two fish close enough to each other in space to cause jamming, the deterioration in electrolocation will be

proportional to the probability of EOD co-

incidences, which will be approximately fx X di X f2 X d2. Here, ix and di are the mean repetition frequency (EODs per sec?

ond), and mean duration of each EOD, for the ith fish. Two fish of the same species could benefit from having reduced chances of coincident EODs by lowering their dis?

charge frequencies, or by reducing the EOD duration. Lowering the discharge frequency could be deleterious to tempo? ral acuity in electrolocation, however, whereas reduction of the EOD duration would not. This effect, if present, would

only be apparent in those species which

aggregated close enough to cause jam? ming, of course.

I censused two small streams in Gabon over a one month period in 1975 and five months in 1976; and in one 100 m plot and one 300 m plot mapped the position of every discharging mormyrid. By carry- ing the portable oscilloscope in the field, I could identify the discharging fish in most cases to species. Fish which have short duration EODs are found either

closely or widely spaced, whereas those

Fig. 2. Oscilloscope tracings of EODs of mormyrid fishes from the Ivindo River and surrounding streams in Gabon, digitized from photographs. All waveforms are oriented with the head-positivity upward and are arranged according to duration. Species identifications are tentative. Abbreviations refer to species complexes distinguishable by EOD characteristics: mp = monophasic, bp = biphasic, tp = triphasic, 1. bp. = long biphasic, b. bp. = brief biphasic, rp = reverse polarity (from Hopkins, 1980).

216

StonrKriorNnus cometi

Carl D. Hopkins

es "\(i

Fig. 3. EOD, Power Spectrum, and Phase Spectrum of three mormyrids from Gabon. Fourier analysis is

accomplished by digitizing the EOD on a digital computer from a magnetic tape record, and then subjecting the record to FFT analysis. Digitizing rate = 50 kHz (drawings by Vera Wong).

with long duration EODs are usually widely separated from members of their own species (Hopkins, 1980). Also, fish which are found close to conspecifics al-

ways have short duration EODs.

Schooling. Certain species such as Petro?

cephalus simus, P. stuhlmani, and juvenile M.

paucisquamatus and /. opdenboschi, school to?

gether. All four species are found in dense

aggregations under root mats or along the

edge of the river in dense floating vege? tation. When using a hoop net in a stream, I often captured all four species in one

scoop. In aquaria all four species live

peacefully together and do not, like many other species of mormyrids from Gabon, bite each other on the sides and remove scales. It is noteworthy that all four species produce identical EODs (Fig. 2). The

mixed-species school may be adaptive for

increasing feeding efficiency, predator avoidance, or some other reason. The sim?

ilarity of the EODs may have resulted from the following three factors: 1) similarity in

EODs may help promote group cohesion;

2) it may reduce individual conspicuous- ness to electrically perceptive predators; and 3) these simple short EODs may result from selection for reduced jamming, as discussed in the previous section. Thus, there may be a tendency for mormyrids living in the same habitat and schooling together, to converge upon the same EOD

Channel privacy. Social signaling will be facilitated if signals are easily discriminat- ed from noise, as discussed for ambient

non-biological noise sources above. Ob-

viously, one important noise source is from other electric fish in the immediate envi?

ronment, which when tens or hundreds

aggregate in the same area, produce an electrical cacophony where communica? tion must be exceedingly difficult. Signal- ers co-existing with a mixture of species may opt for a signal which can be en- hanced relative to the background roar by simple filtering on the part of recipients.


Co-existing species may therefore diverge in their signal structure to enable a degree of privacy or noise immunity. Filtering ac?

cording to spectral frequency is a funda- mental process in other electroreceptors (Scheich et al, 1973; Bastian, 1976; Hop- kins, 1976; Hopkins and Heiligenberg, 1978) thus it is a primary candidate for first-order filtering. Tuning to a narrow

part of the frequency spectrum is also characteristic of auditory receptors.

Representing the EOD in the frequency domain. I hoped to put the EOD signatures of Ivindo mormyrids into a framework which would permit analysis of channel

privacy by subjecting each to Fourier Anal?

ysis. Power and phase spectra of three EOD signatures are shown in Figure 5. EODs were digitized at 50 kHz and sub?

jected to Fast Fourier .Analysis using a PDP-11/34 computer and the DEC pro- gram, Sparta. The resulting power and

phase spectra show some of the following relationships to their time-domain repre- sentations:

1) As expected, the duration of the EOD is inversely related to the peak of the

power spectrum. Stomatorhinus corneti has a 150 to 200 ^tsec EOD, making it the shortest duration seen in this study. The power spectrum peaks at the high? est frequency (10 kHz or more). Para-

mormyrops gabonensis has one of the

longest duration pulses (8 msec) and the power spectrum is one of the lowest

frequencies (200 Hz). 2) Nearly monophasic EODs such as B.

brachyistius (mp), show a peak energy at or near 0 Hz, or D.C.

3) Spectra of these brief, transient EODs are very broad compared to the spectra of EODs of wave species (see Heiligen? berg, 1977).

4) While fish with simple biphasic EODs had simple monotonically increasing and then decreasing power spectra (i.e., B. brachyistius (bp)), while those with multiphasic EODs usually had

multi-peaked power spectra (i.e., Sto?

matorhinus). 5) Phase spectra of EODs with single-

peaked power spectra vary continu-

ously with frequency. Phase spectra of

multi-peaked power spectra tend to have discontinuities.

The peak powers of EODs of Ivindo

mormyrids are iilustrated in Figure 4. Each dot represents the peak of the power spectrum of one individual of a species. Shading delimits one standard deviation of the mean for the species, and the white bar shows the band width of the EOD 10 dB down from the peak power. Clearly, Fig? ure 4 shows that the overlap between

species is large. Nevertheless, the 5-6 oc- tave range of peak powers for this com?

munity of fish is impressive. For the channel privacy hypothesis to be

valid, recipients must be able to filter in-

coming stimuli so as to enhance EODs of

significance compared to others of no con-

sequence. This can be studied electrophys- iologically for mormyrids.

Stimulus fltering by electroreceptors. I re-

port on studies of electroreceptors of two

species of mormyrids, Brienomyrus brachyis? tius (bp) and Pollimyrus isidori, both im-

ported from Nigeria by commercial trop? ical fish importers. Two rnethods were used to record from single receptors. In the first, I used glass microelectrodes to record from single fibers in the dorsal branch of the posterior lateral line nerve while applying stimuli homogeneously across the fish's body through two elec? trodes in the bath (for further details, see

Hopkins and Heiligenberg, 1978). In the

second, a fire-polished glass capillary, 1 mm in diameter, with a silver/silver chlo? ride electrode inside, was connected to an active bridge amplifier (WPI 707) so that the receptor potentials from Knollenorgan receptors on the surface of the skin could be recorded while passing current through the probe to stimulate them (the method is described in Bennett, 1965). In the first

method, the fish are immobilized with cu-

rare, in the second, the fish are awake and

only gently restrained.

Figure 5 illustrates tuning curves for tuberous electroreceptors in the lateral line nerve of B. brachyistius (bp). Tuning curves show the threshold for evoking spikes in the primary afferent nerve, measured in

218 Carl D. Hopkins

Iio

vmm

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~mr-

WZ\

wm-

"i?i 111? ifi i?i 1111 ii

10 100 imi|-1 i i i in

1k

3 S. corneti

Rsimus

P.stuhlmani

I. opdeboschi

H. batesii (b. bp)

P. kingsleyae

M. paucisquamatus

H. batesii (tp)

H. batesii (rp)

B. brachyistius (bp)

B knoepffleri

H. castor (bp)

M. zanclirostris

B. brachyistius (tp)

B. curvifrons

H. castor (mp)

B. brachyistius (l.bp)

I. henryi

P. gabonensis

B. brachyistius (mp)

M.conicephalus

i i 11-

10 kHz

Frequency


terms of the electric field strength external to the fish, as a function of the sinusoidal stimulus frequency. Stimuli are delivered in tone bursts 100 msec in duration, and the response criterion is a just-noticeable increase in spontaneous activity, if any. Two types of electroreceptors apparent in the figure are known as Knollenorgans (solid circles) and Mormyromasts (solid lines) (review of receptor types in Hopkins, 1980a). Knollenorgans are recognized by the following criteria: they have low thresholds compared to mormyromasts, they fire only one spike when stimulated with a 0.1 msec square wave, the latency is fixed in response to square waves rather than showing wide variation, and the re?

ceptor "pore" produces a local all-or-none

receptor potential. Knollenorgan recep? tors are tuned broadly in this species and there is a good match between the tuning curve and the power spectrum of the

species' EOD (above). Mormyromast re?

ceptors are also tuned broadly. They have

higher thresholds; the tuning curve is not well matched to the power spectrum of the EOD recorded at a distance. Individual

mormyromasts vary in the best frequency of the tuning. It is not known whether

Mormyromasts might be tuned to the local EOD field at the skin. Mormyromasts are

probably not involved in social communi?

cation, but rather in electrolocation (re? view in Bell, 1979). Knollenorgan recep? tors are used exclusively in communication

(Bell, 1979; Hopkins, 1980a).

Tuning curves for Knollenorgans from an additional species, Pollimyrus isidori, are shown in Figure 6. These curves were gen? erated using the second method in which

receptor potentials are recorded from the

receptor pore. Tuning curves cannot be calibrated with respect to an external elec? tric field, thus relative thresholds are iilus? trated. This figure again illustrates that

.1 1 10 Stimulus frequency (kHZ)

Fig. 5. Tuning curves of tuberous electroreceptors of B. brachyistius (bp). Threshold electric fields are plotted as a function of sinusoidal stimulus frequen? cy. The EOD of the fish is shown in the upper left, its power spectrum in the upper right. Knollenorgans are lines through solid circles and mormyromast re? ceptors are solid lines.

there is close correspondence between the

power spectrum of the EOD and the best

frequency of the Knollenorgan tuning curve. Pollimyrus is of added interest be? cause the tuning curves have best frequen? cies as high as 18 kHz which makes them tuned higher than any other previously reported electroreceptor.

Comparative studies of Knollenorgan tuning are continuing but it is already clear that Knollenorgan receptors are primarily responsive to the frequency range within which the EOD power spectrum peaks. Both criteria for the filtering and privacy hypothesis are thus shown to be valid?in? dividual EODs diverge on the basis of fre?

quency representation, and species differ in the frequency ranges to which they are

Fig. 4. Species differences in EOD power spectra for mormyrids from the Ivindo region. EODs are grouped by species; each dot represents the peak of the power spectrum of one individual, the shaded area shows one standard deviation in the peak power for the species, and the rectangular area in white show the average bandwidth of the power spectra, 10 dB down from the peak power. The vertical height of the box is a measure of the number of specimens examined (from Hopkins, 1980).

220 Carl D. Hopkins

I Tuning Curves of Knollenorgi

EOD Power Spectrum of EOD

l.i i Imil i i i Iniil

Fig. 6. Three tuning curves of Knollenorgans for Pollimyrus isidori. Threshold voltages are measured in decibels relative to the most sensitive frequency value. EOD and power spectra as in Figure 5.

sensitive. Much further comparative work needs to be done, however, to tell whether an individual is truly on a private channel of communication. Because of the broad- band nature of the signal and the width of the receptor filter, potential exists for considerable overlap between species.

EOD diversity and recognition The diversity of EODs may result from

the obvious need for a signal which is

unique to the recipient. Whether for

species, sex, or age-class recognition, the

importance of signalling with a recogniz- able signature cannot be overlooked. The

following evidence points to the impor? tance of EODs in species- and sex-recognition in one species, Brienomyrus brachyis? tius (tp). Figure 2 shows the differences observed in the EODs of males and fe? males of this species. Males produced a tri-

phasic EOD which lasted for 1.5 to 2.0 msec in duration, compared to females which discharged at 0.8 to 1.4 msec in du? ration. These EODs are constant through? out the breeding season, thus the males can be said to have different electrical sig? natures from the females. In addition, males have distinctive pulse rhythms, and

appear to use patterns of discharges in

Rasps/

7-

6-

5-

4-

3-

2-

H

B. brachytstius(l.bp)$> (tp)$ (tp)juv (tp)o" sine

N? 13 16 10 12

4-j -VT-V VV df

Fig. 7. Results of a playback experiment testing for species recognition by Brienomyrus brachyistius (tp) males in field tests. Isolate male fish are presented with electric discharges from: B. brachyistius (l. bp.) female: B. brachyistius (tp) female, juvenile, and male; and single periods of a sinewave at 1 kHz triggered by the EOD of a B. brachyistius (tp) female. The male responds to these playback signals with rasp dis? charges as he "hears" the EOD of the female of his own species, but not when he hears a male, nor when he hears a female of another species. In this histo- gram, the ordinate is the increase in numbers of rasps during the playback compared to the control period. The rhythm of the EOD is not sufficient to evoke a response, as he does not respond to single-period sine waves when they are given at the female's rhythm.

their reproductive or courtship behavior. One such pattern or display is called a

"rasp" which consists of 20 to 30 EODs in a series delivered at frequencies as high as 150 Hz which is then followed by several hundreds of milliseconds of silence. Rasps are produced by males during the breed?

ing season in Gabon when in the presence of females. They are not heard from iso? lated males, nor from females in the pres? ence of other females or juveniles. Rasps are distinctive to human observers and can be counted during observation periods in


the field as a response to artificial stimu? lation. Results of one series of experiments are shown in Figure 7. Two isolated male B. brachyistius (tp) were used in these ex?

periments. Stimuli were presented to these

males through wire electrodes which were

placed near the habitual hiding place of

the male, at night when the fish were most active. The electrodes were connected to the output of an amplifier which sensed the EOD of a captive fish held in isolation. The signatures of the stimulus fishes are shown in the figure. In this experiment, a

period of 2 minutes preceded each test

during which rasps were counted; this was followed by the stimulus period also of 2 min. The increase in numbers of rasps per minute from the male are shown in Figure 7.

The results indicate that rasp responses are evoked from males when stimuli orig- inated from females of his own species, but are evoked significantly less when origi- nating from males, or females of other

species such as B. brachyistius (l. bp.). When

captive female B. brachyistius (tp) were used to trigger a single period of a sine wave that imitated the peak power of the female's EOD spectrum, the males did not

give rasp responses. Thus, the EOD wave? form is strongly implicated in evoking the

rasp response, not merely the rhymthmic qualities of the EOD. No systematic differ? ences were detected in the number of re?

sponses to females and to juveniles. The results of this experiment are strongly suggestive, yet not conclusive, of an im?

portant additional role for the diversity of EODs in a community of mormyrids, i.e., for signaler identification. This problem will provide a focus for additional work.

ACKNOWLEDGMENTS

This research has been supported by the National Institute of Mental Health

(MH26140); the Research and Exploration Division of the National Geographic Soci?

ety; and the Graduate School, Office of International Programs, and College of

Biological Sciences of the University of Minnesota. I thank Dr. Andre Brosset of the C.N.R.S. (France) for the generous invitation to work at the Laboratoire

d'Ecologie Equatoriale in Makokou, Ga? bon. Robert and Karen Askins, Kathy Hopkins, Georges and Sylvie Michaloud all helped in many ways with the field work. I thank Dany Newbauer and Robert Lewis for technical assistance, and Dr. T. H. Bullock for an invitation to do some

electrophysiological work in his laboratory.

References

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Article Contentsp. 211p. 212p. 213p. 214p. 215p. 216p. 217p. 218p. 219p. 220p. 221p. 222

Issue Table of ContentsAmerican Zoologist, Vol. 21, No. 1 (1981), pp. i+1-316Front Matter [pp. i-109]Functional-Adaptive Analysis in SystematicsIntroduction to the Symposium: Functional-Adaptive Analysis in Systematics [p. 3]Functional-Adaptive Analysis in Evolutionary Classification [pp. 5-20]The Use of Functional and Adaptive Criteria in Phylogenetic Systematics [pp. 21-36]Functional Analysis and the Practice of the Phylogenetic Method as Reflected by Some Mammalian Studies [pp. 37-45]The Role of Functional Analysis in Phylogenetic Inference: Examples from the History of the Xiphosura [pp. 47-62]Relationships between Invertebrate Phyla Based on Functional-Mechanical Analysis of the Hydrostatic Skeleton [pp. 63-81]A Functional Approach to the Phylogeny of the Pharyngognath Teleosts [pp. 83-101]Summary and Comment [pp. 103-108]

Social Signals: Comparative and Endocrine AspectsSocial Signals: An Overview [pp. 111-116]Ontogeny of Ultrasonic and Locomotor Responses to Nest Odors in Rodents [pp. 117-128]The Hormonal Control of Ultrasonic Communication in Rodents [pp. 129-142]Scent Marking, Sexual Behavior and Aggression in Male Gerbils: Comparative Analysis of Endocrine Control [pp. 143-151]Olfaction, Sexual Behavior, and the Pheromone Hypothesis in Rhesus Monkeys: A Critique [pp. 153-164]Sex Differences and Age Gradations in Vocalizations of Japanese and Lion-Tailed Monkeys (Macaca fuscata and Macaca silenus) [pp. 165-183]Reproductive Behavior in the Rhesus Monkey: Social and Endocrine Variables [pp. 185-195]Agonistic Encounters among Male Elephant Seals: Frequency, Context, and the Role of Female Preference [pp. 197-209]On the Diversity of Electric Signals in a Community of Mormyrid Electric Fish in West Africa [pp. 211-222]Social Modulation of Circulating Hormone Levels in the Male [pp. 223-231]Logical Levels of Steroid Hormone Action in the Control of Vertebrate Behavior [pp. 233-242]Social Control of the Ovarian Cycle and the Function of Estrous Synchrony [pp. 243-256]Hormone Specificity, Androgen Metabolism, and Social Behavior [pp. 257-271]Function and Causation of Social Signals in Lizards [pp. 273-294]Physiology of Rana pipiens Reproductive Behavior: A Proposed Mechanism for Inhibition of the Release Call [pp. 295-304]Hormonal Regulation of Female Reproductive Behavior in Fish [pp. 305-316]

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On the Diversity of Electric Signals in a Community of Mormyrid …pages.nbb.cornell.edu/neurobio/Hopkins/PDFS/1981 On the... · 2014. 10. 27. · Carl D. Hopkins Department of Ecology