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Electric in : Certain species of fish produce electric signals that are used for identification, aggregation, and dispersal Author(s): Carl D. Hopkins Reviewed work(s): Source: American Scientist, Vol. 62, No. 4 (July-August 1974), pp. 426-437 Published by: Sigma Xi, The Scientific Research Society Stable URL: http://www.jstor.org/stable/27844991 . Accessed: 21/04/2012 09:46

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http://www.jstor.org CarlD.Hopkins Electric Commiinication in Fish

Certain species offish produce electric signals that are used for identification, aggregation, and dispersal

Communication is a process by which the behavior of one individu al affects the behavior of another. It is not merely a series of responses to stimuli, but rather a relationship that is set up by the transmission of a stimulus and the evocation of a response (Cherry 1961; Altmann 1967). Yet we do not think of a predator's responses to the actions of its prey as communication; we restrict our view to those relation ships in which the transmission of the stimulus and the elicitation of a response are mutually beneficial, in the evolutionary , to both par ticipants. As observers of , we depend heavily upon changes in the recipient's behavior?shown ei ther by a specific response or by a change in the probability of differ ent behaviors?as an indication of the presence of communication.

Animals respond to many channels of stimuli: light, sound, touch, and

Carl Douglas Hopkins is Assistant Professor of Ecology and Behavioral Biology at the University ofMinnesota. After receiving his doctorate from Rockefeller University in 1972, he spent one year as a postdoctoral Figure 1. Gymnarchus niloticus is a well fellow at the University of California, San known found in many rivers in Diego. His current research deals with phys West Africa. (Photo courtesy of H. W. Liss iological properties of electroreceptors, ecol mann.) ogical and behavioral aspects of electric communication, and ecology and social be chemicals are the most widespread tion systems in general, including havior animals. The work here of reported and best known for purposes of possible relationships between an has profited from the extensive interest, communication. The use of the 's ecology and its social be help, and criticism of Peter Marler and col electrical is known for havior and between its leagues at Rockefeller University and Theo modality physiology dore H. Bullock at UCSD. The author is only a few species of aquatic ani and the choice of a modality of to also deeply indebted Joseph Bastian, mals; it is well developed in several communication. Curtis Bell, Carol Gobar, Walter Heiligen divergent groups of berg, Erik Knudsen, and Peter Moller for es from South America and Africa Two of freshwater help and comments during the preparation principal groups commu of the manuscript. The research presented and may be developed in several have well-developed here was supported by grants to P. Marler species ofmarine elasmobranchs. In nication systems using electrical from NSF and to T. H. Bullock from spite of its rarity, the study of this stimuli?the gymnotid fishes of USPHS. Address: Department of Ecology mode of com South America and the mormyri and Behavioral Biology, James Ford Bell relatively unexplored form fishes of Africa. The Museum of Natural History, University of munication may give us some feel Gymno Minnesota, Minneapolis, MN 55455. ing for the of communica toidei are a characoid-related sub

426 American Scientist, Volume 62 order of Cypriniformes consisting of four closely related families (Greenwood et al. 1966), represent ed by 60 to 80 species, including the well-known electric . The Mormyriformes (superorder Osteo glossomorpha) have also evolved current-generating abilities. There may be up to 200 species ofmormy rids (fam. ) and one species of Gymnarchus (fam. Gym narchidae) making up this group. Other electric fishes such as the electric (Malaptururidae), the electric rays (Torpedinidae), the electric skates (Rajidae), and the stargazers (Uranoscopidae) may also use electrical stimuli for com munication, but these species have received little attention. (For gen eral reviews dealing with electric fish, see Lissmann 1958, 1963; Ben nett 1971a and b; Bullock 1973.) Sending and receiving signals Electric communication requires special physiological "hardware" for both the production and the re ception of electric signals. Electric currents are generated in organs that are similar in structure to ei ther muscle tissue (Bennett 1971a) or nerve tissue (Waxman et al. 1972; Couceiro and de Almeida 1961). Muscle-derived electric or gans are the most common type. 2. Electric out in all to a distant circular electrode. Measure Large multinucleated cells or elec Figure signals spread directions, but their range is restricted. ments were made in water 1 m deep (con trocytes (Bennett 1971a) which = X Here lines of peak-to-peak equipotential ductivity 2.6 10"2 mho/m). (Data lack contractile elements are orga surround an Eigenmannia virescens 18.6 cm courtesy of E. I. Knudsen.) nized into long columns in the tail long. The values indicate potential referred region to make up the of most gymnotids and electrocytes summate ter produce a tuberous (see review in Bennett mormyrids. Each electrocyte is in relatively large voltage. In some 1971b; Bullock 1973). All known nervated by a separate spinal elec electric fish current generated in ampullary electroreceptors respond tromotor neuron. A synapse, which this manner is sufficient to shock to low-frequency electrical stimuli appears to be acetylcholine-mediat prey or predators. However, the (less than 50 Hz) with modulations ed, forms the link between the neu discharge of most species?only a in the discharge frequency. All tub rons and the electrically excitable fraction of a volt during the peak of erous electroreceptors adapt rapidly cells of the electric organ. the discharge?is employed in the to sustained electric currents detection of objects and in commu through the receptor and respond Neurally derived electric organs are nication. best to higher-frequency stimuli found only in the gymnotid family (greater than 50 Hz). Apteronotidae (Sternarchidae). In Electric signals are perceived as members of this group, a large bun current flowing through specialized The weak electric signals emitted dle of myelinated nerve fibers electroreceptor organs embedded in by an electric fish can be detected or emerges from the spinal cord and the fish's skin. Although electrore with two metal carbon electrodes near runs along the side of the fish into ceptors almost certainly evolved placed in the water the fish. its tail to form the electric organ. separately in the Mormyriformes The signal is amplified with an or There are no intervening synapses. (Africa) and in the Gymnotoidei dinary high-gain audio amplifier (South America), there is remark and passed through a loudspeaker or During the synchronous discharge able similarity in receptor morphol audio monitor. Amplified signals of all the electrocytes of the electric ogy between the two groups. Both can be recorded on magnetic tape organ, the potentials generated groups have two general classes of for analysis on an oscilloscope, a across the membranes of individual electroreceptors?ampullary and sound spectrograph, or computer.

1974 July-August 427 Both laboratory and field studies proximately dipole-shaped field have contributed to our knowledge (Fig. 2) that is broadcast in all di of electric communication. Whereas rections (Hockett 1960), much like laboratory studies have concentrat the loud territorial calls given by ed on the role of electric signals in many species of or . agonistic behavior?maintaining Attempts to focus the signal by territories or dominance relation bending the body one way or an ships?field studies have explored other probably do not result in a other uses, such as in reproductive significant narrowing of the beam behavior. Early suggestions about of communication. the possible role of electric dis charges in social communication re The distance of transmission of sulted from Lissmann's (1958) field electric signals is short?probably work on the Black Volta River in on the order of 1 to 10 meters. Esti northern Ghana and subsequent mates of the maximum distance of behavioral experiments in the labo communication vary. Using mea ratory using Gymharchus niloticus surements of equipotential lines (Fig. 1). Gymnotids and mormyrids and of conditioned response thresh are nocturnal, and thus most stud olds, Granath and his co-workers ies have been conducted at night or (1968) estimated the maximum dis in a darkened laboratory. The tance of signal reception at 3 m for albi views on the evolution of electric " l?t I Apteronotus (Sternarchus) communication presented here have ^ .'2 5 10 SO frons. Using a similar approach, benefited from field experience in 500r Knudsen (pers. comm.) estimates Guyana, South America. the threshold field strength of Ei genmannia virescens to occur at be The communication tween 25 cm and 200 cm, depend medium ing upon the size of the individual sending the signal, the angular ori Electric currents generated by one entation of the sender with respect fish's electric organ are picked up to the recipient, the electrical con by the electroreceptors of another ductivity of the water, and the individual. It is important at this presence of nonconducting surfaces point to understand some of the near the signaler that might com peculiarities of current flow in press the field. In the mormyrid water that endow this sensory mod Gnathonemus petersii, consistent ality with special properties when it behavioral responses were elicited is used for communication. by the presence of a discharging con specific at a maximum distance of Electric signals are conducted very 30 cm (Moller and Bauer 1973; rapidly in water. Conduction veloc Russell, Myers, and Bell 1974). ity is determined by the conductiv Figure 3. Top: The peak-to-peak potential ity of the medium and the frequen falls off according to the inverse square of Communication distances are short distance from the null of the fish for various cy of the (see Liebermann because of the severe attenuation of signal colored lines For freshwater angles; represent negative electric fields around a 1962). (conductivity values. Bottom: The amplitude of the elec dipole = x source 5 10"3 mho/m) and the low tric field strength falls off according to the (Fig. 3): the electric poten frequencies used by most electric inverse cube of the distance. Measures are of tial surrounding a perfect dipole the same as in 2. fish (1 kHz), the conduction veloci Eigenmannia Fig. (Data falls off according to the inverse courtesy of E. I. Knudsen.) ty is about 1.4 x 106 m/s. In sea square of the distance. The electric water, where the conductivity is as field, which is the driving force for high as 4 mho/m, the velocity may Although electric fish cannot rely the electric current, falls off accord be only 6 X 104 m/s. Nevertheless, upon differences in arrival times for ing to the inverse cube of distance. for biological systems, conduction signal localization, they apparently In shallow water, electric signals times resulting from velocities such are capable of directional reception, may extend farther horizontally be as these may be considered instan as indicated by right-left discrimi cause the rate of attenuation is re taneous, and in this respect the nation tasks using sinusoidal stim duced owing to vertical compres electrical modality resembles the uli with two species of gymnotids sion by the nonconducting surface visual. (Knudsen, pers. comm.). The in and bottom. stantaneous conduction time of the Noninstantaneous conduction times electrical modality contrasts Electric signals are capable of play an important role in other strongly with the chemical modal crooked-line transmission and in communication modalities. With ity, in which signals are transmit this feature are similar to both sound, for example, differences in ted very slowly, especially inwater. sound and chemical signals. Rocks, the time of arrival at the two ears stumps, or vegetation may alter the are important for spatial localiza Electric signals are transmitted shape of a fish's but do tion of sound sources (Marler 1959). from the electric organ as an ap not change the temporal character

428 American Scientist, Volume 62 Figure 4. Certain species of electric fish electric organs of Steatogenes shows the post ous traces; the three traces with arrows were show for modifying the shape of opercular organ, the submental organ, and recorded 2.5 cm rostral to the snout, 4.5 cm the electric field. Steatogenes elegans is the nerve that innervates them. (B) The os caudal to the snout, and near the tip of the one such example. It possesses accessory cilloscope tracings of monopolarly recorded tail. The greatest change in the electric field more occurs near near uro electric organs that alter the typical potentials show how the electric field is dis the and the with shape of the field produced by the tail torted?especially near the head. Colored genital . (From Bennett 1971a, organ. (A) The dissected view of the rostral lines indicate the recording sites of the vari permission.)

istics of its emission. Suspended are not specialized for communica ent responses from the recipient. particulate matter, a common im tion in the sense discussed by Alt Electric signals are diverse, and yet pediment to visual communication mann (1967) and Hockett (1960): it is possible to classify the diversi in tropical freshwater rivers and they are also employed in the de ty according to one or more param streams, does not affect electric tection of objects (Lissmann 1958; eters. The most important parame current flow. Lissmann and Machin 1958). Be ters appear to be the shape of the cause natural selection has oper electric field, the waveform of the 'Electrical emissions have rapid ated upon electric organs and re electric discharge, the discharge fade-out; once the signal is discon ceptors for both functions, we find frequency, timing patterns between tinued, it does not linger as do some compromises in their shared signals from sender and receiver, chemicals or visual marks. Because design, a major one being that elec frequency modulations, and cessa transmission of electric signals is trical emissions potentially conspic tions of the discharge. instantaneous and fade-out rapid, uous to predators are necessarily this modality seems well adapted generated continuously so that the The shape of the electric field of for sending quickly fluctuating object-sensing system can function. most gymnotids and mormyrids re messages. Communication signals sembles a slightly modified dipole that accompany fighting behavior, One final distinctive feature of the (see Fig. 2). Variations of this basic for example, tend to reflect each electrical modality is that electric shape may be due to changes in the participant's rapid changes in ag fish use their own energy to pro position of the electric organs with ressive motivation (Marier and duce signals rather than, as with in the body of the fish; such Hamilton 1966) and demand a most visual signaling mechanisms, changes occur in several species of channel with instantaneous con depending upon an external source gymnotids that possess accessory duction and rapid fade-out. of energy such as sunlight. In addi electric organs in addition to the tion to permitting signaling at more typical ones found in the tail. The electric channel of communica night, this characteristic allows the The best example is Steatogenes tion is contaminated by noise, not fish to generate a signal of suffi elegans, which has two columns of only from other nearby electric fish cient strength to overcome back electrocytes lying in grooves on ei but also from nonbiological sources, ground noise. ther side of the anteriorally posi including lightning. Lightning dis tioned genital papilla, as shown in charges are especially common in Figure 4A. These organs create a South America and Africa and are Signal diversity slight negative phase to the dis often of sufficient amplitude to be If electric communication is to charge in the head region (Fig. 4B; detected by electric fish (Hopkins serve multiple functions in the so also see Bennett 1971a). The signif 1973). cial behavior of electric fish, there icance of accessory organs is un must be a diversity of signals, known; however, Bennett has sug Electric organs and electroreceptors signs, or displays that elicit differ gested that they might increase the

1974 July-August 429 sense a acuity of the fish's ability to Tone discharges cy range that has tone discharge. objects. Species differences in the Overlap that occurs when two macrurus structure and activity of these or Sternopygus species are inactive (day) may not gans might also be important in occur when they are active. Thus, specific identification of the signal although Gymnorhamphichthys hy er at a range of several centimeters. postomus and Hypopomus artedi Eigenmannia virescens have similar frequencies during the Temporal characteristics of the day, they differ at night, thereby electric discharge appear to be an avoiding confusion. In addition, macrostomus important dimension of diversity. Sternarchorhamphus species with similar frequencies at The diversity of discharge wave night, such as Gymnorhamphi forms is shown in the oscilloscope chthys hypostomus and Rhamphi traces in Figure 5 for ten of the chthys rostratus, may never share Apteronotus albifrons most common sympatric species of the same habitat (Hopkins, diss.). gymnotids in my study area in ???I Moco-moco Creek, Guyana. Two Little is known about the discharge 5 msec general classes of discharge wave frequencies ofmormyrids that share forms are apparent immediately? the same habitat, although several tones and pulses. With tone dis species have received considerable Pulse discharges charges (also termed wave dis attention in laboratory studies. In charges), each impulse has a long Rhamphichthys rostratus general the mormyrids vary tre duration compared to the interval mendously in their discharge between impulses. With pulse dis frequencies from moment to mo charges, the impulse is brief com ment; thus identifiable frequency Gymnorhamphichthys hypostomus pared to the interval. All adults of bands may have less importance to a given species seem to have similar mormyrids than to gymnotids. In waveforms. Pulse discharges recur stead, frequency modulations and among the mormyriform fishes in timing patterns may play a more Africa (Fig. 6); Gymnarchus niloti important role in signal identifica cus is the only known species with tion. Hypopomus artedi atone discharge. 4-^ We should not overlook the possi Two sources of selection pressure bility that electric fish might use Hypopomus\r brevirostris are likely to affect the evolution of timing relationships between their discharge waveform. First, the sig own discharge and that of another some -t- 1?h naler may be recognized by Gymnotus carapo individual as a means of communi characteristic of its waveform?its cating, in a manner analogous to shape, duration, amplitude, or spa -J\r- M I I the flash-answer system that has tial features. Second, as Bennett 1msec 10 msec evolved in many species of the It is (1971a) points out, discharge Figure 5. The waveform of the electric dis (Lloyd 1966, 1971). interesting may have evolved multiple phases charge is another parameter of signal diver that the mormyrid Gnathonemus that have little or no energy in the sity. These oscilloscope tracings are from petersii responds to artificial elec the ten most common species of low-frequency or dc range so that gymnotids trical pulses or to the discharge of a in Moco-moco Creek, Guyana. The positive the electric organ does with a characteristic discharge electrode is located near the head, the nega conspecific not a stimulate low-frequency (am tive electrode near the tail. A positive signal "echo" pulse delivered after delay pullary) electroreceptors, which are is deflected upward. of 12 to 14 msec (Russell, Myers, now known to be utilized in the de and Bell 1974). As yet, there is no tection of prey, and possibly preda measure of the species specificity of tors (Kalmijn 1971; Bullock 1973; charge frequencies among the gym this echo response. Roth 1972). Multiple-phasic dis notids suggests that there is some charges may not jam a fish's own selective advantage to difference in All known species of electric fish low-frequency electroreceptors and, frequency of interpulse interval. are capable of modulating the fre in addition, they may not attract Table 1 shows the frequency ranges quency of their electric discharge. potential predators such as for twelve species of gymnotids in In those species that have been fish, which have low-frequency Moco-moco Creek. The tone fish studied, modulations result from (ampullary) but not high-frequency maintain a stable discharge fre depolarization of the large, elec (tuberous) electroreceptors. From quency both day and night, where tronically coupled cells in the pace the wide overlap in the discharge as the pulse fish have somewhat maker nucleus of the medulla waveforms among the gymnotids higher frequencies at night, when (Bennett et al. 1967; Szabo and occur (even those that sympatrical they are active. In some cases, Enger 1964). The modifications are ly, Fig. 5) and among the mormyr overlap in discharge frequency may often rather stereotyped and have ids (Fig. 6), it would appear that not result in confusion as to the been given names such as chirp, species distinctiveness is, in many identity of the signaler. For exam SID (Sudden Increase in frequency . cases, not important ple, Sternopygus macrurus is dis followed by a Decrease to the rest tinctive because it is the only ing frequency), ping, rise, burst, In contrast, the wide range of dis species in the high middle-frequen rasp, and so on. The sound spectro

430 American Scientist, Volume 62 grams in Figure 7 compare frequen cy modulations of several species of electric fish. Some of the records were obtained during aquarium ob servations of fighting behavior, some from field observations of male the during breeding 1msec season, while others were chance field observations, in which the context of the is unknown. -A Gnathonemm petersii The similarity in the time course of the frequency modulations is strik 0.5 msec ing: generally they take the form of a sudden increase in frequency fol lowed by a slow, and generally ex ponential, decrease back to the Gnathonemus resting frequency. There are excep moon tions to this general pattern: Hypo pomus brevirostris produces a rasp discharge during aggressive dis plays in which the normal dis charge frequency of 50 to 60 im pulses per second is suddenly ele M or my rm vated to over 400 per second for ap rume proximately 40 to 50 msec (Fig. 7F). Gymnarchus niloticus pro duces frequency modulations in which a decrease in frequency is followed eventually by an increase back to the resting frequency (Fig. Mormyrops 7H). It is especially interesting that deliciosus the mormyrids in Africa also pro duce frequency modulations funda mentally the same as those pro duced by the gymnotids in South America. Moller and Bauer (1973) and Bell, Myers, and Russell (1974) Gnathonemm have shown that sudden increases tamandua in frequency are followed by de creases to the resting frequency and that these SID patterns alternate with periods of high discharge fre quency or with cessations in the discharge when two individuals are interacting aggressively. Hyperopisus The final known pattern in the di sp. versity of electric signals, which oc curs in all known electric fish ex cept those in the family Apteronot 6. Oscilloscope tracings show dis (Waveforms are from Bennett 1971a; fish consists of a cessa Figure idae, complete charge waveforms of various mormyriform photographs from Boulenger 1909, Daget tion of the discharge for a variable fishes. Gymnarchus niloticus is the only Af 1954, and Poll 1956, with permission.) period. Figure 8 shows both field rican electric fish with a tone discharge. and laboratory records for several species. resting discharge (waveform, fre ?tes through attempted hybridiza Functions of electric quency, shape), come about tion lowers an individual's repro communication through natural selection? ductive success. It may also be im portant at other times, especially What are the functions of all these Identification. Some electrical dis when individuals of the same electric signals? How did the diver plays serve to identify the species, species form protective social sity, which exists not only in the sex, or age class of the signaler groups or when intraspecific aggres variations in the discharge (fre (Smith 1968). Species recognition is sion aids in dispersal over the avail quency modulations, cessations) particularly critical during the able habitat. The electric signals but also in the characteristics of the breeding season, when loss of gam used in object sensing, since they

1974 July-August 431 are emitted continuously, seem well species, such as Sternopygus, is en species, Gymnorhamphichthys hy were adapted to this role. countered, but Eigenmannia will postomus. Sinusoidal stimuli fight vigorously if two are placed also very effective in eliciting ag Eigenmannia virescens, one of the together in a tank. During the gressive responses when the fre common gymnotids encountered in breeding season, males give court quency was 250-700 Hz (Fig. 9). Guyana, uses the resting frequency ship displays (long sequences of of its electric discharge for species discharge interruptions delivered at During the breeding season, Eigen recognition. The range for the a rate of 2 to 3 per second) when mannia respond to signals resem species, in my study area inMoco they are in the presence of a con bling another Eigenmannia with moco Creek, was between 250 and specific (see Fig. 8C). discharge interruptions delivered at 600 Hz (at 25?C), but each individ a high rate, a normal form of court ual is remarkably stable in its own Tests conducted during the non ship display for this species. The frequency?variations amounted to breeding season showed that ag maximum response to sinusoidal less than 0.3 percent during 10 gressive behavior in captive Eigen stimuli was achieved using 500 Hz minute sampling periods (Bullock mannia is elicited primarily by stimuli (Fig. 10). Males pay little 1969). None of the other thirteen electrical stimuli within the fre attention to sinusoidal stimuli out species in this area had frequencies quency range characteristic of the side the species range. that overlapped with Eigenmannia species. When tape recordings of (see Table 1). Species recognition is various species of gymnotids were Another common species in Moco expressed in aggressive behavior played through electrodes placed on moco Creek, Sternopygus macru and in sexual behavior. Eigenman a gymnotid-shaped plexiglass rus, also uses electrical cues for nia are mildly aggressive toward model, Eigenmannia gave the most species recognition. Its frequency conspecifics, and when one Eigen attacks, threats, and discharge in range (50 to 150 Hz) is unique mannia meets another on its night terruptions in response to record among the four species of tone fish ly excursions in the shallow creek, ings of conspecifics. The least effec found in this area, and courtship it gives electrical threat displays. tive electrical stimulus was a re displays are elicited from males No displays are given when another cording of a pulse-discharging only by stimuli in the appropriate range. Sternopygus is particularly interesting because its resting dis also serves to the Table 1. Discharge frequencies of gymnotid fish from Moco-moco charge identify sex of the As males and fe Creek, Guyana. All species may be categorized as pulse (P) or tone signaler. males reach sexual their (T) according to the waveform of the discharge. maturity, discharge frequencies appear to DayNight change: males adopt lower frequen cies than females with Low-frequency species (all P discharge) (see Fig. 11), no evidence of overlap. Electrophorus 1-5 Hz2-10 Hz electricus As with many tropical species of artedi 5-10 Hz 10-30 Hz Hypopomus fish, the reproductive season coin 5-10 Hz Gymnorhamphichthys (see high-middle frequency) cides with the beginning of the hypostomus rainy season, the period with the most food and space. Just prior to Low P middle-frequency species (all discharge) the breeding season, I noted that mature male Hypopygus lepturus 30-40 Hz 40-50 Hz large, reproductively from the Hypopomus 20-30 Hz 25-60 Hz Sternopygus, recognizable brevirostris very low frequency of their dis were found in Gymnotus carapo 40-50 Hz 50-60 Hz charge, hiding deeply undercut in holes in sub Gymnotus anguillaris 30-40 Hz 35-50 Hz banks, merged trees, and under large even the when High middle-frequency species (P and T discharge, as noted) rocks, during night, it was more typical for Sternopygus Rhamphichthys 80-90 Hz 80-90 Hz to swim in the creek to feed. In sev rostratus (P) eral cases, 5 to 6 males were 55-150 Hz 55-150 Hz Sternopygus clumped together within 3 to 5 macrurus (T) square meters. At night, as Sterno 70-90 Hz Gymnorhamphichthys (see low-frequency) pygus that were thought to be fe hypostomus (P) male passed near a male's hiding place, the male produced a series of High-frequency species (all T discharge) dramatic modifications in his dis "of Eigenmannia 250-600 Hz 250-600 Hz charge frequency. Spectrograms virescens some of the modulations are shown in 12. males Apteronotus 750-1,250 Hz 750-1,250 Hz Figure Sternopygus seemed to the albifrons recognize discharge of the female and Sternarchorhamphus 750-1,000 Hz 750-1,000 Hz frequency pro macrostomus duced a type of courtship song in response to it.

432 American Scientist, Volume 62 A Apteronotusalbifrons E Sternopygus macrurus

, 2 500

0 1 2 3 5 0 5 Time (see) Time (see)

B Hypopygus Upturns Hypopomus brevirostris

250

0 10 20 0.1 0.2 0.3 0.4 0.5 0.6 Time (sec)

Sternarckorhampkus maerostomus G Eigenmanniavirescens

0 0.5 J 15 Time (sec)

H Gymnarchusni?oticm

~50

t 400H

300-f r I 10 20 10 20 30 40 50 Time (sec) Time (see)

Figure 7. All known electric fish are capable phus maerostomus. (D) Sequences of SID dividual pulses from the two fish are seen as of producing frequency modulations in their displays produced by Hypopomus breviros vertical lines. The high-frequency rasp dis discharges, thereby adding an important di tris. Two fish are present; the fundamental play is seen as a series of horizontal bands. mension to signal diversity. (A) "Chirp" frequencies are indicated by the two lowest (G) "Long rise" by Eigenmannia virescens; displays given by Apteronotus albifrons. frequency bands, at 50 Hz and 60-70 Hz. two fish are present. (H) Frequency modu The band at 900 Hz is the fundamental fre (E) "Rises" produced by a male Sternopy lations consist of decreases in the resting quency of the discharge; the band at 1,800 gus macrurus. (F) "Rasp" discharges from frequency in Gymnarchus niloticus. Two Hz is the second harmonic. (B) Slight fre Hypopomus brevirostris are used as an ag fish are present. quency modulations in Hypopygus lepturus. gressive threat display. In this spectrogram, (C) "Chirps" produced by Sternarchorham a major time expansion compared to D, in

1974 July-August 433 Figure 8. Discharge cessations are an im portant parameter of signal diversity. Brief cessations are used as courtship displays by Sternopygus macrurus (A) and Eigenmannia (C) and as aggressive threat displays by Gymnarchus niloticus (B) and Gymnotus carapo (D). Cessations of longer duration are used by Gymnotus (E) and Gymnarchus niloticus (not shown) as an indicator of sub mission. (D and E are from Black-Cleworth 1970, with permission.)

signals, much like display postures described for gulls (Tinbergen 1959) or vocal aggregating signals of pri mates (Marler 1968). The se quences of rises and interruptions given by a Sternopygus in the pres ence of a female certainly appear to belong to this category. Their func tion is to attract a female to the male's hiding place so that further courtship activities can take place.

In an early study of electric com munication, Bullock (1969) found that electric will congregate around a discharging eel in a net, around electrodes carrying artificial electrical pulses, or around elec trodes carrying electrical emissions from an aroused eel in another tank. Since high-frequency dis charges are normally emitted dur ing feeding, these aggregations may I tested whether the frequency of atic study of newly hatched fish, be in response to a signal indicat the stimulus was important in elic but I observed in Trinidad that lar ing the presence of food (Bullock iting "song" by delivering stimuli val and postlarval Gymnotus 6 to 1969; Black-Cleworth 1970). from a sine-wave generator into the 25 mm long discharged at a rate of water near the hiding places of sev 15 to 35 pulses per second, which During fighting behavior, a subor eral large male Sternopygus. Sine then gradually increased to the dinate animal may give displays waves with frequencies typical for adult frequency of 40 to 60 pulses that indicate a clear lack of aggres females (130-141 Hz) evoked varia per second. Similarly, in Guyana, siveness on his part. These displays tions in the male's discharge that Hypopomus breuirostris juveniles appear to play a role in permitting consisted of both rises (Fig. 7E) less than 20 mm long discharged at an aggregation to persist or, in and interruptions (Fig. 8A). Al high frequencies (up to 90 per sec Marler 's terms (1968), in helping to though sine waves that corre ond), whereas adults discharged at maintain proximity. Black-Cle sponded in frequency to a female 30 to 40 per second. worth has found, for example, that Sternopygus evoked responses, subordinate Gymnotus will fre those matched to another male Although the frequency of juvenile quently give a discharge arrest?a Sternopygus, an Eigenmannia, or Apteronotus albifrons is exactly the cessation of 1.5 seconds to 3 min an Apteronotus did not (see Fig. same as adults, juveniles have mo utes?during agonistic encounters. 12). nophasic discharges that change A statistical analysis of sequences gradually into the adult, biphasic of events showed that arrests were Signals that identify the age class type (shown in Fig. 5) by the time commonly elicited from a subordi of the signaler have not been stud the juveniles are 50 mm long. Some nate fish by the approach of a dom ied extensively. Black-Cle worth age-specific changes in signaling inant one. Once the arrest had been (1970) suggested that in Gymnotus properties may merely reflect stages given, the dominant showed a re carapo the amplitude of the dis in the development of the electric duced tendency to attack or chase charge could reflect the size, and organ rather than an age-typical the subordinate when compared to consequently the age class, of the social signal. Further work is need its tendency to attack following signaler. (Brown and Coates, 1952, ed to test the responsiveness of other electrical displays. found a nearly linear relationship adults to signals emitted by differ between size and discharge voltage ent age classes. Arrests, therefore, appear to func in .) Gym tion as an aggression-reducing or notids have never bred in captivity, Aggregation. Some electrical dis appeasement signal?one that helps and thus there has been no system plays function as distance-reducing maintain proximity. Similar dis

434 American Scientist, Volume 62 Figure 9. Responses of Eigenmannia vires cens to sine-wave stimuli of various frequen Discharge interruptions cies. Responses of 5 fish to tests conducted during the nonbreeding season include dis Attacks charge interruptions, attacks, approaches, and retreats. The ordinate represents the O Approaches median number of responses during the 2 minute stimulus for the 5 fish tested. (From A Retreats Hopkins, in press.)

Figure 10. The number of discharge inter ruptions given by Eigenmannia virescens in response to sine-wave stimuli. (From Hop kins, in press.)

plays have evolved in the Mormyri form Gymnarchus niloticus. During discharge cessations for periods of up to 20 minutes by subordinate individuals, there is a reduced rate 200 400 800 2,000 of attack by the dominant (Hop Stimulus frequency (Hz) kins, unpub.). Long cessations are Nonbreeding males and females also given by subordinate Gnatho (N=5) nemus petersii during fighting be O Breeding females (N=7) havior, and the function seems to same as be the in Gymnotus and A Breeding males (N=6) Gymnarchus. Subordinates gener ally have a low rate of firing when in the presence of a dominant indi vidual (Bell, Myers, and Russell 1974).

Silencing the electric organ seems well suited as a display used for ap peasement or aggression reduction, because it renders the fish incon spicuous electrically. Especially in species such as Gymnotus and Gymnarchus, which are intolerant of conspecifics and will react ag gressively toward a wide variety of electrical stimuli resembling their own discharge (Lissmann 1958; Black-Cleworth 1970), silencing may have evolved as an appease 50 100 200 400 800 2,000 ment signal because it is the an Stimulus frequency (Hz) tithesis of an attack-eliciting stim ulus (Darwin 1872). Other species produce submissive displays of an own discharge frequency (Watan Dispersal. Another important func entirely different nature. Eigen abe and Takeda 1963), a response tion of electric signals is to increase mannia virescens in subordinate adapted to avoid "jamming" of the or maintain the distance between roles produce prolonged increases in object-sensing capabilities (Bul the sender and the receiver (Tin frequency followed by a slow de lock, Hamstra, and Sheich 1972; bergen 1959; Marler 1968). Threat crease to the resting frequency. Heiligenberg 1973). Whenever two displays fall into this category, and These long rises (see Fig. 7G) are fish with similar frequencies meet, a variety of electrical displays have often given while the subordinate they must perform this "jamming been discovered that are used for fish is retreating from the domi avoidance response" if they are to threat. For example, itwas possible nant's attacks, approaches, or approach close to one another with to make nighttime observations of threats. Long rises are typically 5 out serious deterioration of their freshly captured Eigenmannia by to 40 seconds in duration and con object-sensing abilities. Under placing them in pairs in an aquari sist of a 5 to 20 Hz elevation in fre these circumstances one may say um under dim red illumination. A quency. that the subtle frequency change statistical analysis of their behavior permits aggregation. It is easy to revealed that dominant individuals Long rises in Eigenmannia resem see how such a jamming-avoidance (the member of the pair that made ble, to a certain extent, the slow, response could have become ritual the greatest number of attacks dur subtle frequency changes elicited ized as a display allowing individu ing a standard watch and also won by electrical stimuli near the fish's als to approach without aggression. competitions for daytime hiding

1974 July-August 435 Sternopygus macrurus places) gave many more 0.01 to 0.1 # Immature second (Moco-moco Creek) discharge interruptions (see than subordinate fish. Female Fig. 8C)

150p Male A temporal analysis showed that the discharge interruptions came at the same time as attacks (butts to the opponent's side, or chases) or actions darts di F 90 threatening (rapid g. rected at the opponent), but rarely ? 70 during retreats from the opponent. Further, in an analysis of the be 50 havior of recipients of electrical dis plays, it was shown that retreat 30 was likely to follow a bout of dis charge interruptions by an oppo 10h nent but attack or approach was not in press). Thus, dis 1Q0 200 300 400 500 600 (Hopkins, charge interruptions were shown to Length (mm) act as a threat display in that they Figure 11. Discharge frequencies (in water dition (R) are from those in distinguished resulted in the retreat of the recipi 25?C) of male, female, and immature Ster condition The sex of nonreproductive (NR). ent. It is to note that in nopygus macrurus are plotted against the small immature fish could not be deter interesting length of the fish. Fish in reproductive con mined in the field. field situations discharge interrup tions are detected much more fre quently at night, when Eigenman nia are dispersed over the available habitat, than during the day, when they clump in hiding places; thus the discharge interruptions may play a role in dispersal.

In a remarkable case of convergent evolution, the African fish Gymnar chus niloticus, which morphologists believe evolved independently from Eigenmannia and its relatives, has an electric discharge nearly identi cal to Eigenmannia^ with regard to frequency, waveform, and polarity (compare Figs. 5 and 6). Gymnar chus and Eigenmannia produce al most identical discharge interrup tions (see Fig. 8B and C) that serve as effective threat displays, as shown by a statistical analysis of electrical and motor actions of con specific pairs of fish held in labora tory tanks (Hopkins, unpub.). Con vergence in the physical forms of a communication signal used as a display raises many interesting questions as to the adaptive signifi cance of the particular signal.

Another type of distance-increasing or -maintaining threat display con sists of modulations in discharge frequency. In a laboratory study of Gymnotus carapo, Black-Cleworth (1970) found a significant correlation between SID displays and aggres sive actions such as attacks and chases. She also found that if she 12. Sound indicate that uli males or fish of Figure spectrograms imitating conspecific electrodes inside a a male Sternopygus macrurus responds to other species. Fish imitated are listed at placed hiding an sinusoidal waves imitating a female of its left, and 3 trials are shown for each. The place, introduced Gymnotus own species but hardly reacts at all to stim- scale applies to all 12 trials. showed a reduced tendency to enter

436 American Scientist, Volume 62 and spent less time inside when the Bennett, M. V. L. 1971b. Electroreceptors. In Hopkins, C. D. 1973. Lightning as back Fish vol. Hoar and noise for communication electrodes were emitting artificial Physiology, 5, Randall, ground among eds. New York: Academic 347 electric fish. Nature 242:268-70. emit Press, pp. SID displays than when they 491. C. D. In press. Electric communi ted unmodulated Hopkins, pulses. Bennett, M. V. L, 1971b. Electroreceptors. In cation: Functions in the social behavior of , vol. 5, Hoar and Randall, Eigenmannia virescens. Behaviour. are eds. New York: Academic 493 SID displays associated with Press, pp. Kalmijn, A. J. 1971. The electric sense of 574. threat in numerous pulse species, and rays. J. Exp. Biol. 55:371-83. M. V. G. D. M. Gime including Hypopomus beebei, H. Bennett, L., Pappas, Liebermann, L. N. 1962. Other electromag and Y. 1967. and H. ,as well nez, Nakajima. Physiology netic radiation. In The Sea, vol. I, Physi brevirostris, artedi, and ultrastructure of electrotonic junc cal Oceanography, M. N. Hill, ed. New as numerous mormyrids. The rasp tions. IV. electromotor nuclei Medullary York: Wiley, pp. 469-75. is merely an in gymnotid fish. J. NeurophysioL discharge exaggeration Lissmann, H. W. 1958. On the function and of a similar Tone fish 30:236-300. phenomenon. evolution of electric organs in fish. J. Exp. also use SID displays for threat. Black-Cleworth, P. 1970. The role of electric Biol. 35:156-91. discharges in the non-reproductive social Lissmann, H. W. 1963. Electric location by behavior of carapo. Anim. Both SID and brief cessations act Gymnotus fishes. Sei. Am. 218:50-59. Behau. Monog. 3:1-77. as effective social because Lissmann, H. W., and K. E. Machin. 1958. signals Boulenger, G. A. 1909. Catalogue of the The mechanism of object location in they conspicuously contrast with Fresh-water Fishes of Africa in the British Gymnarchus niloticus and similar fish. J. the fish's normal Museum (Natural History), vol. 1. Lon discharge activity. Exp. Biol. 35:451-86. Of course, an cannot don: British Museum. interruption Lloyd, J. E. 1966. Studies on the flash a Brown, M. V., and C. W. Coates. 1952. Fur persist for long without its loss as communication system in Photinus fire ther comparisons of length and in feature. voltage flies. Univ. ofMichigan: Mise: Puhl. Mus. conspicuous contrasting the electricus. the evolution of these Electrophorus ZooL, No. 130. Although Zoologica 37:191-97. threat is still Lloyd, J. E. 1971. Bioluminescent communi displays uncertain, Bullock, T. H. 1969. Species differences in cation in insects. Ann. Rev. Entomology Black-Cleworth has that effect of on electric suggested electro-receptor input 16:97-122. SID in Gymnotus?also given while organ pacemakers and other aspects of Marier, P. 1959. in the a behavior in gymnotid fish. , Behav. Developments study attacking prey?may be ritualized of animal Bi Euol. 2:85-118. communication. In Darwin's feeding display. Much further work ological Work, P. R. Bell, ed. London. Bullock, T. H. 1973. Seeing the world is needed before we will be able to Cambridge Univ. Press, pp. 150-206. through a new sense: in Marier, P. 1968. and understand the evolution of social fish. Am. Sei. 61:316-25. Aggregation dispersal: electric fish. Two functions in communication. signaling among T. R. H. and H. Bullock, H., Hamstra, Jr., In Primates: Studies in and Scheich. 1972. The jamming-avoidance In summary, certain South Ameri Variability, P. Jay, ed. New York: Holt, response of high-frequency electric fish. I. Rinehart and 420-38. can and fishes Winston, pp. African capable of General features. J. Comp. Physiol. 77:1 Marler, P., and W. J. Hamilton. 1966. and electric dis 22. producing sensing Mechanisms of Animal Behavior. New an C. 1961. On Communica charges have evolved unusual Cherry, York: Wiley. tion: A a and a Criticism. modality of communication?elec Review, Survey Moller, P., and R. Bauer. 1973. "Communi New York: Science Editions. tric signaling. Signals are broadcast cation" in weakly electric fish, Gnathone A., and F. de Almeida. 1961. The mus II. Interaction in all directions within what ap Couceiro, petersii (Mormyridae). electrogenic tissue of some Gymnotidae. of electric activities of to be a limited Never organ discharge pears range. In , C. Chagas and A. P. two fish. Anim. Behav. 21:501-12. theless, to instantaneous de Carvalho, eds. Amsterdam: owing Elsevier, Poll, M. 1957. Les genres des poissons d'eau p. 3. conduction and rapid fade-out, this douce de l'Afrique. Annales du Mus?e seems du Tervuren modality well adapted for Daget, J. 1954. Les poissons du Niger Sup? Royal Congo Belge (Belgi Ser. 54:1-191. transmitting messages quickly. rieur. M?moires de l'Institut Francais que), 8, Noire 36:1-391. A. 1972. Wozu dienen die Electric signals show a great deal of d'Afrique Roth, Elektrorez C. 1872. The the eptoren der Welse? J. Comp. Physiol. diversity, which can be classified Darwin, Expression of Emotions inMan and the Animals. Lon 79:113-35. according to one or more parame don: John Murray Publishers. Russell, C. J., J. P. Myers, and C. C. Bell. ters, the of the 1974. The echo in Gnathonemus including shape Granath, L. P., F. T. Erskine III, B. S. response J. field, waveform, frequency, timing, Maccabee, and H. G. Sachs. 1968. Elec petersii (Mormyridae). Comp. Physiol. W. J. frequency modulations, and cessa tric field measurements on a weakly elec Smith, 1968. Message-meaning analy tric fish. ses. In Animal T. A. Se tions. In addition to helping to in Biophysik. 4:370-72. Communication, beok, ed. Bloomington: Indiana Univ. crease, decrease, or maintain the Greenwood, P. H., D. E. Rosen, S. H. Press, pp. 44-60. distance between and re Weitzman, and G. S. Myers. 1966. Phyle signaler Szabo, T., and P. 1964. Pacemaker tic studies of teleostean fishes with a pro Enger. ceiver, electric communication activity of the medullary nucleus control visional classification of living forms. seems to an electric in play important role in Bull. Am. Mus. Nat. Hist. 131:341-455. ling organs high-frequency gymnotid fish. Z. vergl. Physiol. 49:285 species, sex, and age-class recogni W. 1973. of Heiligenberg, Electrolocation 300. tion. in the electric objects fish, Eigenmannia Tinbergen, N. 1959. Comparative studies of J. (Rhamphichthyidae, Gymnotoidei). the behaviour of gulls (Laridae): A prog Comp. Physiol 87:137-64. ress Behaviour 15:1-70. References report. Hockett, C. F. 1960. Logical considerations Watanabe, A., and K. Takeda. 1963. The Altmann, S. 1967. The structure of primate in the study of . In change of discharge frequency by AC social communication. In Social Commu Animal Sounds and Communication, W. stimulation in a weak electric fish. J. nication among Primates, S. Altmann, ed. E. Lanyon and W. N. Tavolga, eds. Exp. Biol. 40:57-66. of Press. D.C.: Am. Ins. Biol. Chicago: University Chicago Washington, Sei., pp. Waxman, S. G., G. D. Pappas, and M. V. 392-430. Bell, C. C, J. P. Myers, and C. J. Russell. L. Bennett. 1972. Morphological correlates 1974. Electric organ discharge patterns Hopkins, C D. Patterns of electrical com of functional differentiation of nodes of during dominance-related behavioral dis munication among gymnotid fish. Ph.D. Ran vier along single fibers in the neuro plays in Gnathonemus petersii. J. Comp. dissertation, 1972, Rockefeller University, genie electric organ of the knife fish Ster Physiol. New York. narchus. J. Cell Biol. 53:210-24.

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