Effects of social interaction on the electric organ discharge in a mormyrid fish, Gnathonemus petersii (Mormyridae, Teleostei)
1 Hunter College of the City University of New York, Department of
Psychology
2 The American Museum of Natural History, Division of Vertebrate Zoology
(Ichthyology), Central Park West at 79th Street, New York, NY 10024-5192,
USA
* Author for correspondence (e-mail: tterleph{at}hotmail.com)
Accepted 4 April 2003
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: Mormyridae, Gnathonemus, social behavior, electric organ discharge, behavioral plasticity
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
There are, however, a number of factors that can influence the EOD in the
short term, including environmental conditions such as water temperature and
conductivity (reviewed by Moller,
1995) as well as biological factors such as a male's position in
the dominance hierarchy (Carlson et al.,
2000
). Increases in EOD duration comparable with those observed in
dominant fish also occur following androgen treatment
(Bass and Hopkins, 1985
;
Bass, 1986
;
Landsman and Moller, 1988
;
Landsman et al., 1990
;
Herfeld and Moller, 1998
).
South American gymnotiform electric fish also show fluctuations in both EOD
amplitude and duration (Hagedorn,
1995
; Franchina and Stoddard,
1998
; Franchina et al.,
2001
). Social interaction affects the EOD rate
(Dunlap, 2002
;
Dunlap et al., 2002
) and
duration (Franchina et al.,
2001
) of gymnotids, and increases in the EOD duration can be
induced by androgens (Few and Zakon,
2001
).
The current experiment was designed to test the hypothesis that subadult
Gnathonemus petersii are capable of exhibiting socially mediated EOD
changes outside the species' breeding season, i.e. in the absence of exogenous
factors such as water conductivity and water level that trigger the cyclic
reproductive conditions in mormyrid fish (Kirschbaum,
1995,
2000
). The presence of such
changes would suggest that EODs are involved in communication in the context
of territorial and/or dominance interactions and are not restricted to mate
attraction. To date, socially mediated changes in EOD duration and amplitude
have not been reported under non-breeding conditions. The specific aims of
this paper were (1) to ascertain whether the subadult mormyrid EOD is affected
by social interactions in a manner comparable with that observed in adult
fish, (2) to determine whether such changes differ between and within the
sexes and (3) to compare the effects of free and restricted social
interactions on the subadult EOD.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Apparatus
Fish were singly housed in 19-liter aquaria and kept under a 12 h:12 h L:D
regimen with lights on at 07.00. The stimulus (interaction) tanks were
57-liter aquaria (length, 60 cm; width, 30 cm; water depth, 25 cm). Water
conditions in both the holding and interaction tanks were held constant within
limits (conductivity, 178±6.3 µS cm-1; temperature,
24.9±0.2°C). To restrict fish in their interactions, a plastic mesh
divider (0.75 cm thick; mesh squares, 1.5 cmx1.5 cm) was inserted into
the tank, separating the interaction area into two equal compartments
(Fig. 1). This partition
allowed free water flow between compartments, thus permitting electric
interaction but preventing the fish from direct physical contact. The opaque
mesh also partially restricted vision and potential lateral-line-mediated
cues.
|
EOD measurements
EODs were monitored with a pair of Ag/AgCl recording electrodes, placed at
the head and tail region of each fish, preamplified and displayed on an
oscilloscope (Hitachi digital storage, model VC-6023). The EOD of G.
petersii consists of four phases, P1, P2, P3 and P4
(Fig. 2). We restricted our
analysis to P2 and P3, the two phases exhibiting the largest positive and
negative amplitudes, respectively. We will refer to the sum of P2 and P3
durations as EOD duration. P2 duration was measured from its initial
positive-going zero crossing to the intersection with baseline. P3 duration
was measured from the end of P2 to the ascending intersection with baseline.
Peak amplitude measures were taken for P2 and P3. The amplitude ratio
A2/A3 served as a derived variable. EOD duration and
amplitude ratio were collected daily (during the fish's early subjective day).
EOD duration is affected by temperature; therefore, data were adjusted to a
conventional standard of 25°C using a calibration function based on a data
set obtained from G. petersii (see
Herfeld and Moller, 1998).
|
Interaction conditions
Fish were initially housed singly for 4 days and were subsequently placed
into a tank with a neighbor for a 4-day interaction period. Following this
period, they were returned to their home tanks for another 4 days. The social
interaction varied in three ways.
Statistical procedures
Between-subjects analysis of variances (ANOVAs) were run with repeated
measures within subjects (mixed-model ANOVAs). ANOVAs were performed using
Statistica for Windows (Statsoft, Inc., Tulsa, OK, USA). The significance
level was set at P<0.05. The dependent measures for different
ANOVAs were EOD duration and A2/A3 amplitude ratio. The
independent variables in different ANOVAs (depending on the group being
tested) were interaction level, dominance status and sex. Separate ANOVAs were
run for malemale and femalefemale pairs. The ANOVAs and the
independent variables tested for each group are listed in the Results. Where
applicable, Tukey's honest significant difference post-hoc tests were
performed. Mean data for the three individual manipulation periods (days
14, pre-interaction; days 58, interaction; and days 912,
post-interaction) were used as repeated measures in all ANOVAs.
Post-hoc comparisons of interaction effects (manipulation period x dominance status) were not possible, however. This was due to the fact that there was no clear choice of an appropriate error term for comparisons that involve between- and within-group interactions (Statistica for Windows program manual).
All procedures complied with local, state and federal regulations and were approved by the Hunter College Institutional Animal Care and Use Committee (protocol # PM/TT 6/03-02).
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
EOD duration also changed in males (F2,24=6.32, P<0.01; Fig. 3B); there were significant differences between interaction (297.9 µs) and both the pre-interaction (308.8 µs) and post-interaction (308.6 µs) periods. These differences were due to a decrease in the EOD duration in subordinates and controls but not in dominant fish, as suggested by a status x manipulation period interaction (F4,24=9.13, P<0.0001).
In different mixed-sex pairs, individuals of each sex established dominance. Of the five mixed-sex pairs, three possessed dominant males and two possessed dominant females. These pairs showed dominance-associated EOD differences similar to those in the same-sex dyads (Fig. 3C). EOD duration increased in dominants relative to subordinates, as shown by a significant dominance x manipulation period interaction (Table 1, ANOVA 5; F=3.29, P<0.05).
Amplitude ratios (Table 1, ANOVAs 2, 4) increased in malemale (F2,24=3.68, P<0.05) and femalefemale (F2,24=3.48, P<0.05) pairs. In females, a post-hoc analysis revealed a significant difference between pre-interaction (0.649) and interaction (0.670) periods. In males, the amplitude ratios were higher during interaction (0.640) than during post-interaction (0.617). Dominant fish (i.e. that excluded their neighbors from access to the shelter) thus showed a trend of increased amplitude ratio during the interaction periods (Fig. 4AC). These changes in amplitude ratio corresponded with increases in EOD duration. In mixed-sex pairs, however, the difference in amplitude ratios was not significant (Table 1, ANOVA 6).
|
Restricted interaction
During restricted interactions, fish could not make physical contact but
were able to detect each other's EODs. We hypothesized that under such
conditions the EOD would (1) not change in either fish, (2) assume dominant
characteristics in one fish or (3) assume such characteristics in both. A
comparison of EOD durations (under restricted and free conditions) showed a
comparable increasing trend in femalefemale pairs
(Fig. 5A) and no change in
malemale pairs (Fig.
5B). The EOD in solitary fish of both sexes remained, as expected,
unchanged.
|
There was a significant manipulation period effect upon EOD duration in both femalefemale (F2,44=8.25, P<0.001) and malemale (F2,44=3.66, P<0.05) pairs (Table 2, ANOVAs 1, 3). In females, EOD duration during the interaction (326.5 µs) and post-interaction (321.0 µs) periods was significantly longer than during pre-interaction (303.6 µs). The EOD duration in femalefemale pairs also showed a significant interaction between manipulation periods and the free, restricted or solitary types of interaction (F4,44=3.73, P<0.05; Table 2, ANOVA 1). Although post-hoc tests could not be performed on this interaction effect, Fig. 5A shows that during the interaction period the solitary group differed most from the freely interacting and restricted groups. In malemale pairs, there was no difference in EOD duration between the different types of interaction (Fig. 5B) and there were no significant differences in amplitude ratios between any freely interacting, restricted and solitary groups (Table 2, ANOVAs 2, 4).
|
Dominant fish in freely interacting malemale and femalefemale groups showed no sex difference in EOD duration, although the differences in EOD duration did approach significance (F1,24=3.87, P=0.0609). There was a significant sex difference in amplitude ratio between these groups (F1,24=4.72, P<0.05). Post-hoc analysis of these data showed that females (0.658) had a significantly higher amplitude ratio than males (0.629), but no significant interaction between sex and dominance status existed.
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Signaling dominance
Signaling dominance may be equally important for subadults of both sexes,
particularly during the dry season as territories dry up and food supplies
diminish. In many mormyrids, the EOD sex difference is prominent only during
the breeding season (Hopkins,
1981; Landsman,
1993a
). This difference, as Carlson et al.
(2000
) have shown, can be
further enhanced (in males) during social/dominance interactions. During the
breeding season, females may suppress dominance signaling in order to
facilitate access to a male-defended territory. Thus, dominance signaling in
female G. petersii should occur only prior to sexual maturity and/or
during the non-breeding season. Our hypothesis predicts that the female EOD
during breeding conditions will resist social and/or androgen-mediated
changes, remaining consistently shorter and with less inter-individual
variability than the EODs of males under similar conditions. This is indeed
the case in other mormyrids such as B. brachyistius
(Carlson et al., 2000
) and
Mormyrus rume proboscirostris (P. Moller, C. Schugardt and F.
Kirschbaum, unpublished).
That subadult female mormyrids can respond to circulating androgens has
been amply demonstrated in hormone administration studies, resulting in
male-like changes in the EOD waveform (Bass
and Hopkins, 1985; Landsman
and Moller, 1988
; Landsman,
1995
; Herfeld and Moller,
1998
). Such laboratory tests have always been conducted under
carefully controlled environmental conditions, including relatively invariant
water conductivity, mimicking aquatic conditions typical of the non-breeding
season.
EODs as a status badge
The EOD changes resulting from social interaction may serve to
differentiate individual status in groups. Differences in inter-individual EOD
duration may serve as badges of current status, reducing unnecessary conflict.
Many species of fish use coloration and markings to signal dominance, with
high-ranking individuals taking on coloration (associated with hormonal
condition) only as a result of social dominance
(Magurran, 1986).
Communication using status badges is well documented in birds (e.g. Harris
sparrows Zonotrichia querula), where black feathers correlate with
both testosterone and social dominance (Rohwer,
1975
,
1982
; Rohwer and
Rohwer, 1978
). The mormyrid
EOD might serve as an electric badge, as EOD duration correlates with both
androgens and social dominance in these fish.
Our data lend support to the hypotheses that in restricted interactions there are either dominant-like changes in one fish (suggesting that dominant status is attained under restricted conditions) or that dominant-like EOD changes occur in both individuals (suggesting that changes that can occur in both members of a restricted pair are suppressed in subordinates only as a result of free interaction). During restricted interactions, we recorded dominant-like EOD changes in either one or both members of a female pair. To assess whether only one or both fish in an interacting dyad showed dominant-like changes, we reanalyzed the data collected from restricted femalefemale interactions (Fig. 6). Within-pair differences were used to designate members to one of two groups: pseudo-dominant or pseudo-subordinate. Individuals that showed a larger increase in EOD duration relative to their neighbor at the onset of restricted interaction were designated as pseudo-dominant. The neighbors of these pseudo-dominant individuals were assigned to pseudo-subordinate status (it was not possible to perform parametric statistical analyses on these data, as group assignment was based upon EOD measures). Without exception, freely interacting dominant females (see Fig. 3A), like pseudo-dominant females, showed increases in EOD duration relative to their neighbors. In both pseudo-dominant and pseudo-subordinate groups, we noted an increasing trend in EOD duration during interaction (Fig. 6A).
|
In the pseudo-subordinate fish, there was no increase in amplitude ratio during the interaction period, although amplitude ratio in this group did remain higher than or comparable with that of the pseudo-dominant group throughout this period (Fig. 6B). The possibility that pseudo-dominant restricted fish would also show dominant status in free interaction was not tested.
The EOD duration of dominant females and males
(Fig. 3A and
Fig. 3B, respectively) and both
pseudo-dominant and pseudo-subordinate females under restricted conditions
(Fig. 6A) returned towards
shorter pre-treatment levels in the days following interaction. The return to
shorter pre-interaction EODs suggests that elongated EODs are costly to
maintain. There is evidence supporting this assertion: longer EODs are less
efficient at precision time marking. As patterned EOD inter-pulse intervals
encode information in time intervals, short-duration EODs should result in
more accurate signaling (Kramer,
1990). In addition, increases in EOD duration correlate with
increases in circulating androgen levels, and the maintenance of elevated
androgen levels is known to be costly for many species. Androgens adversely
impact immune systems and reduce survivorship by increasing metabolic costs
(Grossman, 1985
; Marler and
Moore, 1988
,
1989
;
Folstad and Carter, 1992
). It
is possible that the social signaling benefits associated with an elongated
EOD outweigh the costs endured. EOD parameters may serve as
condition-dependent indicators of the fish's resource holding potential.
During free interactions, some subordinates that had shown no EOD duration
increases during interaction exhibited post-treatment increases
(Fig. 3A,B). The reasons for
this opposite post-interaction response are not clear.
Role of EOD amplitude in communication
The role of the EOD in mormyrid communication has mostly focused on
differences in its temporal characteristics (Hopkins,
1981,
1986
,
1999
;
Kramer, 1990
). Little
attention has been paid to the phase amplitude of the EOD
(Bass, 1986
). The socially
mediated change in phase amplitude ratio shown here suggests a possible
communicative function. Thus, in addition to EOD duration, the relative phase
amplitude might serve as a cue to conspecifics about a neighbor's social
status. The knollenorgan receptor pathway (mediating communication) is
sensitive to temporal rather than amplitude differences
(Hopkins and Bass, 1981
;
Hopkins, 1983
,
1988
,
1999
;
Bass and Hopkins, 1985
;
Zakon, 1986
;
Xu-Friedman and Hopkins,
1999
). Are the observed changes in amplitude ratios a mere side
effect or do these variations actually affect social communication?
The detection threshold for the individual phases of a single EOD will
depend on their phase amplitudes. When the threshold for a transition between
phases is reached, knollenorgans will produce a single spike for each detected
EOD phase transition (Hopkins and Bass,
1981; Bell, 1986
).
We hypothesize that at a distance, within the signal's active space but below
the detection threshold of one or more phases, a conspecific should detect the
presence of an immature sender as being different from that of a socially
dominant or sexually mature male. At the detection boundary of the signal's
active space, signals with phases of different relative amplitude may be
detected as monophasic, biphasic or triphasic. Thus, the higher
A2/A3 ratio characteristic of the dominant fish in this
experiment should, at a distance, be detected more often as biphasic rather
than as monophasic.
At the boundary of the electro-communication range, where fish can first
detect a potential mate or rival, the EODs broadcast by sexually mature and
immature/subordinate individuals should differ in a simple quantitative way.
Determining the number of discrete detectable phases may aid these fish in
assessing dominance/sexual receptivity. A multiphasic EOD may also be less
likely to attract electroreceptive predators
(Stoddard, 1999). As a fish
emits EODs in the context of defending its territory and/or attracting mates,
it may also attract predators (specifically, the catfish Clarias).
Multiple phases may allay the predation cost of increased signaling during
agonistic or mating behavior by making the signal cryptic.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Bass, A. H. (1986). A hormone-sensitive communication system in an electric fish. J. Neurobiol. 17,131 -156.[Medline]
Bass, A. H. and Hopkins, C. D. (1985). Hormonal control of sex differences in the electric organ discharge (EOD) of mormyrid fishes. J. Comp. Physiol. A 156,587 -604.
Bell, C. C. (1986). Electroreception in mormyrid fish: central physiology. In Electroreception (ed. T. H. Bullock and W. Heiligenberg), pp. 423-452. New York: Wiley.
Brown, B., Benveniste, L. M. and Moller, P. (1996). Basal expansion of anal fin-rays: a new osteological character in weakly discharging electric fish (Mormyridae). J. Fish Biol. 49,1216 -1225.[CrossRef]
Carlson, B. A., Hopkins, C. D. and Thomas, P. (2000). Androgen correlates of socially induced changes in the electric organ discharge waveform of a mormyrid fish. Horm. Behav. 38,177 -186.[CrossRef][Medline]
Crockett, D. P. (1986). Agonistic behavior of the weakly electric fish, Gnathonemus petersii (Mormyridae, Osteoglossomorpha). J. Comp. Psychol. 100, 3-14.[CrossRef][Medline]
Dunlap, K. D. (2002). Hormonal and body size correlates of electrocommunication behavior during dyadic interactions in a weakly electric fish, Apteronotus leptorhynchus. Horm. Behav. 41,187 -194.
Dunlap, K. D., Pelczar, P. L. and Knapp, R. (2002). Social interactions and cortisol treatment increase the production of aggressive signals in male electric fish, Apteronotus leptorhynchus. Horm. Behav. 42, 97-108.[CrossRef][Medline]
Few, W. P. and Zakon, H. H. (2001). Androgens alter electric organ discharge pulse duration despite stability in electric organ discharge frequency Horm. Behav. 40,434 -442.[CrossRef][Medline]
Folstad, I. and Carter, A. J. (1992). Parasites, bright males, and the immunocompetence handicap. Am. Nat. 139,603 -622.[CrossRef]
Franchina, C. R. and Stoddard, P. K. (1998). Plasticity of the electric organ discharge waveform of the electric fish Brachyhypopomus pinnicaudatus I. Quantification of day-night changes. J. Comp. Physiol. A 183,759 -768.[CrossRef][Medline]
Franchina, C. R., Salazar, V. K., Volmar, C. H. and Stoddard, P. K. (2001). Plasticity of the electric organ discharge waveform of male Brachyhypopomus pinnicaudatus II. Social effects. J. Comp. Physiol. A 187,45 -52.[CrossRef][Medline]
Grossman, C. J. (1985). Interactions between the gonadal steroids and the immune system. Science 227,838 -840.
Hagedorn, M. (1995). The electric fish Hypopomus occidentalis can rapidly modulate the amplitude and duration of its electric organ discharges. Anim. Behav. 49,1409 -1413.[CrossRef]
Herfeld, S. and Moller, P. (1998). Effects of
17-methyltestosterone on sexually dimorphic characters in the weakly
discharging electric fish, Brienomyrus niger (Günther, 1866)
(Mormyridae): electric organ discharge, ventral body wall indentation, and
anal-fin ray expansion. Horm. Behav.
34,303
-319.[CrossRef][Medline]
Hopkins, C. D. (1980). Evolution of electric communication channels of mormyrids. Behav. Ecol. Sociobiol. 7,1 -13.
Hopkins, C. D. (1981). On the diversity of electric signals in a community of mormyrid electric fish in West Africa. Am. Zool. 21,211 -222.
Hopkins, C. D. (1983). Neuroethology of species recognition in electroreception. In Advances in Vertebrate Neuroethology. NATO ASI series, A56 (ed. J. P. Ewert, R. R. Capranica and D. J. Ingle), pp. 871-881. New York: Plenum.
Hopkins, C. D. (1986). Behavior in mormyridae. In Electroreception (ed. T. H. Bullock and W. Heiligenberg), pp. 527-576. New York: Wiley.
Hopkins, C. D. (1988). Neuroethology of electric communication. Annu. Rev. Neurosci. 11,497 -535.[CrossRef][Medline]
Hopkins, C. D. (1999). Design features for
electric communication. J. Exp. Biol.
202,1217
-1228.
Hopkins, C. D. and Bass, A. H. (1981). Temporal coding of species recognition signals in an electric fish. Science 212,85 -87.[Medline]
Kirschbaum, F. (1987). Reproduction and development of the weakly electric fish, Pollimyrus isidori (Mormyridae, Teleostei) in captivity. Environ. Biol. Fishes 20,11 -31.
Kirschbaum, F. (1995). Reproduction and development in mormyriform and gymnotiform fishes. In Electric Fishes: History and Behavior (ed. P. Moller), pp.267 -301. London: Chapman and Hall.
Kirschbaum, F. (2000). The breeding of tropical freshwater fishes through experimental variation of exogenous parameters Breeding through simulation of high and low water conditions. Aqua Geographia 7,95 -105.
Kramer, B. (1990). Electrocommunication in Teleost Fishes: Behavior and Experiments. Berlin: Springer-Verlag.
Kramer, B. and Bauer, R. (1976). Agonistic behaviour and electric signaling in a mormyrid fish, Gnathonemus petersii. Behav. Ecol. Sociobiol. 1, 45-61.
Landsman, R. E. (1993a). Sex differences in external morphology and electric organ discharges in imported Gnathonemus petersii (Mormyriformes). Anim. Behav. 46,417 -429.[CrossRef]
Landsman, R. E. (1993b). The effects of captivity on the electric organ discharge and plasma hormone levels in Gnathonemus petersii Mormyriformes). J. Comp. Physiol. A 172,619 -631.[Medline]
Landsman, R. E. (1995). Sources of plasticity in behavior and its physiology: sex, hormones, environment and the captivity model. In Electric Fishes: History and Behavior (ed. P. Moller), pp. 303-343. London: Chapman and Hall.
Landsman, R. E., Harding, C. F., Moller, P. and Thomas, P. (1990). The effects of androgens and estrogen on the external morphology and electric organ discharge waveform of Gnathonemus petersii (Mormyridae, Teleostei). Horm. Behav. 24,532 -553.[Medline]
Landsman, R. E. and Moller, P. (1988). Testosterone changes the electric organ discharge and external morphology of the mormyrid fish, Gnathonemus petersii (Mormyriformes). Experientia 44,900 -903.[Medline]
Magurran, A. E. (1986). Individual differences in fish behaviour. In The Behaviour of Teleost Fishes (ed. T. J. Pitcher), pp. 338-365. Baltimore, MD: Johns Hopkins University Press.
Marler, C. A. and Moore, M. C. (1988). Evolutionary costs of aggression revealed by testosterone manipulations in free-living male lizards. Behav. Ecol. Sociobiol. 23, 21-26.[CrossRef]
Marler, C. A. and Moore, M. C. (1989). Time and energy costs of aggression in testosterone-implanted free-living male mountain spiny lizards (Sceloporus jarrovi). Physiol. Zool. 62,1334 -1350.
Moller, P. (1995). Electric Fishes: History and Behavior. London: Chapman and Hall.
Pezzanite, B. and Moller, P. (1998). A sexually dimorphic basal anal-fin ray expansion in the weakly discharging electric fish Gnathonemus petersii. J. Fish Biol. 53,638 -644.[CrossRef]
Rohwer, S. A. (1975). The social significance of avian winter plumage variability. Evolution 29,593 -610.
Rohwer, S. A. (1982). The evolution of reliable and unreliable badges of fighting ability. Am. Zool. 22,531 -546.
Rohwer, S. A. and Rohwer, F. C. (1978). Status signaling in Harris' sparrows: experimental deceptions achieved. Anim. Behav. 26,1012 -1022.
Rojas, R. and Moller, P. (2002). Multisensory contributions to the shelter-seeking behavior of a mormyrid fish, Gnathonemus petersii Günther (Mormyridae, Teleostei): the role of vision, and the passive and active electrosenses. Brain, Behav. Evol. 59,211 -221.[CrossRef][Medline]
Stoddard, P. K. (1999). Predation enhances complexity in the evolution of electric fish signals. Nature 400,254 -256.[CrossRef][Medline]
von der Emde, G. (1998). Electroreception. In The Physiology of Fishes, 2nd edition (ed. D. H. Evans), pp. 313-343. New York: CRC Press.
Westby, G. W. M. and Kirschbaum, F. (1977). Emergence and development of the electric organ discharge in the mormyrid fish, Pollimyrus isidori. I. The larval discharge. J. Comp. Physiol. A 122,251 -271.
Westby, G. W. M. and Kirschbaum, F. (1978). Emergence and development of the electric organ discharge in the mormyrid fish, Pollimyrus isidori. II. Replacement of the larval by the adult discharge. J. Comp. Physiol. A 127, 45-59.
Westby, G. W. M. and Kirschbaum, F. (1982). Sex differences in the waveform of the pulse-type electric fish, Pollimyrus isidori (Mormyridae). J. Comp. Physiol. A 145,399 -403.
Xu-Friedman, M. A. and Hopkins, C. D. (1999).
Central mechanisms of temporal analysis in the knollenorgan pathway of
mormyrid electric fish. J. Exp. Biol.
202,1311
-1318.
Zakon, H. H. (1986). The electroreceptive periphery. In Electroreception (ed. T. H. Bullock and W. Heiligenberg), pp. 103-156. New York: Wiley.