Journal of Fish Biology (2001) 58, 1489–1511

doi:10.1006/jfbi.2001.1625, available online at http://www.idealibrary.com on

REVIEW PAPER
The evolution of electroreception and bioelectrogenesis in
teleost fish: a phylogenetic perspective
J. A. A-G
Instituto Nacional de Pesquisas da Amazônia, INPA-CPBA, CP 478, Manaus AM,
69083-000, Brazil

(Received 30 October 2000, Accepted 27 March 2001)

According to current phylogenetic theory, both electroreceptors and electric organs evolved
multiple times throughout the evolution of teleosts. Two basic types of electroreceptors have
been described: ampullary and tuberous electroreceptors. Ampullary-type electroreceptors
appeared once in the common ancestor of the Siluriformes+Gymnotiformes (within the
superorder Ostariophysi), and on two other occasions within the superorder Osteoglos-
somorpha: in the African Mormyriformes and in the African Notopteriformes. Tuberous
receptors are assumed to have evolved three times; all within groups that already possessed
ampullary receptors. With the exception of a single catfish species, for which studies are
still lacking, all fish with tuberous electroreceptors also have an electric organ. Tuberous
electroreceptors are found in the two unrelated electrogenic teleost lineages (orders
Gymnotiformes and Mormyriformes) and in one non-electrogenic South American catfish
species (order Siluriformes). Electric organs evolved eight times independently among teleosts:
five of them among the ostariophysans (once in the gymnotiform ancestor and in four
siluriform lineages), once in the common ancestor of Mormyriformes, and in two uranoscopids.
With the exception of two uranoscopid genera, for which no electroreceptive capabilities have
been discovered so far, all electric organs evolved as an extension of a pre-existing electrorecep-
tive (ampullary) condition. It is suggested that plesiomorphic electric organ discharges (EODs)
possessed a frequency spectrum that fully transgressed the tuning curve of ampullary receptors,
i.e. a signal such as a long lasting monophasic pulse. Complex EOD waveforms appeared as a
derived condition among electric fish. EODs are under constant evolutionary pressure to
develop an ideal compromise between a function that enhances electrolocation and electrocom-
munication capabilities, and thereby ensures species identity through sexual and behavioural
segregation, and minimizes the risk of predation.  2001 The Fisheries Society of the British Isles

Key words: electric organs; electroreceptors; Teleostei; electric organ discharges.

INTRODUCTION
Electric fields in the aquatic environment are relevant to the behavioural biology
of fishes in two ways: there are fish that are able to detect electric gradients in
the surrounding medium through a set of specialized sensorial cells (electro-
receptors), and fish that possess specialized organs that generate electric
discharges on a more or less regular basis.
Electroreception is an ancient sensory modality in vertebrate history, believed
to have appeared more than 500 million years ago as it is present in all the
ancient vertebrate lineages such as in the Petromyzontiformes and the
Chondrichthyes; it is also present in some of the Sarcopterygii (in lungfishes, in
Tel./fax: +55 92 643-3249; email: puraque@inpa.gov.br
1489
0022–1112/01/061489+23 $35.00/0  2001 The Fisheries Society of the British Isles
1490 . . -

the coelacanth and in some amphibians) as well as in some Actinopterygii

(Bullock et al., 1983; New, 1997). The functional unit, known as the
‘ electroreceptor ’, embraces several types of specialized cells that transduce
electric gradients in the environment into action potentials that are relayed up to
the central nervous system.
Electric organs are also assumed to be an ancient development, but presum-
ably a more recent feature than electroreceptors, since in vertebrate evolutionary
history, they first appeared within cartilaginous fish [there are three genera of
rays that produce Electric Organ Discharges (EODs) [Torpedo Houttuyn,
Narcine Henle and Raja Linnaeus] and later evolved independently in several
groups of teleosts. A more precise estimate of the geological time associated with
the appearance of electric organs in teleosts (or in non-teleosts) is more difficult
to establish than for electroreceptors. This is mainly because only a few
elasmobranchs are electrogenic and there is no direct way of establishing
approximately when the electric organs first evolved as an evolutionary novelty
within a particular fish lineage. The absence or inadequacy of fossil material for
most clades involved plus the obvious absence of soft tissue (electric organs) in
the fossil records only adds to the confusion. One possible alternative is to use
indirect estimates, as rates of molecular evolution (molecular clock) when these
are available. Alves-Gomes (1999), calibrated absolute rates of molecular
evolution for the 12S and 16S mitochondrial rRNA genes of ostariophysans and
osteoglossomorphs and estimated that Gymnotiformes (their electric organ is
assumed to be present in their common ancestor) differentiated between 79 and
117 million years ago, whereas the Mormyriformes differentiated between 61
and 72 million years ago. Unfortunately, no such data is yet available for the
remaining electrogenic teleosts. The functional unit of the electric organ is the
electrocyte which is (in all fish studied to the present) a modified cell derived from
a muscular precursor.
In this review, the appearance of electroreceptors and electric organs within
the extant teleosts is discussed, taking into consideration their phylogenetic
history and some of the evolutionary aspects related to the diversification of
EOD waveforms. Here, following de Pinna (1996), Teleostei is defined as ‘ the
largest (i.e., most inclusive) actinopterygian clade not including either the
Halecormophi (Amia and close relatives) and/or the Gynglymodi (Lepisosteus
and close relatives) ’. Bennett (1971a,b), Bass (1986), Zakon (1986) and Moller
(1995) give comprehensive reviews of electroreception and electric organs in
other non-teleost fish that are outside the scope of this review.

THE ELECTROGENIC-ELECTROSENSORY SYSTEM IN TELEOSTS

Despite the obvious benefit of having both systems, bioelectrogenesis and
electroreception do not always co-occur. There are several electroreceptive
fish that do not produce electricity, and there is at least one example of a
bioelectrogenic teleost that does not possess any evident electroreceptive
capability (Bullock et al., 1983; and see below). For those fish that possess
electrogenic and electroreceptive organs, the electric field generated during an
EOD is monitored by an array of electroreceptors distributed over the fish’s skin.
The electric organ and the electroreceptors working in tandem constitute an
       1491

effective sensory-motor system that is particularly important for electrolocation

and communication. The co-ordinated action of the motor and the sensory
components leads to what is called active electrolocation, as opposed to the
passive electrolocation present in those fish that are only electroreceptive.
Alves-Gomes (1999) drew attention to the fact that electric organs and
electroreceptors represent distinct evolutionary novelties, and used the term
‘ Electrogenic and Electrosensory System ’ (EES) to refer to both sets of organs
working as a functional unit, thus emphasizing their co-ordinated performance.

PHYLOGENETIC OCCURRENCE OF ELECTRORECEPTION IN TELEOSTS

Electroreceptors can be divided into two major classes according to their
morphological and physiological properties: ampullary and tuberous
electroreceptors. Ampullary receptors respond optimally to DC signals and
low-frequency AC signals of biological and non-biological origin. These types of
low-frequency electricity detectors have been identified either morphologically or
physiologically in only four teleost orders (see below and Fig. 1), but their origin
is found in the early Paleozoic (500–600 million years ago), as they are present in
the Petromyzontiformes (lampreys), in all Chondrichthyes (cartilaginous fish),
in the Sarcopterygii (Dipnoi, Coelacanthimorpha and in some amphibians), and
in both extant Chondrostean orders (Ascipenseriformes and Polypteriformes)
(Bullock et al., 1983; New, 1997).
Although it remains uncertain whether all non-teleost electroreceptors are
homologous, there are several lines of evidence suggesting that ampullary
electroreception was lost in the teleost ancestor and evolved de novo more
recently within the group. First, there is neither physiological nor anatomical
evidence that electroreception is present in Lepisosteus Lacepède and in Amia
Linnaeus (Bullock et al., 1983; Northcutt, 1986) the two closest extant relatives
of teleosts (Nelson, 1994; de Pinna, 1996; Gardiner et al., 1996). Second, only
four derived teleost orders, out of more than 35 extant, have electroreceptive
representatives. This limited distribution suggests an absence of electroreceptors
in the clades’ basal state. Third, there are significant physiological and anatom-
ical differences between teleost and non-teleost ampullary systems. In non-
teleosts, primary electroreceptive information is conveyed to the medullary
octavolateralis nucleus, and ampullary electroreceptors respond to cathodal
stimulus polarity. The ampullary electroreceptors present in teleosts are respon-
sive to anodal stimuli instead, and electroreceptive information is first relayed
to the electroreceptive lateral line lobe in the medullar (Bennett, 1971b;
McCormick, 1982, 1983; Obara & Sugawara, 1984; Finger et al., 1986;
Northcutt, 1986; Zakon, 1986, 1987).
Among teleosts, ampullary electroreceptors are found only within two
distantly related and large groups (Fig. 1), namely the superorders
Osteoglossomorpha and Ostariophysi. According to our current understanding
of the phylogeny of these clades, teleost ampullary-like receptors evolved once in
the common ancestor of Siluriformes+Gymnotiformes (Fink & Fink, 1981,
1996; Alves-Gomes, 1995), and again in the ancestor of Notopteriformes+
Mormyriformes. The situation of notopteriforms and mormyriforms is
particularly interesting as one takes the osteoglossomorph phylogeny into
consideration and the fact that ampullary electroreceptors are present in the
1492 . . -

Semionotiformes

Amiiformes

Mormyriformes
?

Osteoglossomorpha
African notopteriforms
Neopterygii
Asian notopteriforms

Osteoglossiformes

Hiodontiformes

Elopomorpha
(157 genera)
Teleostei
Clupeomorpha
(68 genera)

Gymnotiformes

Siluriformes

Ostariophysi
Characiformes

Cypriniformes

Gonorynchiformes

Euteleostei Remaining teleosts

(27 orders)
F. 1. Cladogram depicting the appearance of ampullary electroreceptors in extant teleost fish,
represented as dotted vertical bars in the tree. Among ostariophysans, ampullary electrodetection
evolved once in the common ancestor of catfishes (Siluriformes)+South American electric fishes
(Gymnotiformes). Within the Osteoglossomorpha, there are two fish clades that are electro-
sensitive: the Mormyriformes and the African Notopteriformes. It is very likely that ampullary
organs evolved once in the common ancestor of the Mormyriformes and for a second time in the
African Notopteriformes. However, other hypotheses are also plausible (see Fig. 2). The
cladogram was compiled from Nelson (1994), Johnson & Paterson (1996), Lecontrie & Nelson
(1996), and de Pinna (1996).

African but not in the Asian notopteriforms (Braford, 1982, 1986). It is

well established from wide sources of evidence, including morphological and
molecular studies, that Mormyriformes and Notopteriformes are sister groups
(Greenwood, 1971, 1973; Lauder & Liem, 1983; Benveniste, 1995; Li & Wilson,
1996). However, within Notopteriformes, the African genera Xenomystus
Günther and Papyrocranus Greenwood are electroreceptive whereas the Asian
genera Notopterus Lacepède and Chitala Fowler are not (Braford, 1982, 1986).
Braford (1986, fig. 7) already considered the possibility that the order
Notopteriformes could be an unnatural clade, and that perhaps the African
notopteriforms were the sister group of Mormyriformes. Such a hypothesis
appears improbable, due to the obvious morphological similarities among the
Asian and African notopteriforms, but further phylogenetic studies are required
before the possibility that Notopteriformes is not monophyletic can be
       1493

(a) Mormyriformes

African notopteriforms

Asian notopteriforms

Osteoglossiformes

(b) Mormyriformes

African notopteriforms

Asian notopteriforms

Osteoglossiformes

(c) Mormyriformes

African notopteriforms

Asian notopteriforms

Osteoglossiformes
F. 2. There are three possible scenarios for the evolution of ampullary receptors between mormyriforms
and notopteriforms. (a) The ampullary organs evolved once on the common ancestor of the
Mormyriformes and again in the African Notopteriformes. Such scenario demands two steps, with
a convergent evolution of electroreceptors between the two clades. (b) Ampullary electroreceptors
first appeared in the common ancestor of Notopteriformes+Mormyriformes and subsequently the
Asian genera lost their ampullary system. Such scenario also requires two steps, being one gain
and one lost. (c) A third hypothesis, already considered by Braford (1986) is that the African
notopteriforms are the sister group of the Mormyriformes. In this case Notopteriformes would be
paraphyletic and the ampullary system would have evolved only once: in the common ancestor of
Mormyriformes+African Notopteriformes. The dashed vertical bars and branches represent the
appearance of ampullary receptors, and the dotted bar and branch represents the loss of receptors.

discarded. Until then, there are three possible scenarios for the evolution of
ampullary electroreceptors in these fish (Fig. 2). If we accept the conventional
hypothesis, i.e. that Notopteriformes is monophyletic, then it is equally parsi-
monious to consider that ampullary electroreception evolved in the common
ancestor of Mormyriformes and Notopteriformes and that the Asian clade lost
it (2 steps), as it is to consider that ampullary electroreceptors evolved twice
and independently in the mormyriforms and in the African notopteriforms
(2 steps). On the other hand, if the African notopteriforms are shown to be
more closely related to the mormyriforms, then the most likely hypothesis
would be that electroreception was present in the common ancestor of
Mormyriformes+African ‘ notopteriforms ’ and that ampullary electroreceptors
never evolved in the Asian clades. As it seems very unlikely that evolutionary
processes would select against the maintenance of an electroreceptive capability
1494 . . -

Semionotiformes

Amiiformes

Mormyriformes

Osteoglossomorpha
African notopteriforms
Neopterygii
Asian notopteriforms

Osteoglossiformes

Hiodontiformes

Elopomorpha
(157 genera)
Teleostei
Clupeomorpha
(68 genera)

Gymnotiformes

Siluriformes

Ostariophysi
Characiformes

Cypriniformes

Gonorynchiformes

Euteleostei Remaining teleosts

(27 orders)
F. 3. Cladogram displaying the evolution of tuberous receptors in teleosts. This type of electroreceptor,
physiologically tuned to detect alternating electric signals with carrier frequencies very close to the
fish’s own EOD, are assumed to have evolved three times independently among teleosts: in the
common ancestor of the extant Mormyriformes (dotted vertical bar and branch), in the common
ancestor of Gymnotiformes (dotted vertical bar and branch), and in one single lineage within
the siluriforms (grey vertical bar and black branch): the South American cetopsid catfish
Pseudocetopsis sp. (see Fig. 4). Cladogram adapted from Nelson (1994), Johnson & Paterson
(1996), Lecontrie & Nelson (1996), and de Pinna (1996).

in an aquatic organism, especially a fish, the scenario of convergent evolution of

ampullary electroreceptors between the mormyriforms and the African
notopteriforms is favoured.
Within the Ostariophysi, there is a strong body of evidence that Siluriformes
and Gymnotiformes are sister groups (Fink & Fink, 1981, 1986; Alves-Gomes,
1995; Dimmick & Larson, 1996), and the monophyly of the Siluriphysi (sensu
Fink & Fink, 1996) is not currently disputed. Since electroreceptors have been
described in all catfish examined so far, it is possible that, in this case,
ampullary-type electroreceptors evolved once in the common ancestor of catfish
and electric knife fish.
The second class of electroreceptors, the tuberous electroreceptors, is known
to be present only in those clades that also have electric organs, with only one
known exception to date (Fig. 3). Tuberous receptors are found in the South
       1495

American Gymnotiformes as well as in the African Mormyriformes, and are

physiologically tuned to alternating electric signals of high carrier frequencies,
being most sensitive to the dominant frequencies of the fish’s own EOD (Obara
& Sugawara, 1984; Zakon, 1986). In contrast to the ampullary electroreceptors,
tuberous electroreceptors are actually subdivided into different classes in both
Mormyriformes and Gymnotiformes according to their physiological properties,
but in both fish groups they code the amplitude and the time of the zero crossing
(phase) of the fish’s own EOD (reviewed in Zakon, 1986). Because these
receptors are mainly tuned to the fish’s own EOD frequencies, they are of special
relevance during intra and interspecific communication. Despite being physio-
logically similar, the tuberous electroreceptors found in Mormyriformes and
Gymnotiformes are anatomically quite distinct (Zakon, 1986, 1987) and repre-
sent another extraordinary example of convergence (homoplasy) between the
African and South American clades.
Since the presence of a tuberous receptor has been associated with electrogenic
fish only, the morphological description of a tuberous electroreceptor in the
genus Pseudocetopsis Bleeker (Fig. 3), a South American catfish from the family
Cetopsidae by Andres et al. (1988) was unexpected. The fish shown in figure 1
of Andres et al. (1988) as an undescribed species of Pseudocetopsis, in fact,
appears to be a species of the genus Hemicetopsis. In general, Pseudocetopsis has
a larger gill aperture, larger mouth and a body that is taller and shorter than
the fish shown in the figure (J. Zuanon & L. Rapp Py-Daniel, pers. comm.).
However, since a formal re-evaluation of the specimen is not available,
Pseudocetopsis is used throughout this paper. The physiological properties of this
receptor and its behavioural relevance however still remain to be studied.
Andres et al. (1988) noted that the species studied was judged to be blind.
Despite its reduced eyes, further studies of this catfish would help to determine if
complete blindness is really the case. Blindness would confer an additional
ecological and behavioural relevance to the presence of tuberous electroreceptors
in this catfish. It would be interesting to verify if the physiological tuning of
Pseudocetopsis’s electroreceptors allows this species to detect gymnotiforms’
EODs, since they may be sympatric, or if there is any kind of behavioural or
ecological relationship between these fish. Nevertheless, the presence of these
receptors in Pseudocetopsis confer to this genus a differentiated status within the
siluriform phylogeny, since it holds important information about the evolution
of electrodetection and its utilization in ostariophysan fish. It is also possible
that, instead of using its tuberous receptors to monitor external sources of
electric potentials, perhaps Pseudocetopsis is monitoring an endogenous signal,
such as the field potential of a very active muscle. As will be discussed below,
electric organs have evolved several times among catfishes, but always in African
clades. If there are electrogenic catfish in South America, cetopsids may be
strong contenders.

PHYLOGENETIC OCCURRENCE OF ELECTRIC ORGANS IN TELEOSTS

According to our current understanding of fish phylogeny, electric organs have
evolved independently eight times in the teleost lineage (Fig. 4), and up to five
times within the Superorder Ostariophysi alone (Fig. 5). The independent
(homoplasic) evolution of electric organs in several fish lineages must reflect, at
1496 . . -

Mormyriformes
Asian notopteriforms
African notopteriforms
Osteoglossomorpha Osteoglossiformes
Teleostei Hiodontiformes
Elopomorpha - 4 orders
Gymnotiformes
Clupeiformes Siluriformes (4 times)
Characiformes
Ostariophysi - 5 orders Cypriniformes
Gonorhynchiformes
Protacanthopterygii - 3 orders
Stenopterygii - 2 orders
Aulopiformes
Myctophiformes
Euteleostei Lampridioformes
Polymixiiformes
Paracanthopterygii - 5 orders
Acantopterygii Mugiliformes
Atherinomorpha - 3 orders
Percomorpha Tetraodontiformes
Pleuronectiformes
Scorpaeniformes
Synbranchiformes
Gasterosteiformes
Zeiformes
Stephanoberyciformes
Beryciformes
Perciformes (2 times)

F. 4. Electric organs in teleosts. Fish lineages with representatives possessing an electric organ
are depicted by dotted lines. Electric organs are assumed to have evolved eight times among
teleosts: within the Osteoglossomorpha, in the common ancestor of Mormyriformes; within the
Ostariophysi, in the common ancestor of Gymnotiformes and four times among the Siluriformes
(see Fig. 4); and within the Percomorpha, in two uranoscopid genera of the order Perciformes.
Additional studies may change the current view, either by revealing new phylogenetic relationships
among and between the electrogenic lineages, or by the discovery of new electrogenic taxa.
Uranoscopids, Malapterurus, Auchenoglanis and the remaining auchenoglanidids, and the
cetopsids are groups requiring closer investigation. Cladogram compiled from Nelson (1994),
Johnson & Paterson (1996), Lecontrie & Nelson (1996), and de Pinna (1996).

least in part, the large benefits of such evolutionary novelty in aquatic organisms
especially if electroreceptive capability is already present. EODs range from
weak (up to few volts, as in the great majority of electrogenic teleosts) to
intermediate (tens of volts such as in Astroscopus Brevoort) to strong (hundreds
of volts as in Malapterurus Lacepède and Electrophorus Gill). Weak discharges
are mainly used as a part of the EES for active electrolocation of organisms and
objects, and for communication. Strong discharges can be used to stun prey and
as a defensive mechanism.
In the osteoglossomorphs, an electric organ was presumably present in the
common ancestor of all mormyriforms. Within the ostariophysans, the subject
becomes more complex, as electric organs evolved in the gymnotiforms’ ancestor
and in four siluriform genera: Clarias Scopoli, Malapterurus, Auchenoglanis
Günther and in Synodontis Cuvier (Hagedorn et al., 1990; Baron et al., 1994a,b;
Moller, 1995; Baron et al., 1996a, b). Until recently, these four genera were
believed to be only distantly related, but new evidence based upon morphological
       1497

Pimelodinae
some Bagridae
Claroteidae
Schilbidae
Pangasiidae
Horobagrus
Austroglanididae
Clariidae
Plotosidae
Chacidae
Malapteruridae
Auchenoglanidinae
Siluridae
Ariidae
Mochokidae
Auchenopteridae
Doradidae
Ictaluridae
Cranoglanididae
some Bagridae
Heptaterinae
Pseudopimelodinae
Aspredinidae
Erethistidae
Sisoridae
Siluriformes Akysidae
Amblycipitidae
Hemicetopsis
Amphiliidae
Loricariodea Cetopsis
Cetopsidae Pseudocetopsis
Cetopsogiton
Diplomystes
Denticetopsis
Bathycetopsis
Gymnotiformes

F. 5. Cladogram depicting a recent phylogenetic hypothesis for the order Siluriformes (modified from
de Pinna, 1996) and the evolution of tuberous electroreceptor and electric organs within the order.
The dashed vertical bars and branches show the occurrence of tuberous electroreception, whereas
the dotted bars and branches the evolution of electric organs among the catfish. Within the
Ostariophysi, tuberous electroreceptors are assumed to have appeared in the common ancestor of
all the extant gymnotiform lineages. The only catfish lineage for which tuberous electroreceptors
have been described is Pseudocetopsis sp., a South American species. However, it possible that
Andres’ et al. (1988) work was based upon a misidentified specimen of Hemicetopsis. Further
phylogenetic analyses about this group are urgently necessary. The paper by Andres et al.
describes the tuberous electroreceptor morphologically. Complementary physiological exper-
iments would help to establish not only if the receptors are functionally similar to other tuberous
receptors, but also if Pseudocetopsis can detect the gymnotiforms’ EODs, or even if Pseudocetopsis
is monitoring its own electric potentials. Electric organs were already identified in four siluriform
genera Clarias, Synodontis, Malapterurus and Auchenoglanis. Since there is good morphological
evidence pointing to Malapteruridae as the sister group of auchenoglanidids (de Pinna, 1993,
1996), it may be possible that an electric organ was already present in the common ancestor of the
two clades and a single evolutionary event happened, specially if other auchenoglanidids are also
electrogenic.

characters has pointed to a close phylogenetic relationship between

Malapteruridae and Auchenoglanididae (the latter was formerly considered a
subfamily of Bagridae) (de Pinna, 1993). De Pinna (1993) further suggests that
Malapterurus may be more closely related to two other auchenoglanidid genera
1498 . . -

(Notoglanidium Günther and Liauchenoglanis Boulenger) than to Auchenoglanis.

A more complete study of the phylogenetic relationships among Malapterurus
and the members of Auchenoglanididae would help to determine if the common
ancestor of the two clades was already electrogenic, or if electric organs evolved
more than once among these clades. Likewise, further studies are needed in
order to clarify the phylogenetic relationships of the electrogenic clades in
relation to the remaining catfish. Until more information is available, I will
assume that an electric organ evolved independently in Malapterurus and in
Auchenoglanis and, therefore, there were four independent evolutionary events of
electric organ appearance within the siluriforms.
The other teleosts with an electric organ are the two genera of the perciform
family Uranoscopidae: Astroscopus and Uranoscopus Linnaeus (Bennett, 1971a;
Moller, 1995). The order Perciformes, according to Nelson (1994), contains
about 9300 species, but only the two uranosopid genera above are known to
produce EODs. According to morphological studies (Pietsch, 1989), these two
genera are not sister groups. Furthermore, it has been shown that their electric
organs are derived from different sets of muscles (Moller, 1995) and therefore are
not homologous. Such evidence very strongly suggests two events among the
uranoscopids.
In summary, electric organs appear to have evolved independently in
the following teleost lineages: (1) Mormyriformes, (2) Gymnotiformes,
(3) Synodontis, (4) Clarias, (5) Malapterurus, (6) Auchenoglanis, (7) Astroscopus,
and (8) Uranoscopus. In all the cases studied, electrogenic cells (electrocytes)
appear in ontogeny as specialized cells differentiated from myocytes from various
portions of the body (review in Bass, 1986). Ontogenetic information is still
lacking for the siluriform genera Auchenoglanis and Clarias. In both genera the
exact location and the embryological origin of electric organs still has yet to be
discovered (Baron et al., 1994b, 1996b). In Mormyriformes, electrocytes are
associated with the caudal peduncule musculature in mormyrids, and are
modified from tail muscles in Gymnarchus Cuvier (Dahlgren, 1914; Srivastava &
Szabo, 1972). In most gymnotiforms as well as in the siluriform Malapterurus,
electric organs are derived from trunk or hypaxial musculature (Johnels, 1956;
Bennett, 1971a; Kirschbaum, 1977, 1983). In all species of Synodontis examined,
EODs are believed to be generated by an electrogenic tissue associated with the
sonic muscle which lies next to the swim bladder (Hagedorn et al., 1990). In the
uranoscopids, electrogenic tissue is derived from the eye musculature in
Astroscopus (White, 1918) and from sonic muscles in Uranoscopus (Mikhailenko,
1973 in: Moller, 1995).
In gymnotiforms and mormyriforms, embryological studies have shown that
the larvae possess a larval electric organ, also derived from muscular cells, that
may or may not persist in the adults (Kirschbaum, 1977, 1983; Postner &
Kramer, 1995; Franchina, 1997). Further, several gymnotiform genera of the
Rhamphicthyioidea clade (families Hypopomidae+Rhamphicthyidae) also have
accessory electric organs, but their embryological origin is not clear. In the
gymnotiform family Apteronotidae, the initial myogenic electric organ is
replaced, during the first 60–70 days of life, by an adult electric organ formed
only of motor neurons (Kirschbaum, 1983). By having a ‘ neurogenic ’ electric
organ and, therefore, mainly electrical synapses associated with the EOD
       1499

generation, the apteronotids are able to produce the highest repetition rates
known for any electric fish, with carrier frequencies that exceed 1500 Hz. There
is still a great deal to learn about the ontogenetic development of the electric
organ in most of the electrogenic genera.
Despite the diversity of electric organs, the physiological principles driving
bioelectrogenesis are quite similar among all teleosts: the excitable membrane(s)
of the electrocytes generates an action potential under cholinergic excitation
from spinal motor neurons. However, in the apteronotids, the EOD is produced
by the action potential of the neurons. Although sharing the same basic
principles, EODs become species specific once the waveforms depend upon a
complex interaction of several anatomical and physiological variables. Among
these are the innervation pattern and the distribution of ionic channels in
the electrocytes, the number of excitable membranes of the cells, the number
and disposition of electrocytes in the electric organ, and the presence or absence
of accessory electric organs in the fish (review in Bass, 1986). According to their
temporal patterns, EODs have been classified as two basic types: pulse-type
EODs are characterized by a long interval between successive spikes, whereas
wave-type EODs contain interspike intervals that are less distinct and
the waveform assumes a distorted sinusoidal shape when displayed on an
oscilloscope screen.
The vast majority of electrogenic teleosts produce pulse-type discharges with
rates of <10 – >100 Hz, depending upon the species and whether the fish is at
rest or active. Wave-type discharges evolved three times among teleosts. Within
gymnotiforms, wave-type EODs have evolved twice (Alves-Gomes et al., 1995):
in the genus Sternopygus Müller & Troschel and in the common ancestor of
Apteronotidae+Eigenmanniidae. The gymnoliform genus Microsternarchus
Fernández-Yépez, with a pulse of relatively long duration (3–5 msec) and a very
stable firing rate (Sullivan, 1997; J. A. Alves-Gomes, pers. obs.), currently
represents a transition from pulse to wave. The only other wave-type
electrogenic teleost fish is the mormyriform Gymnarchus. Species with wave-type
discharges may fire their electric organ with repetition rates of <100 Hz such as
in gymnotiform Sternopygus, up to >1500 Hz as in some genera of the
gymnotiform family Apteronotidae. Both uranoscopid genera produce pulse-
type EODs, generated mainly during feeding activity or when the fish is
disturbed (Pickens & McFarland, 1964). All electrogenic catfishes also produce
pulse-type EODs.

EVOLUTION OF ELECTRIC ORGANS AND EOD WAVEFORMS

As one maps the evolution of electric organs on teleost phylogeny, it appears
that, with exception of the uranoscopids, all electric organs evolved in fish that
were already electroreceptive. Furthermore, it is likely that the common
ancestor of the electroreceptive teleosts had only ampullary organs, with
tuberous electroreceptors evolving later in a few select electrogenic groups. The
development of active electrolocation (i.e. an electric organ) on top of an already
existing electroreceptive capability probably represents a relatively minor step
for a great reward in terms of the evolutionary fitness gained. A probable
scenario is as follows: if a particular set of highly active muscle of an already
1500 . . -

electroreceptive fish increased the peak-to-peak voltage of its action or contrac-

tion potentials, then the signal could become strong enough to be detected by the
fish’s own electroreceptors. Because ampullary receptors are physiologically
tuned to low-frequency alternating current (AC) or direct current (DC) signals,
there must have been an evolutionary advantage for signals that matched the
electroreceptors’ tuning curve. The possibility of monitoring its own electric field
would enhance the fish’s ability to navigate, orientate and to communicate. A
key component of this hypothesis is that plesiomorphic waveforms were com-
posed of low-frequency signals, such as long lasting monophasic discharges.
There are numerous reasons to infer a monophasic or quasi-monophasic EOD
waveform, generated by a ‘ simple ’ electric organ, as the plesiomorphic con-
dition in fish. The anatomical and physiological features of existing electric
organs analysed from a phylogenetic perspective, and the fact that in all teleosts
studied to date electric organs have been ontogenetically associated with
muscular precursors, suggest that the cells of the plesiomorphic electric organs,
like muscles in general, had a simple innervation pattern. Such a pattern, for
instance, would imply a cell with a single excitable membrane, or the terminals of
the motor neurons driving the electric organ’s electrocytes arriving at only one
side of the cell, either in the anterior or in the posterior membrane. This type of
innervation and excitation pattern, currently found in several electric fish,
produces a monophasic EOD, as a single depolarizing event occurs, with current
flowing in only one direction during the discharge of the electric organ’s
electrocytes. Since Lissmann’s study (1958), several authors have reinforced the
idea of a plesiomorphic monophasic pulse (Hopkins & Heiligenberg, 1978;
Kirschbaum, 1995; Stoddard, 1999). It is suggested by the present author that
the ancestral pulses were probably of large duration to maximize ampullary
detection.
The condition of a simple, monophasic pulse as the first state during the
evolution of electric organs in fish finds corroboration in additional lines of
evidence. The only non-teleost electrogenic fish, the elasmobranchs of the genus
Raja, Torpedo and Narcine, have a monophasic EOD (Keynes, 1957; Bennett,
1971a). Among the electrogenic teleosts, the basal lineage within the
Mormyriformes is Gymnarchus, a fish with a monophasic EOD and a simple
innervation pattern (Taverne, 1972; Alves-Gomes & Hopkins, 1997).
Gymnarchus is also the only Mormyriform with a wave-type discharge. Here it
is assumed that pulse-type EODs were the original condition due to the
plesiomorphic condition of muscle action potentials (Hopkins & Heiligenberg,
1978) and also because the transition from a monophasic pulse to a wave-type
discharge does not require major anatomical or physiological changes. A pulse
fish may change its EOD to a wave-type by simply increasing the duration of the
EOD (or shortening the interval between EODs) and stabilizing the firing rate of
its electric organ. Such a transitional state can currently be found in the
gymnotiform genus Microsternarchus, a pulse-type fish with relatively long pulse
duration and a very stable repetition rate.
In the case of Gymnotiformes, while there is no consensus about the basal
lineage within the order, there is agreement that the wave-type fish of the families
Eigenmanniidae (sensu Alves-Gomes et al., 1995) and Apteronotidae, are derived
lineages (Alves-Gomes et al., 1995; Albert & Campos-da-Paz, 1998). According
       1501

to Alves-Gomes et al. (1995) either Sternopygus or Electrophorus+Gymnotus

Linnaeus represent the sister group lineage of all remaining gymnotiforms.
Sternopygus has a monophasic wave discharge on top of a negative baseline, with
the slowest repetition rate recorded for a wave-type gymnotiform (below
100 Hz). As in the case of Gymnarchus, it is believed that the current wave-
type EOD in Sternopygus is a derivation of an original pulse-type discharge
(Alves-Gomes et al., 1995; Alves-Gomes, 1998). The second contender for a
basal gymnotiform lineage is the Electrophorus+Gymnotus clade. Electrophorus
is a monotypic genus and possesses a monophasic pulse, whereas Gymnotus is
composed of 15 nominal species plus several currently under descrip-
tion (Mago-Leccia, 1994; Fernandes-Matioli, 1999; W. G. R. Crampton,
pers. comm.) with complex, multiphasic EODs. Gymnotus cylindricus La Monte
from Central America has reversed its EOD into a monophasic discharge
(Stoddard, 1999). The evolution of multiphasic EODs found in several electric
fish clades can be related to a large number of environmental-driven factors
associated with several types of evolutionary constraints. For now, it is worth
mentioning that the development of multiphasic EODs is an effective way to
increase waveform diversity and consequently to obtain species specificity within
specious clades.
In catfishes (Siluriformes), electric organs have been described in four lineages
so far. In two of them there is strong indication that the initial condition was a
monophasic pulse. Malapterurus was first thought to produce head-negative,
purely monophasic pulses. However, through more elaborate recordings made
in the sixties, it was possible to identify a very small positive phase in the EOD
of this fish, which was explained by the depolarization of the enervating stalk of
the electrocyte (Bennett, 1971a). Auchenoglanis has a biphasic pulse, but we do
not presently know if its EOD is a plesiomorphic or derived condition within the
auchenoglanidids, since it is still to be established if other genera in the clade are
electrogenic. It is also crucial to know the phylogenetic relationships among the
different genera of the clade and between them and the other siluriforms,
including Malapterurus. Clarias produces long lasting monophasic discharges
during agonistic encounters, although the exact location and anatomy of the
electric organ is not well known (Baron et al., 1996a,b). The fourth catfish
lineage, the genus Synodontis (family Mochokidae), is composed of >100 species
(Nelson, 1994) for which no phylogenetic hypothesis is available. The original
paper describing EODs in this genus is that of Hagedorn et al. (1990), with three
species studied: Synodontis nigrita Valenciennes, S. obesus Boulenger and S.
schoutedeni David. Later, weak electric activity was described in S. schall Bloch
& Schneider (Baron et al., 1994a). Recent and unpublished data (V. Baron, pers.
comm.) indicates that several other species of Synodontis are also electrogenic.
Considering those species for which EOD waveforms are available, none possess
a truly monophasic EOD, but S. schall has a very small negative phase after a
positive pulse, giving a quasi-monophasic aspect to the pulse (Baron et al.,
1994a), similar to Malapterurus but of opposite polarity. It is notable that, as
in Clarias, S. schall only produce EODs during social interaction. During
aggressive interactions for instance, the number and the amplitude of the EODs
increase as the inter-spike interval decreases. Eventually the successive EODs
merge and a long monophasic discharge results, i.e. a signal that can strongly
1502 . . -

stimulate the ampullary system. Until more complete studies on the phylogeny
of the genus Synodontis are available, it is not possible to know if the biphasic
EOD waveforms represent a derived condition. Still in relation to catfishes, it
would be interesting to investigate if tuberous-like electroreceptors are present in
any genera that produce biphasic pulses, or pulses with high frequency compo-
nents. It is also intriguing, considering the recent discovery of new electrogenic
catfish genera, that all of them only occur in Africa. It is my personal belief that
electrogenic South American catfish are very likely to exist, and are waiting to be
discovered and studied.
The EODs of Astroscopus and Uranoscopus, the two electrogenic
acanthopterygians of the order Perciformes, despite being generated by
electrogenic tissues derived from two different muscle groups, are also
monophasic (Bennett & Grundfest, 1961; Bennett, 1971a; Baron & Michaelenko,
1976).
Another important source of corroboration for a plesiomorphic monophasic
pulse in teleosts is that genera with adult multiphasic EODs, such as the
gymnotiforms Brachyhypopomus Mago-Leccia and Apteronotus Lacepède and
the mormyriforms Pollimyrus Taverne and Mormyrus Linnaeus, have a
monophasic EOD during the early stages of ontogenic development
(Kirschbaum, 1977, 1983, 1995; Postner & Kramer, 1995; Franchina, 1997). The
more complex waveform is acquired as the fish grows and the firing physiology
of the electrocytes becomes more complex. It is likely that as more species are
studied, other larval monophasic EODs will be found.
Nevertheless, it would be misleading to conclude that complex, multiphasic
EOD waveforms are always derived because in the Gymnotiformes there are at
least two known cases in which a species nested within a genus in which all the
representatives that have bi- or multiphasic EOD has reversed its discharge to a
monophasic pulse. Monophasic EODs are found in one species of Gymnotus
from Central America (Stoddard, 1999), in a new Brachyhypopomus species
(J. Sullivan, pers. comm.), and in an undescribed species of Microsternarchus
(Alves-Gomes, unpubl. data). In mormyriforms, at least one species,
Brienomyrus batesii Boulenger, has also reversed its EOD to a head-negative
monophasic pulse (Alves-Gomes & Hopkins, 1997).
The development of a multiphasic, complex EOD waveform was probably the
best evolutionary option to solve two significant limitations of monophasic
pulses. First, it allowed a much larger number of possibilities in terms of
waveforms, supporting species specificity. Second, by adding fast-frequency
components in the EOD, fish were able to broaden the spectral frequency of their
discharges. As the discharge frequencies will be differentially attenuated, accord-
ing to the electrical properties of the different elements in the habitat, broader
spectral frequencies may be advantageous by improving the efficiency of the EES
to probe the environment. However, if this type of electrical signal, containing
fast components, is to be effective, the fish require an electroreceptor physiolog-
ically tuned to the frequency spectrum of the new waveform. This role was filled
by the tuberous electroreceptors as we find in gymnotiforms and mormyriforms.
A major puzzle regarding the evolution of electric organs in fish are the
two uranoscopid genera. Bullock et al. (1983) examined the brain anatomy and
recorded evoked potentials of Astroscopus during several types of stimuli,
       1503

including electric, and concluded that the genus does not possess electroreceptive
capabilities. Therefore, the fish cannot use electric discharges for any type of
social interaction or electrolocation. No studies regarding the electroreceptive
capabilities of Uranoscopus were carried out. It is known that Astroscopus
always activates its electric organ during feeding activity, whereas in
Uranoscopus the electric organ is associated with the sound producing muscles.
The evolutionary driving forces in this case are less apparent, and additional
studies on the embryogenesis and utilization of the electric organs in both genera
are needed. However, the probability that the two uranoscopid genera would,
only by chance, develop electric organs completely independently from each
other is about the inverse of the total number of marine teleost species. Thus,
uranoscopids appear to possess a particular tendency favouring electric organ
evolution, although the evolutionary nature of this feature is not clear.

EODs AND ENVIRONMENTAL CONSTRAINTS

Presumably, EOD waveforms would evolve so as to increase a fish’s chances to
survive and reproduce in its environment. It is beyond the scope of this paper to
discuss in detail all the variables that may influence the development of an
effective EOD. Here, the focus has been on some of the relevant ecological and
environmental aspects that may influence the evolution of the EOD waveform.
According to theory, fish EODs should reflect the best compromise possible
between the generation of a signal that maximally exploits the sensitivity of the
electroreceptors allowing for efficient electrodetection and electrocommuni-
cation, while at same time being cryptic to predators (Bradbury & Vehrencamp,
1998).
The first relevant aspect considered in this complex equation is habitat
composition, as different elements in the environment with different capacitive
and/or resistive properties will affect differentiatlly the spectral components of
the EODs (von der Emde, 1990). For instance, lower frequencies are more
attentuated by capacitive elements such as dense vegetation than are higher
frequency EODs. Therefore, a fish living within dense vegetation would benefit
by having an EOD with high frequency components, as in the case of fish with
very short (fast) pulses or high-frequency wave-type fish. Rocky and sandy
substrata also have different electrical properties than muddy or soft substrata
and affect the EODs differently. Taking these few basic physical principles into
consideration, an EOD waveform will be more or less efficient depending upon
whether a fish lives or forages in open water or in dense vegetation, near the
bottom or in the water column. Hopkins (1999) has shown a direct correlation
between the electric organ anatomy (number of electrocytes per row and per
column) and the physico-chemical properties of the water. The electric organs of
the different species appear to have adapted to produce EODs that match the
impedance of the water in which the fish lives as an evolutionary solution to
maximize the output signal and to literally save energy. Under this circum-
stance, once an electric organ becomes well adapted to a certain habitat, with a
particular type of water, the exploration of a different environment may imply
less efficiency. Therefore, water conductivity may also work as an ‘ invisible
barrier ’ for different species (Hopkins, 1999). The electric properties of different
1504 . . -

food items are also important. Piscivorous fish present an electrically different
target compared to insect larvae or crustaceans that have highly resistive
carapaces and appendages. The water velocity of the habitat in which the fish
lives is also important. Fast moving waters require a better temporal resolution
than lentic environments. High repetition rates become advantageous in
fast flowing rivers or streams. Crampton (1988b) has published an important
study about gymnotiforms in their natural habitats, and demonstrated a good
correlation between EOD types and habitat preference. Some clades, like the
neurogenic and high-frequency wave-type apteronotids, are very unlikely to be
found in stagnant waters; on the other hand, slow repetition rate pulse-type fish
such as Brachyhypopomus are mainly found in calm waters, and are never found
in the main river channels (Cox Fernandes, 1995; Crampton, 1998b). Some
gymnotiform species have become highly tolerant to low levels of oxygen or have
developed auxiliary breathing mechanisms to deal with oxygen depletion in some
habitats during the dry season in the Amazon (Johansen et al., 1968; Crampton,
1998a,b). Alves-Gomes et al. (1995) have addressed briefly the relationship
between phylogeny and EODs in some pulse-type gymnotiforms, but further
generalizations are difficult, once there are pulse species living in relatively fast
flowing waters, and wave species that can be found in lentic habitats (Crampton,
1998b; Alves-Gomes, pers. obs.). The argument here is that the EOD waveform
must be suited to the microhabitat in which the fish lives, as a function of fish’s
own ecological and behavioural needs, but a clear relationship between type of
EOD and habitat characteristics require further studies.
Another important environmental aspect is predator avoidance. Active
electrolocation, from a functional point of view, combines properties found in
other senses such as vision, hearing and the lateral line. In other words,
electrolocation could be considered a ‘ multi-modal ’ sense that, for instance,
allows the fish to explore their environment without the need for light. The
nocturnal habits of most electric fishes serve to minimize predation by visual
predators. However, in tropical environments there are large numbers of
nocturnal electroreceptive predators. In Africa, catfishes and Gymnarchus are
the electroreceptive predators. In South America, catfishes are joined by several
piscivorous gymnotiforms genera such as Electrophorus, Gymnotus, several
apteronotids, large Sternopygus to a lesser extent, and perhaps few large
hypopomids that may prey on fish larvae. In order to avoid predation, some
small pulse emitting gymnotiforms like Brachyhypopomus can, for example, cease
to emit EODs for brief moments as a predator like Electrophorus approaches.
Other hypopomids cease the emissions from their electric organ for different
period of times when mechanically disturbed (Alves-Gomes, pers. obs.). Such
behaviour is neurophysiologically mediated in this fish by the release of an
inhibitory neurotransmitter (GABA) in their pacemaker nucleus (Kawasaki &
Heiligenberg, 1990). Other strategies have also evolved to avoid detection by
electroreceptive predators. One such mechanism is to shift the peak of the
spectral frequencies of the EOD away from the turning curve of the predator’s
electroreceptors. It has been proposed that predation may drive EOD waveform
evolution in electric fishes (Stoddard, 1999). Adding a second phase on top of a
monophasic pulse, shortening the duration of a pulse, or becoming a wave-type
with high carrier frequencies, may cause the shift of the EOD spectral peak
       1505

frequency above ampullary thresholds. Moreover, considering that the large

majority of predatory pressure comes from catfishes, shifting the EODs’ funda-
mental frequency away from the ampullary receptor physiology appears as a
sensible alternative. This is what apparently happened with some of the
wave-type clades, most notably in the gymnotiform family Apteronotidae. None
of its species have adults EOD carrier frequencies below 650 Hz, which are very
unlikely to be detected by catfishes. There is no evidence yet that a neurogenic
electric organ has eased predatory pressures on the apteronotids, but this family
is by far the most successful gymnotiform clade in the Neotropics, and contains
about 40% of all described gymnotiform species (Mago-Leccia, 1994).

EOD DIFFERENTIATION AND ELECTRIC FISH SPECIATION

EODs are species-specific and therefore are thought to play a major role in
species recognition and other types of social interactions (Black-Cleworth, 1970;
Hopkins & Bass, 1981; Hagedorn & Carr, 1985). Even within populations,
males can be distinguished from females and adults from juveniles by means of
their EODs, and certain EOD characteristics such as amplitude and repetition
rate are correlated with a hierarchical relationship among individuals (Black-
Cleworth, 1970; Hagedorn & Zelick, 1989). Females will spawn if electrically
stimulated by conspecific males or by an electronically generated mimic of their
EODs (Alves-Gomes, unpubl. data). Playback experiments have also demon-
strated that female electric fish can be quite selective in responding to electric
stimulation, as only the EOD of a male of the same species will elicit a
behavioural response (Hopkins, 1972, 1974; Moller, 1995). In most species,
differences between male and female EODs are more conspicuous during the
reproductive period, as hormones act directly on the electrocytes’ physiology
(Hagedorn & Carr, 1985; Bass, 1986; Zakon, 1986; Freedman et al., 1989).
The importance of the EOD as a species-specific characteristic, which acts as a
fundamental component in sexual isolation and consequently during speciation,
has been supported by studies combining behaviour and genetics. Recent and
on-going field work in Africa and South America has revealed a number of
examples of clades that, while hardly distinguishable by morphological
standards, possess distinct EOD waveforms (Heiligenberg & Bastian, 1981;
Hopkins, 1986; Alves-Gomes & Hopkins, 1997; Sullivan, 1997). The most well
studied case of this is the mormyriform Brienomyrus Taverne ‘ group ’ (Bass,
1986; Hopkins, 1986; Alves-Gomes & Hopkins, 1997), a clade containing five
morphologically similar species that coexist in African streams. In this clade,
several species apparently were originated from an ancestral and broadly
distributed stock, as different individuals/populations adapted to exploit specific
habitats that became available. Presently, the different clades can be distin-
guished easily by their EOD waveforms, electrocyte innervation patterns, and
mitochondrial DNA sequences, but are indistinguishable by their external
morphology (Alves-Gomes & Hopkins, 1997). Closer analyses of their behav-
iour have also revealed that each clade prefers a more restricted microhabitat in
the streams they inhabit.
The compilation of field information, behavioural studies and genetic data,
means it is possible to speculate about how habitat characteristics, EOD
1506 . . -

waveform, sexual isolation and speciation are closely connected. In a simplified

example, a subset of a population originally living in open water may invade a
densely vegetated area where shelter and/or food are more abundant. In these
fish, selective pressure would act on the EOD waveform to change its properties
to better match the new biophysical properties of the environment. Given
enough time, changes in the EOD waveform could become fixed in the
population, provoking sexual (and probably behavioural) isolation between the
ancestral population living in open water and the offshoot population, with
consequent cladogenesis. The example of Brienomyrus suggests that the EOD
waveform is a plastic character, intimately related to sexual and behaviour
isolation. Such plasticity might cause this specific character to become inappro-
priate in phylogenetic estimations, especially for distantly related clades. As they
are among the first characters to change in electric fish speciation, homoplasic
acquisitions (mainly due to reversals) are likely to occur.

FUTURE WORK
The evolution of electroreceptors and electric organs in teleost fishes is a
fascinating topic in evolutionary biology. Both systems have evolved multiple
times throughout teleost evolution and this opens up a wide horizon in terms of
evolutionary questions that require answers. For instance, what types of
evolutionary forces are behind their repeated appearance? We already know a
great deal about the physiological, morphological, and pharmacological aspects
of the EES in some species of gymnotiforms and mormyriforms, but we still do
not know how many electrogenic/electrosensory species exist. Recent studies are
beginning to show that several species of electric fish that previously were
considered monotypic are complex multi-species clades. The incredible diversity
of catfishes also makes this group a fantastic model-clade. As we move to salt
water and consider uranoscopids, the obvious questions concerns the evolution-
ary advantage of being electrogenic without being able to detect their own
discharge. Another important aspect that needs more attention is the relation-
ship between the species and their habitats. How are particular waveforms better
or less well adapted to certain habitats? On the other hand, how much variation
may exist in the EODs at the inter-populational level, and how may this correlate
to speciation? The answers to these and other questions related to the evolution-
ary aspects of the EES, need a fundamental push from phylogenetic studies. The
following research would contribute significantly to our understanding about the
evolution of electroreceptors and electric organs in teleosts:
(1) We should expand our phylogenetic studies regarding all the clades in-
volved. Some of them like the Cetopsidae, Mochokidae, Malapterurus+
auchenoglanidids, Uranoscopus+Astroscopus+other uranoscopids, and
Notopteriformes+Mormyriformes, are urgent.
(2) Intensify the behavioural studies that will help us to understand how fish
use their EES in their natural habitats especially during social interaction
and food search and capture.
(3) Execute a large survey to study the possible occurrence of electrogenic
catfish outside Africa.
       1507

(4) Promote a large survey to ascertain the presence tuberous of electro-

receptors in cetopsids, but also in other catfish species.
(5) Perform a careful search for bioelectrogenic activity in the close relatives
of electrogenic fish genera and species, such as the notopteriforms,
cetopsids, mochokids, auchenoglanidids, clarids and uranoscopids.
(6) Continue the current research effort to learn about the anatomical,
physiological and pharmacological aspects of the EES.
(7) Examine more carefully the embryological origin electric organs in the
electrogenic lineages.
(8) Investigate in more detail the ecological and evolutionary relationships
between electrogenic prey and electrosensitive predators.
(9) Intensify field work trying to establish a more refined correlation between
the chemical and physical aspects of species’ microhabitats, their electric
organs and EOD waveforms.
(10) Compile the available information from a phylogenetic perspective.

SUMMARY
It has been shown that ampullary electroreception is an old sensory
modality in vertebrate history that had disappeared in the common ancestor
of the teleosts, to be ‘ re-invented ’ independently three times within Teleostei:
once in the common ancestor of Gymnotiformes+Siluriformes (within the
superorder Ostariophysi), and twice within the distantly related superorder
Osteoglossomorph, i.e. in the Mormyriformes and in the closely related Afrian
notopteriforms. Tuberous electroreceptors also appeared three times, but only
in fish that already had ampullary receptors. Furthermore, in two out of three
times, in fish that also had an electric organ (order Gymnotiformes and
Mormyriformes). The presence of tuberous receptors in the non-electrogenic
South American catfish Pseudocetopsis claims for further investigations. Electric
organs evolved eight times in teleosts, and five times among ostariophysans
alone. With the exception of the two uranoscopid genera, for whom no
electroreceptive capability have been discovered so far, all electric organs evolved
on top of a pre-existing electroreceptive condition based upon an ampullary
system. By evaluating the phylogenetic distribution of electric organs, their
physiology and EOD waveforms, it is assumed that plesiomorphic electric organs
were simply innervated and produced monophasic/long lasting pulse discharges
to maximize ampullary detection. Complex, multiphasic EOD waveforms and
wave-type discharges with high carrier frequencies are derived conditions. The
EOD waveform reflects a complex interaction of several morphological and
physiological features of individual electrocytes and their dispositions in the
whole electric organ. Nonetheless, the EOD waveform is a plastic character
under constant selective pressure to evolve the best compromise between an
appropriate spectral frequency to enhance electrolocation and electro-
communication, to ensure species identity through sexual and behavioral
segregation, and to avoid predation.

This paper has benefited tremendously from insightful suggestions by Jeff Podos,
Jansen Zuanon, and Lúcia Rapp Py-Daniel. Many ideas formalized here have evolved
1508 . . -

from fruitful discussions with several people along many years, including Walter
Heiligenberg, Carl Hopkins, Ted Bullock, Chris Braun, Glenn Northcutt, Calvin Wong,
John Spiro, John Lundberg, Phill Stoddard, Jansen Zuanon, Lucia Rapp Py-Daniel and
Cristina Cox Fernandes. Two anonymous reviewers provided critical suggestions to
improve the paper. The author’s research related to this paper has been partially funded
PPI 1-3050 of INPA.

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