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III. Brachyhypopomus

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III. Brachyhypopomus J Comp Physiol A (1999) 184: 609±630 Ó Springer-Verlag 1999 ORIGINAL PAPER P. K. Stoddard á B. Rasnow á C. Assad Electric organ discharges of the gymnotiform ®shes: III. Brachyhypopomus Accepted: 22 September 1998 Abstract We measured and mapped the electric ®elds Key words Bioelectricity á Communication á Electric produced by three species of neotropical electric ®sh of ®sh á Electrogenesis á Electroreception the genus Brachyhypopomus (Gymnotiformes, Rham phichthyoidea, Hypopomidae), formerly Hypopomus. Abbreviations EOD electric organ discharge á IPI These species produce biphasic pulsed discharges from interpulse interval á LEA length to end of anal ®n á myogenic electric organs. Spatio-temporal false-color P1 phase 1 of EOD á P2 phase 2 of EOD á rms root maps of the electric organ discharges measured on the mean square skin show that the electric ®eld is not a simple dipole in Brachyhypopomus. Instead, the dipole center moves rostro-caudally during the 1st phase (P1) of the electric Introduction organ discharge, and is stationary during the 2nd phase (P2). Except at the head and tip of tail, electric ®eld lines Over the past four decades, scientists have discovered an rotate in the lateral and dorso-ventral planes. Rostro- unexpected diversity and abundance of electrogenic caudal dierences in ®eld amplitude, ®eld lines, and ®shes in the fresh waters of the New World tropics and spatial stability suggest that dierent parts of the electric West Africa. Of particular interest to comparative neu- organ have undergone selection for dierent functions; robiologists is the diversity of electric organ discharge the rostral portions seem specialized for electrosensory (EOD) waveforms produced by these ®sh for active processing, whereas the caudal portions show adapta- electrolocation and communication. Because electrolo- tions for d.c. signal balancing and mate attraction as cation appears to have been the driving force behind well. Computer animations of the electric ®eld images the evolution of electric signals in the gymnotiforms, we described in this paper are available on web sites http:// assume that the demands of electrolocation in dierent www.bbb.caltech.edu/ElectricFish or http://www.®u.edu/ ecological niches are probably responsible for much of ~stoddard/electric®sh.html. the EOD variation seen in modern gymnotiform taxa. We do not rule out, a priori, the possibility that gross EOD variation has resulted from genetic drift as much P.K. Stoddard (&) as from functional adaptation. We would argue that Department of Biological Sciences, regardless of its evolutionary origins, the structure of Florida International University, the EOD constitutes each individual's immediate sen- Miami, FL 33199, USA sory world, and must be re¯ected in its strategies for e-mail: stoddard@®u.edu Fax: +1-305-348-1869 electrolocation, communication, and electrosensory processing. B. Rasnow á C. Assad Divisions of Biology and Electrical Engineering, Active electrolocation and courtship behavior in California Institute of Technology, gymnotiform ®shes occur within some fraction of a body Pasadena, CA 91125, USA length from the ®sh (Bastian 1976b; Hagedorn and Heiligenberg 1985; Stoddard et al. 1996). In most spe- B. Rasnow Amgen, One Amgen Center Drive, cies, the near electric ®elds have been found to be far Thousand Oaks, CA 91320, USA more heterogeneous than would be expected from the simple dipolar EOD waveforms measured beyond a C. Assad body length (Bennett 1961; Bastian 1976a; Caputi et al. Jet Propulsion Laboratory, MS 303-300, 4800 Oak Grove Drive, 1989; Rasnow et al. 1993; Rasnow and Bower 1996). To Pasadena, CA 91109, USA understand electrolocation and close-range communi- 610 Fig. 1 Remote electric organ discharges (EODs) of the three portion, in which the polarities reverse, is referred to Brachyhypopomus species presented in this study. The photo scale is as the ``2nd phase'' or P2. In most species of Bra- in centimeters. EODs, shown to the same amplitude scale, were digitized during the daytime from unsedated ®sh centered lengthwise chyhypopomus, the 2nd phase of the male's EOD is in an aquarium 120 ´ 44 ´ 44 cm. Dierential recording electrodes longer than the female's. Male Brachyhypopomus mod- were located on opposite walls 120 cm apart. The photographs are of ulate the magnitude and duration of their EODs be- dierent individuals than those that we mapped, although they are tween day and night and in response to changing social similar in size and remote EOD waveform. The B. sp. ``walteri'' female conditions (Hagedorn and Zelick 1989; Hagedorn 1995; shown here is noticeably gravid, whereas those we mapped became gravid only subsequent to mapping Franchina et al. 1998; Franchina and Stoddard 1999). Changes in the EOD appear to stem from changes in local action potentials under the regulation of hormones cation, we must distinguish between local and remote (Hagedorn and Carr 1985). Thus, Brachyhypopomus electric currents and ®eld vectors, much as scientists shows signi®cant promise as a model for exploration of have distinguished between near-®eld and far-®eld behavioral and hormonal control of action potential acoustic eects in the exploration of auditory processes. waveforms. Based on the assumption that Bra- Understanding variation in local currents is a key step chyhypopomus is capable of discriminating species and towards understanding the mechanisms involved in sex dierences in its pulsed EOD waveform, the genus electric imaging of nearby objects as well as the sec- Brachyhypopomus has also received attention as a model ondary electrosensory strategies of communication and system for discrimination of transient waveforms (He- concealment from predators. iligenberg and Altes 1978, Hopkins and Westby 1986, This paper is the third in our series on the ®ne spatio- Shumway and Zelick 1988). temporal structure of EODs of the gymnotiform ®shes. The genus Brachyhypopomus includes all species for- Our previous studies examined electric ®eld structure merly in genus Hypopomus except a couple of species generated by the gymnotiform ®shes in the families from the coastal streams of the Guianas typi®ed by Apteronotidae (Rasnow et al. 1993; Rasnow and Bower H. artedi (Mago-Leccia 1994). Members of the genus 1996) and Eigenmanniidae (Assad et al. 1998). This Brachyhypopomus inhabit slow-moving or still waters of paper is the ®rst to map systematically the electric ®elds the neotropics from Costa Rica to Argentina (Sullivan generated by ®sh of a gymnotiform family with a pulse- 1997). Electric discharge rates during normal nocturnal type EOD. Members of the family Hypopomidae activity range from 8 to 70 EODs s)1 for dierent produce EODs with a wide range of macrovariation, members of the genus, dropping to less than half that ranging from one to ®ve distinct peaks or phases. Most during the day when they are inactive. EOD duration Hypopomid species produce a biphasic EOD (Fig. 1). ranges from about 0.5 ms to 5 ms across species, cor- Brachyhypopomus, the largest genus in this family, has relating roughly with the interpulse interval (IPI) received much attention for the sexual variation in its (Hopkins and Heiligenberg 1978). Congeners with usually biphasic waveform (Hagedorn 1986, 1988, 1995; widely varying EOD characteristics frequently inhabit Hagedorn and Zelick 1989; Shumway and Zelick 1988; the same bodies of water (Hopkins and Heiligenberg Westby 1988; Kawasaki and Heiligenberg 1989; Com- 1978; Hagedorn and Keller 1996; Crampton 1998). fort 1990; Hopkins et al. 1990; Hopkins 1991; Franchina The electric organ of Brachyhypopomus is a bilateral and Stoddard 1999). The electric potential of the bi- structure of myogenic origin. The electrocytes consti- phasic EOD of Brachyhypopomus ®rst becomes positive tuting the electric organ are box-shaped cells, innervated at the head and negative at the tail. This portion of the only on their posterior surface by cholinergic spinal EOD is referred to as the ``1st phase'' or P1. The second motor aerents (Fig. 2; Bennett 1961, 1971). Electro- 611 the non-innervated anterior face as well. Bastian (1976a) inferred that spectral dierences in the local EOD re- sulted from temporal asynchrony of several spatially heterogeneous local currents. These ®ndings of local EOD heterogeneity have sig- ni®cant implications for electroreception in the contexts of active electrolocation, communication, and passive detection of conspeci®cs. Variation in local EOD cur- rents will aect the electric images of local objects. For communication and passive detection of other electric ®shes, the perceived EOD of a remote ®sh will be very Fig. 2 Schematic of B. pinnicaudatus showing the location and extent dierent in structure from that of a ®sh close by. of the electric organ. A single electrocyte from the posterior region of Further use of the genus Brachyhypopomus as a the electric organ is shown below, innervated by spinal electromoto- model system for waveform control and transient anal- neurons on its posterior face. Electromotoneurons trigger an action ysis depends on a better understanding of its electric ®eld potential in the posterior face of the electrocyte, producing a headward sodium current indicated here by arrows with ®lled heads. structure. We present in this paper detailed representa- These action potentials sum across all the electrocytes in the electric tions of the electric ®elds of individuals of three species organ to produce the head-positive phase of the EOD (P1). of Brachyhypopomus. Using a robotic
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