Plasticity of the electric organ discharge waveform of male Brachyhypopomus pinnicaudatus. II. Social effects.

Many electric fish produce sexually dimorphic electric organ discharges. Although electric organ discharges are comprised of action potentials, those of the Gymnotiform family Hypopomidae show significant plasticity in response to stress and time of day. We show here that male Brachyhypopomus pinnicaudatus (Hopkins 1991), adjusts the degree of sexual dimorphism in its electric organ discharge depending on immediate social conditions. Three to five days of isolation resulted in gradual decrease of two sexually dimorphic waveform characters: duration and amplitude. Introduction of a second fish to the experimental tank restored electric organ discharge duration and amplitude. Duration recovered quicker than amplitude, and both recovered faster in the presence of males than females. In studies of other electric fish species, treatment with steroid sex hormones have taken several days to increase sexual dimorphism in the electric organ discharge. The socially induced changes seen in this study are initiated too quickly to involve classic steroid action of genomic transcription and thus may depend on another mechanism. Socially induced regulation of the male's electric organ discharge waveform is consistent with the compromises in signaling strategy shown by other taxa with costly sexual advertisement signals.

Predation enhances complexity in the evolution of electric fish signals.

Theories of sexual selection assume that predation is a restrictive, simplifying force in the evolution of animal display characters and many empirical studies have shown that predation opposes excessive elaboration of sexually selected traits. In an unexpected turnaround, I show here that predation pressure on neotropical, weakly electric fish (order Gymnotiformes) seems to have selected for greater signal complexity, by favouring characters that have enabled further signal elaboration by sexual selection. Most gymnotiform fish demonstrate adaptations that lower detectability of their electrolocation/communication signals by key predators. A second wave phase added to the ancestral monophasic signal shifts the emitted spectrum above the most sensitive frequencies of electroreceptive predators. By using playback trials with the predatory electric eel (Electrophorus electricus), I show that these biphasic signals are less detectable than the primitive monophasic signals. But sexually mature males of many species in the family Hypopomidae extend the duration of the second phase of their electric signal pulses and further amplify this sexual dimorphism nightly during the peak hours of reproduction. Thus a signal element that evolved for crypsis has itself been modified by sexual selection.

Electric organ discharges of the gymnotiform fishes: III. Brachyhypopomus.

We measured and mapped the electric fields produced by three species of neotropical electric fish of the genus Brachyhypopomus (Gymnotiformes, Rham phichthyoidea, Hypopomidae), formerly Hypopomus. These species produce biphasic pulsed discharges from myogenic electric organs. Spatio-temporal false-color maps of the electric organ discharges measured on the skin show that the electric field is not a simple dipole in Brachyhypopomus. Instead, the dipole center moves rostro-caudally during the 1st phase (P1) of the electric organ discharge, and is stationary during the 2nd phase (P2). Except at the head and tip of tail, electric field lines rotate in the lateral and dorso-ventral planes. Rostrocaudal differences in field amplitude, field lines, and spatial stability suggest that different parts of the electric organ have undergone selection for different functions; the rostral portions seem specialized for electrosensory processing, whereas the caudal portions show adaptations for d.c. signal balancing and mate attraction as well. Computer animations of the electric field images described in this paper are available on web sites http:/(/) www.bbb.caltech.edu/ElectricFish or http:/(/)www.fiu.edu/-stoddard/electric fish.html.

Electric organ discharges and electric images during electrolocation.

Weakly electric fish use active electrolocation - the generation and detection of electric currents - to explore their surroundings. Although electrosensory systems include some of the most extensively understood circuits in the vertebrate central nervous system, relatively little is known quantitatively about how fish electrolocate objects. We believe a prerequisite to understanding electrolocation and its underlying neural substrates is to quantify and visualize the peripheral electrosensory information measured by the electroreceptors. We have therefore focused on reconstructing both the electric organ discharges (EODs) and the electric images resulting from nearby objects and the fish's exploratory behaviors. Here, we review results from a combination of techniques, including field measurements, numerical and semi-analytical simulations, and video imaging of behaviors. EOD maps are presented and interpreted for six gymnotiform species. They reveal diverse electric field patterns that have significant implications for both the electrosensory and electromotor systems. Our simulations generated predictions of the electric images from nearby objects as well as sequences of electric images during exploratory behaviors. These methods are leading to the identification of image features and computational algorithms that could reliably encode electrosensory information and may help guide electrophysiological experiments exploring the neural basis of electrolocation.

Plasticity of the electric organ discharge waveform of the electric fish Brachyhypopomus pinnicaudatus. I. Quantification of day-night changes.

The electric organ discharge of the gymnotiform fish Brachyhypopomus pinnicaudatus is a biphasic waveform. The female's electric organ discharge is nearly symmetric but males produce a longer second phase than first phase. In this study, infrared-sensitive video cameras monitored the position of unrestrained fish, facilitating precise measurement of electric organ discharge duration and amplitude every 2 h for 24 h. Males (n = 27) increased electric organ discharge duration by 37 +/- 12% and amplitude by 24 +/- 9% at night and decreased it during the day. In contrast, females (n = 8) exhibited only minor electric organ discharge variation over time. Most of a male's increase occurred rapidly within the first 2-3 h of darkness. Electric organ discharge values gradually diminished during the second half of the dark period and into the next morning. Modulation of the second phase of the biphasic electric organ discharge produced most of the duration change in males, but both phases changed amplitude by similar amounts. Turning the lights off at mid-day triggered an immediate increase in electric organ discharge, suggesting modification of existing ion channels in the electric organ, rather than altered genomic expression. Exaggeration of electric organ discharge sex differences implies a social function. Daily reduction of duration and amplitude may reduce predation risk or energy expenditure.

The electric organ discharges of the gymnotiform fishes: II. Eigenmannia.

We present detailed measurements of the electric organ discharge of the weakly electric fish, Eigenmannia sp. These maps illuminate, with high resolution in both space and time, the electric organ discharge potential and electric field patterns in the water about the fish and on the skin surface itself. The results demonstrate that the electric organ discharge of Eigenmannia approximates a simple oscillating dipole, which confirms previous descriptions and assumptions, but is in contrast to the electric organ discharges of several other gymnotiform species. Over each cycle of Eigenmannia's electric organ discharge, the electric field amplitude measured at any point near the fish oscillates from positive to negative, but the field vector remains nearly constant in direction. This electric organ discharge pattern is correlated with known anatomical and physiological features of the fish's electric organ, and confirms that the activation of electrocytes comprising the organ is well synchronized. As a result, the relatively simple electric organ discharge leads to a fairly uniform pattern of electrosensory stimuli along the body surface, which may facilitate central processing of electrosensory images. Electric organ discharge maps and animations resulting from this series of studies are available via the Internet (http:@www.bbb.caltech.edu/ElectricFish, or www.fiu.edu/ approximately stoddard/electricfish.html).

Detection of multiple stimulus features forces a trade-off in the pyramidal cell network of a gymnotiform electric fish's electrosensory lateral line lobe.

Modification of an existing neural structure to support a second function will produce a trade-off between the two functions if they are in some way incompatible. The trade-off between two such sensory functions is modeled here in pyramidal neurons of the gymnotiform electric fish's medullar electrosensory lateral line lobe (ELL). These neurons detect two electric stimulus features produced when a nearby object interferes with the fish's autogenous electric field: (1) amplitude modulation across a cell's entire receptive field and (2) amplitude variation within a cell's receptive field produced by an object's edge. A model of sensory integration shows that detection of amplitude modulation and enhancement of spatial contrast involve an inherent mechanistic trade-off and that the severity of the trade-off depends on the particular algorithm of sensory integration. Electrophysiology data indicate that of the two algorithms for sensory integration modeled here for the gymnotiform fish Brachyhypopomus pinnicaudatus, the algorithm with the better trade-off function is used. Further, the intrinsic trade-off within single cells has been surmounted by the replication of ELL into multiple electrosensory map segments, each specialized to emphasize different sensory features.

Correlation of song learning and territory establishment strategies in the song sparrow.

In a field study, we show that a young song sparrow (i) selects his songs from three or four older birds who have neighboring territories, (ii) preferentially learns song types that these tutor neighbors share, and (iii) ultimately sets up his territory next to, or replaces, one of these tutor neighbors. The consequence of this song learning strategy is that the young bird's song repertoire represents the "logical intersection" of the song repertoires of his tutor neighbors. We argue that this repertoire is optimally designed for mimicry (sounding like your neighbors) and for communication between neighbors (song sparrows address or reply to a neighbor with a song they share with that neighbor).

Perception of cliff swallow calls by birds (Hirundo pyrrhonota and Sturnus vulgaris) and humans (Homo sapiens).

We tested for species differences in the perception of the cliff swallow chick begging call. One cliff swallow (Hirundo pyrrhonota), 3 European starling (Sturnus vulgaris), and 3 human (Homo sapiens) subjects were trained on go-no-go or repeating background tasks to discriminate between all possible stimulus pairs, measured by percentage of correct response and latency. We used multidimensional scaling to convert the similarity measures into a 2-dimensional map for each subject. Most of the maps were significantly correlated in Dimension 1 but not in Dimension 2. A cluster analysis separated bird and human maps. To identify the most important acoustic cues for each subject, we regressed the coordinates of each dimension on acoustic variables measured from the stimuli. For all subjects, center frequency was Dimension 1. Different acoustic cues were associated with Dimension 2, with agreement only on bandwidth, by the cliff swallow and 1 starling.

Acoustic adaptations for parent-offspring recognition in swallows.

We have used field and laboratory studies to investigate acoustic adaptations for parent-offspring recognition in two closely related pairs of swallows: (a) bank swallow (Riparia riparia) and northern rough-winged swallow (Stelgidopteryx serripennis), and (b) cliff swallow (Hirundo pyrrhonota) and barn swallow (Hirundo rustica). Cross-fostering and playback experiments show that bank swallow and cliff swallow parents recognize their offspring by voice while rough-winged swallow and barn swallow parents do not. We argue that this species difference is due to an evolutionary history of strong selection for recognition in bank swallows and cliff swallows, which live in large, dense colonies, and of weak or no selection for recognition in rough-winged swallows and barn swallows, which live solitarily or in small groups. We consider two possible acoustic adaptations which may underlie the observed species difference. First, the "signature" calls of cliff swallow and bank swallow chicks appear to be more individually distinctive than the homologous calls of rough-winged swallows and barn swallows. This conclusion is supported by a sonographic analysis of among- and within-individual call variation: The information content of bank swallow and cliff swallow calls is considerably greater than that of rough-winged swallow or barn swallow calls. We also discuss our more recent work on the hypothesis that the colonial swallow species are better able to discriminate these sorts of auditory stimuli. We conclude with the caution that auditory specializations may be unnecessary given the signature call adaptation and the general capabilities of the avian ear.