scholarly journals Electrocommunication in pulse Gymnotiformes: the role of electric organ discharge (EOD) time course in species identification

2020 ◽  
Vol 223 (16) ◽  
pp. jeb226340
Author(s):  
Joseph C. Waddell ◽  
Angel A. Caputi

ABSTRACTUnderstanding how individuals detect and recognize signals emitted by conspecifics is fundamental to discussions of animal communication. The species pair Gymnotus omarorum and Brachyhypopomus gauderio, found in syntopy in Uruguay, emit species-specific electric organ discharge (EOD) that can be sensed by both species. The aim of this study was to unveil whether either of these species is able to identify a conspecific EOD, and to investigate distinctive recognition signal features. We designed a forced-choice experiment using a natural behavior (i.e. tracking electric field lines towards their source) in which each fish had to choose between a conspecific and a heterospecific electric field. We found a clear pattern of preference for a conspecific waveform even when pulses were played within 1 Hz of the same rate. By manipulating the time course of the explored signals, we found that the signal features for preference between conspecific and heterospecific waveforms were embedded in the time course of the signals. This study provides evidence that pulse Gymnotiformes can recognize a conspecific exclusively through species-specific electrosensory signals. It also suggests that the key signal features for species differentiation are probably encoded by burst coder electroreceptors. Given these results, and because receptors are sharply tuned to amplitude spectra and also tuned to phase spectra, we extend the electric color hypothesis used in the evaluation of objects to apply to communication signals.

1999 ◽  
Vol 202 (10) ◽  
pp. 1229-1241 ◽  
Author(s):  
A.A. Caputi

An understanding of how the nervous system processes an impulse-like input to yield a stereotyped, species-specific electromotor output is relevant for electric fish physiology, but also for understanding the general mechanisms of coordination of effector patterns. In pulse gymnotids, the electromotor system is repetitively activated by impulse-like signals generated by a pacemaker nucleus in the medulla. This nucleus activates a set of relay cells whose axons descend along the spinal cord and project to electromotor neurones which, in turn, project to electrocytes. Relay neurones, electromotor neurones and electrocytes may be considered as layers of a network arranged with a lattice hierarchy. This network is able to coordinate a spatio-temporal pattern of postsynaptic and action currents generated by the electrocyte membranes. Electrocytes may be innervated at their rostral face, at their caudal face or at both faces, depending on the site of the organ and the species. Thus, the species-specific electric organ discharge patterns depend on the electric organ innervation pattern and on the coordinated activation of the electrocyte faces. The activity of equally oriented faces is synchronised by a synergistic combination of delay lines. The activation of oppositely oriented faces is coordinated in a precise sequence resulting from the orderly recruitment of subsets of electromotor neurones according to the ‘size principle’ and to their position along the spinal cord. The body of the animal filters the electric organ output electrically, and the whole fish is transformed into a distributed electric source.


PLoS ONE ◽  
2008 ◽  
Vol 3 (5) ◽  
pp. e2038 ◽  
Author(s):  
Alejo Rodríguez-Cattaneo ◽  
Ana Carolina Pereira ◽  
Pedro A. Aguilera ◽  
William G. R. Crampton ◽  
Angel A. Caputi

2012 ◽  
Vol 2012 ◽  
pp. 1-12 ◽  
Author(s):  
Ruth F. Castillo Cajas ◽  
Oliver M. Selz ◽  
Erwin A. P. Ripmeester ◽  
Ole Seehausen ◽  
Martine E. Maan

Environmental variation in signalling conditions affects animal communication traits, with possible consequences for sexual selection and reproductive isolation. Using spectrophotometry, we studied how male coloration within and between populations of two closely related Lake Victoria cichlid species (Pundamilia pundamilia and P. nyererei) covaries with water transparency. Focusing on coloration patches implicated in sexual selection, we predicted that in clear waters, with broad-spectrum light, (1) colours should become more saturated and (2) shift in hue away from the dominant ambient wavelengths, compared to more turbid waters. We found support for these predictions for the red and yellow coloration of P. nyererei but not the blue coloration of P. pundamilia. This may be explained by the species difference in depth distribution, which generates a steeper gradient in visual conditions for P. nyererei compared to P. pundamilia. Alternatively, the importance of male coloration in intraspecific sexual selection may differ between the species. We also found that anal fin spots, that is, the orange spots on male haplochromine anal fins that presumably mimic eggs, covaried with water transparency in a similar way for both species. This is in contrast to the other body regions studied and suggests that, while indeed functioning as signals, these spots may not play a role in species differentiation.


1999 ◽  
Vol 202 (10) ◽  
pp. 1417-1426 ◽  
Author(s):  
J.D. Crawford ◽  
X. Huang

The African weakly electric fishes Pollimyrus isidori and Pollimyrus adspersus (Mormyridae) produce elaborate acoustic displays during social communication in addition to their electric organ discharges (EODs). In this paper, we provide new data on the EODs of these sound-producing mormyrids and on the mechanisms they use to generate species-typical sounds. Although it is known that the EODs are usually species-specific and sexually dimorphic, the EODs of closely related sound-producing mormyrids have not previously been compared. The data presented demonstrate that there is a clear sexual dimorphism in the EOD waveform of P. isidori. Females have a multi-phasic EOD that is more complex than the male's biphasic EOD. In this respect, P. isidori is similar to its more thoroughly studied congener P. adspersus, which has a sexually dimorphic EOD. The new data also reveal that the EODs of these two species are distinct, thus showing for the first time that species-specificity in EODs is characteristic of these fishes, which also generate species-specific courtship sounds. The sound-generating mechanism is based on a drumming muscle coupled to the swimbladder. Transverse sections through decalcified male and female P. adspersus revealed a muscle that envelops the caudal pole of the swimbladder and that is composed of dorso-ventrally oriented fibers. The muscle is five times larger in males (14.5+/−4.4 microl, mean +/− s.d.) than in females (3.2+/−1.8 microl). The fibers are also of significantly larger diameter in males than in females. Males generate courtship sounds and females do not. The function of the swimbladder muscle was tested using behavioral experiments. Male P. adspersus normally produce acoustic courtship displays when presented with female-like electrical stimuli. However, local anesthesia of the swimbladder muscle muted males. In control trials, males continued to produce sounds after injection of either lidocaine in the trunk muscles or saline in the swimbladder muscles.


Author(s):  
Frédéric Boyer ◽  
Vincent Lebastard

Underwater navigation in turbid water for exploration in catastrophic conditions or navigation in confined unstructured environments is still a challenge for robotics. In these conditions, neither vision nor sonar can be used. Pursuing a bio-inspired approach in robotics, one can seek solutions in nature to solve this difficult problem. Several hundred fish species in families Gymnotidae and Mormyridae have developed an original sense well adapted to this situation: the electric sense. Gnathonemus petersii first polarizes its body with respect to an electric organ discharge located at the base of its tail and generates a dipolar electric field in its near surroundings. Then, using many transcutaneous electro-receptors distributed along its body, the fish “measures” the distortion of the electric field and infers an image of its surroundings. Understanding and implementing this bio-inspired sense offers the opportunity to enhance the navigation abilities of our underwater robots in confined spaces bathed by turbid waters.


2018 ◽  
Vol 92 (3-4) ◽  
pp. 125-141
Author(s):  
Alejandro Vélez ◽  
Da Yeon Ryoo ◽  
Bruce A. Carlson

The ability to localize communication signals plays a fundamental role in social interactions. For signal localization to take place, the sensory system of the receiver must extract information about distance and direction to the sender from physical characteristics of the signal. In many sensory systems, information from multiple peripheral receptors must be integrated by central sensory pathways to determine the sender location. Here, we asked whether evolutionary divergence in the electrosensory and visual systems of mormyrid fish is associated with signal localization behavior. In mormyrids, differences in the distribution of electroreceptors on the surface of the skin are associated with differences in the midbrain exterolateral nucleus (EL). Species with electroreceptors clustered in three rosettes on both sides of the head have a small and undifferentiated EL. In contrast, EL is enlarged and subdivided into anterior (ELa) and posterior (ELp) regions in species that have electroreceptors broadly ­distributed throughout the body. Interestingly, species with EL and clustered electroreceptors also have larger visual systems and higher visual acuity than species with ELa/ELp and broadly distributed electroreceptors. Species with broadly distributed electroreceptors and ELa/ELp approached a simulated conspecific by following the curved electric field lines generated by the electrosensory stimulus. In contrast, a species with small EL and clustered electroreceptors, but an enlarged visual system, followed shorter and straighter paths to the stimulus source. In the central electrosensory system, evoked field potentials in response to stimuli delivered from the left versus the right differed more in EL than in ELa/ELp. Our results suggest that signal localization behavior is associated with differences in sensory specializations. We propose that the distribution of electroreceptors on the body affects the ability of individuals to align parallel to electric field lines and maintain such alignment while approaching the signal source. The spatial resolution of sensory information relayed from the periphery to the midbrain in species with clustered electroreceptors may allow for gross, but not fine, processing of sender location. Furthermore, visual information may play an important role in localizing signaling individuals in species with small EL and clustered electroreceptors. In line with previous studies, we suggest that the physiological and behavioral differences associated with signal localization reflect adaptations to different habitats and social environments.


2014 ◽  
Vol 112 (4) ◽  
pp. 752-765 ◽  
Author(s):  
Henriette Walz ◽  
Jan Grewe ◽  
Jan Benda

Although communication signals often vary continuously on the underlying signal parameter, they are perceived as distinct categories. We here report the opposite case where an electrocommunication signal is encoded in four distinct regimes, although the behavior described to date does not show distinct categories. In particular, we studied the encoding of chirps by P-unit afferents in the weakly electric fish Apteronotus leptorhynchus. These fish generate an electric organ discharge that oscillates at a certain individual-specific frequency. The interaction of two fish in communication contexts leads to the emergence of a beating amplitude modulation (AM) at the frequency difference between the two individual signals. This frequency difference represents the social context of the encounter. Chirps are transient increases of the fish's frequency leading to transient changes in the frequency of the AM. We stimulated the cells with the same chirp on different, naturally occurring backgrounds beats. The P-units responded either by synchronization or desynchronization depending on the background. Although the duration of a chirp is often shorter than a full cycle of the AM it elicits, the distinct responses of the P-units to the chirp can be predicted solely from the frequency of the AM based on the static frequency tuning of the cells.


2008 ◽  
Vol 5 (2) ◽  
pp. 225-228 ◽  
Author(s):  
Philine G.D Feulner ◽  
Martin Plath ◽  
Jacob Engelmann ◽  
Frank Kirschbaum ◽  
Ralph Tiedemann

Mate choice is mediated by a range of sensory cues, and assortative mating based on these cues can drive reproductive isolation among diverging populations. A specific feature of mormyrid fish, the electric organ discharge (EOD), is used for electrolocation and intraspecific communication. We hypothesized that the EOD also facilitates assortative mating and ultimately promotes prezygotic reproductive isolation in African weakly electric fishes. Our behavioural experiments using live males as well as EOD playback demonstrated that female mate recognition is influenced by EOD signals and that females are attracted to EOD characteristics of conspecific males. The dual function of the EOD for both foraging and social communication (including mate recognition leading to assortative mating) underlines the importance of electric signal differentiation for the divergence of African weakly electric fishes. Thus, the EOD provides an intriguing mechanism promoting trophic divergence and reproductive isolation between two closely related Campylomormyrus species occurring in sympatry in the lower Congo rapids.


Author(s):  
Mehrnoush Nourbakhsh-Rey ◽  
Michael Markham

Animal communication signals are regulated by multiple hormonal axes that ensure appropriate signal targeting, timing, and information content. The regulatory roles of steroid hormones and many peptide hormones are well understood and documented across a wide range of vertebrate taxa. Two recent studies have reported a novel function for leptin, a peptide hormone central to energy balance regulation: regulating communication signals of weakly electric fish and singing mice. With only limited evidence available at this time, a key question is just how widespread leptinergic regulation of communication signals is within and across taxa. A second important question is what features of communication signals are subject to leptinergic regulation. Here we consider the functional significance of leptinergic regulation of animal communication signals in the context of both direct and indirect signal metabolic costs. Direct costs arise from metabolic investment in signal production, while indirect costs arise from the predation and social conflict consequences of the signal’s information content. We propose a preliminary conceptual framework for predicting which species will exhibit leptinergic regulation of their communication signals and which signal features leptin will regulate. This framework suggests a number of directly testable predictions within and across taxa. Accounting for additional factors such as life history and reproductive strategies will likely require modification or elaboration of this model.


Author(s):  
Joseph C. Waddell ◽  
Angel A. Caputi

Some fish communicate using pulsatile, stereotyped electric organ discharges (EODs) that exhibit species- and sex-specific time courses. To ensure reproductive success, they must be able to discriminate conspecifics from sympatric species in the muddy waters they inhabit. We have previously shown that they use the electric field lines as a tracking guide to approach conspecifics (electrotaxis) in both Gymnotus and Brachyhypopomus genera. Here we show that the social species Brachyhypopomus gauderio uses electrotaxis to arrive abreast a conspecific, coming from behind. Stimulus image analysis shows that, even in a uniform field, every single EOD causes an image in which the gradient and the local field time courses contain enough information to allow the fish to evaluate conspecific sex, and to find the path to reach it. Using a forced-choice test we show that sexually mature individuals orient themselves along a uniform field in the direction encoded by the time course characteristic of the opposite sex. This indicates that these fish use the stimulus image profile as a spatial guidance clue to find a mate. Embedding species, sex, and orientation cues is a particular example of how species can encode multiple messages in the same self-generated communication signal carrier, allowing for other signal parameters (e.g., EOD timing) to carry additional, often circumstantial, messages. This ‘multiple messages’ EOD embedding approach expressed in this species is likely to be a common and successful strategy widespread across evolutionary lineages and among varied signaling modalities.


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