A simple model of the electrosensory electromotor loop in Gymnotus omarorum.

This article introduces and tests a simple model that describes a neural network found in nature, the electrosensory control of an electromotor pacemaker. The cornerstone of the model is an early-stage filter based on the subtraction of a feedforward integrated version of the recent sensory past from the present input signal. The output of this filter governs the modulation of a premotor pacemaker command driving the sensory signal carrier generation and, in consequence, the timing of subsequent electrosensory input. This early filter has a biological parallel in the known connectivity of the first electrosensory relay within the brain stem of the weakly electric fish Gymnotus omarorum. Our biomimetic model of this active, perception-driven action-sensation cycle was contrasted with previously published and here provided new data. When the amplitude of the electrosensory input was manipulated to mimic previous experiments on the novelty detection characteristics, the model reproduces them rather faithfully. In addition, when we applied continuous variations to the input it shows that increases in stimulus amplitudes are followed by increases in the EOD rate, but decreases do not cause rate modulation suggesting a rectification in some stage of the loop. These behavioral experiments confirmed results generated the simulations suggesting that beyond explaining the novelty detection process this simple model is a good description of the electrosensory -electromotor loop in pulse weakly electric fish.

Getting the news in milliseconds: The role of early novelty detection in active electrosensory exploration.

The pulse emitting weakly electric fish Gymnotus omarorum shows stereotyped "novelty responses" consisting of a transient acceleration of the rhythm of a self-emitted electric organ discharge that carries electrosensory signals. Here we show that rapid increases in electric image amplitude cause a "novelty detection potential" in the first electrosensory relay. This sign precedes and its amplitude predicts, the amplitude of the subsequent behavioral novelty response. Current source density analyses indicates its origin ar the layers of the electrosensory lobe where the main output neurons occur. Two types of units, referred to as "ON" and "OFF". Were recorded there in decerebrated fish. Firing probability of "OFF" units drastically decreased after a stepwise increase in electric image. By contrast, the very first novel stimuli after the increase evoked a sharp peak in firing rate of "ON" units followed by a very fast adaptation phase that contrasted with the slow adaptation observed in previous recordings of primary afferents. The amplitudes of this peak, the novelty detection potential, and the behavioral novelty responses, show the same dependence on the departure of the newest stimulus intensity from the weighted average of preceding ones suggesting that the signals encoded by "ON" neurons underlay the novelty detection potential, propagates through the hierarchical organization of the electromotor control, and finally contribute to accelerate the electric organ discharge rate. This suggests that detecting novelty at the very early processing stage of electrosensory signals is essential to adapt the electrosensory sampling rate to exploration requirements as they change dynamically.

The captivating effect of electric organ discharges: species, sex and orientation are embedded in every single received image.

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 fish in both Gymnotus and Brachyhypopomus genera use the electric field lines as a tracking guide to approach conspecifics (electrotaxis). 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 the 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 that is widespread across evolutionary lineages and among varied signaling modalities.

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

Understanding 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.

Waveform discrimination in a pair of pulse-generating electric fishes.

Studies of pulse-type gymnotiform electric fishes have suggested that electric organ discharge waveforms (EODw) allow individuals to discriminate between conspecific and allospecific signals, but few have approached this experimentally. Here we implement a phase-locked playback technique for a syntopic species pair, Brachyhypopomus gauderio and Gymnotus omarorum. Both species respond to changes in stimulus waveform with a transitory reduction in the interpulse interval of their self-generated discharge, providing strong evidence of discrimination. We also document sustained rate changes in response to different EODws, which may suggest recognition of natural waveforms.

Reproductive life-history strategies in a species-rich assemblage of Amazonian electric fishes.

The reproductive biology of only a small fraction of Neotropical freshwater fishes has been described, and detailed comparative studies of reproductive life-history variation in the Neotropical ichthyofauna are lacking. Here we describe interspecific variation in reproductive life history for a multi-species assemblage of the electric knifefish genus Brachyhypopomus (Hypopomidae: Gymnotiformes: Ostariophysi) from Amazonian floodplain and terra firme stream systems. During a year-round quantitative sampling program, we collected and measured key life-history traits from 3,410 individuals. Based on oocyte size distributions, and on circannual variation in gonadosomatic indices, hepatosomatic indices, and capture-per-unit-effort abundance of reproductive adults, we concluded that all species exhibit a single protracted annual breeding season during which females spawn fractionally. We found small clusters of post-larval individuals in one floodplain species and one terra firme stream species, but no signs of parental care. From analyses of body size-frequency distributions and otolith growth increments, we concluded that five species in our study area have approximately one-year (annual) semelparous life history with a single reproductive period followed by death, while two species have a two-year iteroparous life history, with breeding in both year-groups. Despite predictions from life-history theory we found no salient correlations between life history strategy (semelparity or iteroparity) and habitat occupancy (floodplain or terra firme stream). In the iteroparous species B. beebei, we documented evidence for reproductive restraint in the first breeding season relative to the second breeding season and argue that this is consistent with age-regulated terminal investment.

Unexpected species diversity in electric eels with a description of the strongest living bioelectricity generator.

Is there only one electric eel species? For two and a half centuries since its description by Linnaeus, Electrophorus electricus has captivated humankind by its capacity to generate strong electric discharges. Despite the importance of Electrophorus in multiple fields of science, the possibility of additional species-level diversity in the genus, which could also reveal a hidden variety of substances and bioelectrogenic functions, has hitherto not been explored. Here, based on overwhelming patterns of genetic, morphological, and ecological data, we reject the hypothesis of a single species broadly distributed throughout Greater Amazonia. Our analyses readily identify three major lineages that diverged during the Miocene and Pliocene-two of which warrant recognition as new species. For one of the new species, we recorded a discharge of 860 V, well above 650 V previously cited for Electrophorus, making it the strongest living bioelectricity generator.

A new and improved electric fish finder with resources for printed circuit board fabrication

We describe the circuit design, construction, and operation of a field-portable electric fish finder (an AC-coupled wide-band differential bio-amplifier with loudspeaker output). This device permits detection and monitoring of the electric organ discharges generated by neotropical gymnotiform fishes (as well as the mormyroid fishes of tropical Africa). Our design is modified from earlier versions to optimize detection performance and stability over a wider range of ambient water conductivity, including under conditions of extremely low conductivity (< ca. 10 μScm-1). Our new electric fish finder design also incorporates complete waterproofing and longer battery autonomy. We provide Gerber and Eagle files made with the electronic design automation software 'Autodesk Eagle' to allow researchers to order printed circuit boards directly from commercial manufacturers.(AU)

Nós descrevemos o projeto de circuitos eletrônicos e as instrucões para a construção e uso de um detector de peixes elétricos portátil (bio-amplificador diferencial de banda-larga com acoplamento AC). Este aparelho permite a detecção e o monitoramento das descargas de órgãos elétricos gerados por peixes neotropicais da ordem Gymnotiformes (assim como dos peixes mormirídeos da África Tropical). Nosso projeto é modificado a partir de versões anteriores para otimizar o desempenho e a estabilidade sob uma faixa de condutividades ambientais mais ampla, incluindo condições de condutividade extremamente baixa (< ca. 10 μScm-1). Nosso detector de peixes elétricos novo também foi otimizado a fim de proporcionar impermeabilização completa e vida longa para as baterias. Nós fornecemos arquivos 'Gerber' e 'Eagle' preparados com o software de automação de projeto eletrônico 'Autodesk Eagle' para permitir aos pesquisadores a possibilidade de efetuar encomendas de nossa placa de circuito impresso direitamente das empresas de fabricação.(AU)

Karyotypic Diversity and Evolution in a Sympatric Assemblage of Neotropical Electric Knifefish.

Chromosome changes can perform an important role in speciation by acting as post-zygotic reproductive barriers. The Neotropical electric fish genus Brachyhypopomus (Gymnotiformes, Hypopomidae) has 28 described species, but cytogenetic data are hitherto available only for four of them. To understand karyotype evolution and investigate the possible role of chromosome changes in the diversification of this genus, we describe here the karyotype of eight species of Brachyhypopomus from a sympatric assemblage in the central Amazon basin. We analyzed cytogenetic data in the context of a phylogenetic reconstruction of the genus and known patterns of geographical distribution. We found a strong phylogenetic signal for chromosome number and noted that sympatric species have exclusive karyotypes. Additional insights into the role of chromosome changes in the diversification of Brachyhypopomus are discussed.

Electric organ discharges and near-field spatiotemporal patterns of the electromotive force in a sympatric assemblage of Neotropical electric knifefish.

Descriptions of the head-to-tail electric organ discharge (ht-EOD) waveform - typically recorded with electrodes at a distance of approximately 1-2 body lengths from the center of the subject - have traditionally been used to characterize species diversity in gymnotiform electric fish. However, even taxa with relatively simple ht-EODs show spatiotemporally complex fields near the body surface that are determined by site-specific electrogenic properties of the electric organ and electric filtering properties of adjacent tissues and skin. In Brachyhypopomus, a pulse-discharging genus in the family Hypopomidae, the regional characteristics of the electric organ and the role that the complex 'near field' plays in communication and/or electrolocation are not well known. Here we describe, compare, and discuss the functional significance of diversity in the ht-EOD waveforms and near-field spatiotemporal patterns of the electromotive force (emf-EODs) among a species-rich sympatric community of Brachyhypopomus from the upper Amazon.

Phylogenetic Systematics, Biogeography, and Ecology of the Electric Fish Genus Brachyhypopomus (Ostariophysi: Gymnotiformes).

A species-level phylogenetic reconstruction of the Neotropical bluntnose knifefish genus Brachyhypopomus (Gymnotiformes, Hypopomidae) is presented, based on 60 morphological characters, approximately 1100 base pairs of the mitochondrial cytb gene, and approximately 1000 base pairs of the nuclear rag2 gene. The phylogeny includes 28 species of Brachyhypopomus and nine outgroup species from nine other gymnotiform genera, including seven in the superfamily Rhamphichthyoidea (Hypopomidae and Rhamphichthyidae). Parsimony and Bayesian total evidence phylogenetic analyses confirm the monophyly of the genus, and identify nine robust species groups. Homoplastic osteological characters associated with diminutive body size and occurrence in small stream habitats, including loss of squamation and simplifications of the skeleton, appear to mislead a phylogenetic analysis based on morphological characters alone-resulting in the incorrect placing of Microsternarchus + Racenisia in a position deeply nested within Brachyhypopomus. Consideration of geographical distribution in light of the total evidence phylogeny indicates an origin for Brachyhypopomus in Greater Amazonia (the superbasin comprising the Amazon, Orinoco and major Guiana drainages), with subsequent dispersal and vicariance in peripheral basins, including the La Plata, the São Francisco, and trans-Andean basins of northwest South America and Central America. The ancestral habitat of Brachyhypopomus likely resembled the normoxic, low-conductivity terra firme stream system occupied by many extant species, and the genus has subsequently occupied a wide range of terra firme and floodplain habitats including low- and high-conductivity systems, and normoxic and hypoxic systems. Adaptations for impedance matching to high conductivity, and/or for air breathing in hypoxic systems have attended these habitat transitions. Several species of Brachyhypopomus are eurytopic with respect to habitat occupancy and these generally exhibit wider geographical ranges than stenotopic species.

Mitochondrial genomes of the South American electric knifefishes (Order Gymnotiformes).

Three complete mitochondrial genomes of South American electric fishes (Gymnotiformes), derived from high-throughput RNA sequencing (RNA-Seq), are reported herein. We report the complete mitochondrial genome of the bluntnose knifefish Brachyhypopomus n.sp. VERD, determined from newly sequenced data. We also provide the complete mitochondrial genomes for Sternopygus arenatus and the electric eel Electrophorus electricus, assembled from previously published transcriptome data. The mitochondrial genomes of Brachyhypopomus n.sp. VERD, Sternopygus arenatus and Electrophorus electricus have 13 protein-coding genes, 1 D-loop, 2 ribosomal RNAs and 22 transfer RNAs, and are 16,547, 16,667 and 16,906 bp in length, respectively. Phylogenetic analysis of the eight available mitochondrial genomes of gymnotiform fishes shows Apteronotus to be the sister lineage of other gymnotiformes, contradicting the "Sinusoidea" hypothesis that Apteronotidae and Sternopygidae are sister taxa.

A taxonomic revision of the Neotropical electric fish genus Brachyhypopomus (Ostariophysi: Gymnotiformes: Hypopomidae), with descriptions of 15 new species

The bluntnose knifefish genus BrachyhypopomusMago-Leccia, 1994, is diagnosed from other Rhamphichthyoidea (Rhamphichthyidae + Hypopomidae) by the presence of a disk-like ossification in the anterior portion of the palatoquadrate, and by the following external characters: short snout, 18.7-32.6% of head length (vs. 33.3-68.6% in Hypopomus, Gymnorhamphichthys, Iracema, and Rhamphichthys), absence of a paired accessory electric organ in the mental or humeral region (vs. presence in Hypopygus and Steatogenys), presence of 3-4 pectoral proximal radials (vs. 5 in Akawaio), presence of the antorbital + infraorbital, and the preopercular cephalic lateral line canal bones (vs. absence in Racenisia). Brachyhypopomus cannot be diagnosed unambiguously from Microsternarchus or from Procerusternarchus on the basis of external characters alone. Brachyhypopomus comprises 28 species. Here we describe 15 new species, and provide redescriptions of all 13 previously described species, based on meristic, morphometric, and other morphological characters. We include notes on ecology and natural history for each species, and provide regional dichotomous keys and distribution maps, based on the examination of 12,279 specimens from 2,787 museum lots. A lectotype is designated for Brachyhypopomus pinnicaudatus (Hopkins, Comfort, Bastian & Bass, 1990). Brachyhypopomus species are abundant in shallow lentic and slow-flowing freshwater habitats from southern Costa Rica and northern Venezuela to Uruguay and northern Argentina. Species diversity is highest in Greater Amazonia, where 20 species occur: B. alberti, new species, B. arrayae, new species, and B. cunia, new species, in the upper rio Madeira drainage; B. batesi, new species, in the central Amazon and rio Negro; B. beebei, B. brevirostris, B. regani, new species, B. sullivani, new species, and B. walteri, widespread through the Amazon and Orinoco basins and the Guianas; B. belindae, new species, in the central Amazon basin; B. benjamini, new species, and B. verdii, new species, in the upper Amazon basin; B. bennetti, in the upper, central, and lower Amazon, lower Tocantins, and upper Madeira basins; B. bullocki in the Orinoco, Negro and Essequibo drainages; B. diazi in the Orinoco Llanos; B. flavipomus, new species, and B. hamiltoni, new species, in the central and upper Amazon basin; B. hendersoni, new species, in the central Amazon, lower Negro and Essequibo basins; B. pinnicaudatus in the central and lower Amazon, lower, upper Madeira, lower Tocantins and Mearim basins, and coastal French Guiana; and B. provenzanoi, new species, in the upper Orinoco and upper Negro basins. Five species are known from the Paraná-Paraguay-Uruguay basin and adjacent southern Atlantic drainages: B. bombilla in the lower Paraná, upper, central, and lower Paraguay, Uruguay and Patos-Mirim drainages; B. brevirostris in the upper Paraguay basin; B. draco in the lower Paraná, lower Paraguay, Uruguay, Patos-Mirim, and Tramandaí basins; B. gauderio in the lower Paraná, upper, central, and lower Paraguay, Uruguay, Patos-Mirim and Tramandaí basins; and B. walteri in the lower Paraná and upper Paraguay basins. Two species occur in small Atlantic drainages of southern Brazil: B. janeiroensis in the São João, Paraíba and small intervening drainages; and B. jureiae in the Ribeira de Iguape and Una do Prelado. One species occurs in the middle and upper São Francisco basin: B. menezesi, new species. Three species occur in trans-Andean drainages: B. diazi in Caribbean drainages of northern Venezuela; B. occidentalis in Atlantic and Pacific drainages of southern Costa Rica and Panama to Darién, and the Maracaibo, Magdalena, Sinú and Atrato drainages; and B. palenque, new species, in Pacific drainages of Ecuador.(AU)

Peixes elétricos do gênero Brachyhypopomus Mago-Leccia, 1994, são diagnosticados dos outros Rhamphichthyoidea (Rhamphichthyidae + Hypopomidae) pela presença de uma ossificação discóide na porção anterior do palatoquadrado, e pelos seguintes caracteres externos: focinho curto, 18,7-32,6% do comprimento da cabeça (vs. 33,3-68,6% em Hypopomus, Gymnorhamphichthys, Iracema e Rhamphichthys), ausência de um órgão elétrico acessório pareado na região mental ou humeral (vs. presença em Hypopygus e Steatogenys), presença de 3-4 proximais peitorais radiais (vs. 5 em Akawaio), presença do antiorbital + infraorbital, e dos canais ossificados da linha lateral da região cefálica do pré-opérculo (vs. ausência em Racenisia). Brachyhypopomus não pode ser diagnosticado de maneira não-ambígua de Microsternarchus ou Procerusternarchus, com base em caracteres de morfologia externa. Brachyhypopomus compreende 28 espécies válidas. Aqui nós descrevemos 15 espécies novas, e fornecemos a redescrição de 13 espécies previamente descritas, baseado em caracteres merísticos, morfométricos e outros caracteres morfológicos. Nós incluímos notas sobre à ecologia e história natural para cada uma das espécies, e fornecemos chaves dicotômicas regionais e mapas de distribuição baseado no exame de 12.279 espécimes de 2.787 lotes de museus. Um lectótipo é designado para Brachyhypopomus pinnicaudatus (Hopkins, Comfort, Bastian & Bass, 1990). Espécies de Brachyhypopomus são abundantes em habitats de águas rasas lênticas e com correntes fracas, ocorrendo do sul da Costa Rica e norte da Venezuela ao Uruguai e norte da Argentina. A diversidade de espécies é maior na Grande Amazônia, onde 20 espécies ocorrem: B. alberti, espécie nova, B. arrayae, espécie nova e B. cunia, espécie nova, na drenagem do alto rio Madeira; B. batesi, espécie nova, na Amazônia central e rio Negro; B. beebei, B. brevirostris, B. regani, espécie nova, B. sullivani, espécie nova e B. walteri, amplamente distribuídas nas bacias Amazônicas e do Orinoco, e nas Guianas; B. belindae, espécie nova, bacia Amazônica central; B. benjamini, espécie nova e B. verdii, espécie nova, na bacia do alto Amazonas; B. bennetti, no alto, médio e porções baixas da bacia Amazônica, baixo Tocantins e alto rio Madeira; B. bullocki nas drenagens do Orinoco, Negro e Essequibo; B. diazi nos Llanos do Orinoco; B. flavipomus, espécie nova e B. hamiltoni, espécie nova, no médio e alto Amazonas; B. hendersoni, espécie nova, na Amazônia central, baixo Negro e Essequibo; B. pinnicaudatus no médio e baixo Amazonas, baixo e alto Madeira, baixo Tocantins, bacia do Mearim e rios costeiros da Guiana Francesa; e B. provenzanoi, espécie nova, nas bacias do alto Orinoco e alto Negro. Cinco espécies são conhecidas das bacias Paraná-Paraguai-Uruguai e bacias adjacentes das drenagens do sul do Brasil: B. bombilla no alto, médio e baixo Paraguai, baixo Paraná, Uruguai e drenagens Patos-Mirim; B. brevirostris da bacia do alto Paraguai; B. draco das bacias do baixo Paraguai, baixo Paraná, Uruguai, Patos-Mirim e Tramandaí; B. gauderio das bacias do alto, médio e baixo Paraguai, baixo Paraná, Uruguai, Patos-Mirim e Tramandaí; e B. walteri das bacias do alto Paraguai e baixo Paraná. Duas espécies ocorrem nas drenagens costeiras do sudeste do Brasil: B. janeiroensis no São João, Paraíba e em drenagens menores nas adjacências; e B. jureiae no Ribeira de Iguape e Una do Prelado. Uma espécie ocorre no médio e alto rio São Francisco: B. menezesi, espécie nova. Três espécies ocorrem nas drenagens trans-Andinas: B. diazi nas drenagens do Caribe no norte da Venezuela; B. occidentalis nas drenagens do Atlantico e Pacífico do sul da Costa Rica e Panamá até Darién, e nas drenagens do Maracaibo, Magdalena, Sinú e Atrato; e B. palenque, espécie nova, nas drenagens do Pacífico no Equador.(AU)

Reproductive character displacement and signal ontogeny in a sympatric assemblage of electric fish.

The reproductive signals of two or more taxa may diverge in areas of sympatry, due to selection against costly reproductive interference. This divergence, termed reproductive character displacement (RCD), is expected in species-rich assemblages, where interspecific signal partitioning among closely related species is common. However, RCD is usually documented from simple two-taxon cases, via geographical tests for greater divergence of reproductive traits in sympatry than in allopatry. We propose a novel approach to recognizing and understanding RCD in multi-species communities--one that traces the displacement of signals within multivariate signal space during the ontogeny of individual animals. We argue that a case for RCD can be made if the amount of signal displacement between a pair of species after maturation is negatively correlated to distance in signal space before maturation. Our application of this approach, using a dataset of communication signals from a sympatric Amazonian assemblage of the electric fish genus Gymnotus, provides strong evidence for RCD among multiple species. We argue that RCD arose from the costs of heterospecific mismating, but interacted with sexual selection--favoring the evolution of conspicuous male signals that not only serve for mate-choice, but which simultaneously facilitate species recognition.