Androgen receptors rapidly modulate non-breeding aggression in male and female weakly electric fish (Gymnotus omarorum).

The South American weakly electric fish, Gymnotus omarorum, displays territorial aggression year-round in both sexes. To examine the role of rapid androgen modulation in non-breeding aggression, we administered acetate cyproterone (CPA), a potent inhibitor of androgen receptors, to both male and females, just before staged agonistic interactions. Wild-caught fish were injected with CPA and, 30 min later, paired in intrasexual dyads. We then recorded the agonistic behavior which encompasses both locomotor displays and emission of social electric signals. We found that CPA had no discernible impact on the levels of aggression or the motivation to engage in aggressive behavior for either sex. However, CPA specifically decreased the expression of social electric signals in both males and female dyads. The effect was status-dependent as it only affected subordinate electrocommunication behavior, the emission of brief interruptions in their electric signaling ("offs"). This study is the first demonstration of a direct and rapid androgen effect mediated via androgen receptors on non-breeding aggression. Elucidating the mechanisms involved in non-breeding aggression in this teleost model allows us to better understand potentially conserved or convergent neuroendocrine mechanisms underlying aggression in vertebrates.

Derived loss of signal complexity and plasticity in a genus of weakly electric fish.

Signal plasticity can maximize the usefulness of costly animal signals such as the electric organ discharges (EODs) of weakly electric fishes. Some species of the order Gymnotiformes rapidly alter their EOD amplitude and duration in response to circadian cues and social stimuli. How this plasticity is maintained across related species with different degrees of signal complexity is poorly understood. In one genus of weakly electric gymnotiform fish (Brachyhypopomus), only one species, B. bennetti, produces a monophasic signal while all other species emit complex biphasic or multiphasic EOD waveforms produced by two overlapping but asynchronous action potentials in each electric organ cell (electrocyte). One consequence of this signal complexity is the suppression of low-frequency signal content that is detectable by electroreceptive predators. In complex EODs, reduction of the EOD amplitude and duration during daytime inactivity can decrease both predation risk and the metabolic cost of EOD generation. We compared EOD plasticity and its underlying physiology in Brachyhypopomus focusing on B. bennetti. We found that B. bennetti exhibits minimal EOD plasticity, but that its electrocytes retained vestigial mechanisms of biphasic signaling and vestigial mechanisms for modulating the EOD amplitude. These results suggest that this species represents a transitional phenotypic state within a clade where signal complexity and plasticity were initially gained and then lost. Signal mimicry, mate recognition and sexual selection are potential factors maintaining the monophasic EOD phenotype in the face of detection by electroreceptive predators.

The weakly electric fish, Apteronotus albifrons, actively avoids experimentally induced hypoxia.

Anthropogenic environmental degradation has led to an increase in the frequency and prevalence of aquatic hypoxia (low dissolved oxygen concentration, DO), which may affect habitat quality for water-breathing fishes. The weakly electric black ghost knifefish, Apteronotus albifrons, is typically found in well-oxygenated freshwater habitats in South America. Using a shuttle-box design, we exposed juvenile A. albifrons to a stepwise decline in DO from normoxia (> 95% air saturation) to extreme hypoxia (10% air saturation) in one compartment and chronic normoxia in the other. On average, A. albifrons actively avoided the hypoxic compartment below 22% air saturation. Hypoxia avoidance was correlated with upregulated swimming activity. Following avoidance, fish regularly ventured back briefly into deep hypoxia. Hypoxia did not affect the frequency of their electric organ discharges. Our results show that A. albifrons is able to sense hypoxia at non-lethal levels and uses active avoidance to mitigate its adverse effects.

Distribution of the cholinergic nuclei in the brain of the weakly electric fish, Apteronotus leptorhynchus: Implications for sensory processing.

Acetylcholine acts as a neurotransmitter/neuromodulator of many central nervous system processes such as learning and memory, attention, motor control, and sensory processing. The present study describes the spatial distribution of cholinergic neurons throughout the brain of the weakly electric fish, Apteronotus leptorhynchus, using in situ hybridization of choline acetyltransferase mRNA. Distinct groups of cholinergic cells were observed in the telencephalon, diencephalon, mesencephalon, and hindbrain. These included cholinergic cell groups typically identified in other vertebrate brains, for example, motor neurons. Using both in vitro and ex vivo neuronal tracing methods, we identified two new cholinergic connections leading to novel hypotheses on their functional significance. Projections to the nucleus praeeminentialis (nP) arise from isthmic nuclei, possibly including the nucleus lateralis valvulae (nLV) and the isthmic nucleus (nI). The nP is a central component of all electrosensory feedback pathways to the electrosensory lateral line lobe (ELL). We have previously shown that some neurons in nP, TS, and tectum express muscarinic receptors. We hypothesize that, based on nLV/nI cell responses in other teleosts and isthmic connectivity in A. leptorhynchus, the isthmic connections to nP, TS, and tectum modulate responses to electrosensory and/or visual motion and, in particular, to looming/receding stimuli. In addition, we found that the octavolateral efferent (OE) nucleus is the likely source of cholinergic fibers innervating the ELL. In other teleosts, OE inhibits octavolateral hair cells during locomotion. In gymnotiform fish, OE may also act on the first central processing stage and, we hypothesize, implement corollary discharge modulation of electrosensory processing during locomotion.

Individual Repeatability of Locomotor Kinematics and Swimming Performance in a Gymnotiform Swimmer.

AbstractGymnotiform swimming is a specialized form of swimming wherein thrust is produced by the ribbonlike motion of an elongate anal fin, while the body is held relatively stiff. This form of swimming has been extensively examined in relation to the biomechanics of thrust production, the kinematics of the anal fin, and neuromuscular control, whereas few studies have examined whole-animal performance parameters of this swimming mode. The goals of this research were to (1) assess the maximum abilities and repeatability of two swimming performance measures, sprinting and prolonged swimming, which would indicate that these performance measures in a gymnotiform swimmer may be a target for selection, similar to body-caudal fin-swimming fish; (2) examine how a gymnotiform swimmer modulates swimming speed; and (3) determine whether modulatory behavior is consistent across different-sized fish and within individuals across time. Sprinting and prolonged swimming were examined in black ghost knifefish (Apteronotus albifrons; N=15), multiple times on the same day, and were measured again 4 wk later. Sprinting ability was measured by chasing a fish down a photocell-lined racetrack and obtaining the fastest speed between any 8-cm span. Prolonged swimming abilities were measured in a constant acceleration test (Ucat) in a Brett-style swim tunnel by measuring the maximum speed the fish could attain against a steadily increasing water velocity. We determined frequency, wavelength, and amplitude of the anal fin sine wave in fish swimming at different speeds during the Ucat trials. We found repeatable measures of sprint speed and Ucat performance over short (day) and medium (4 wk) time periods for both tests. Neither sprint nor Ucat performance was significantly dependent on size, suggesting that the primary driver of performance variation was individual differences in physiology. Most modulation of swimming speed occurred through changes in the frequency of the wave train processing down the anal fin, with only modest changes to the wavelength and minimal changes to amplitude. Finally, we compare our measures of swimming performance in this gymnotiform swimmer to published values of body-caudal fin swimmers to demonstrate that this form of locomotion results in comparable sprint and constant-acceleration values.

An immunohistochemical study on the distribution of vasotocin neurons in the brain of two weakly electric fish, Gymnotus omarorum and Brachyhypopomus gauderio.

Hypothalamic nonapeptides (arginin vasotocin-vasopressin, oxytocin-isotocin) are known to modulate social behaviors across vertebrates. The neuroanatomical conservation of nonapeptide systems enables the use of novel vertebrate model species to identify general strategies of their functional mechanisms. We present a detailed immunohistochemical description of vasotocin (AVT) cell populations and their projections in two species of weakly electric fish with different social structure, Gymnotus omarorum and Brachyhypopomus gauderio. Strong behavioral, pharmacological, and electrophysiological evidence support that AVT modulation of electric behavior differs between the gregarious B. gauderio and the solitary G. omarorum. This functional diversity does not necessarily depend on anatomical differences of AVT neurons. To test this, we focus on interspecific comparisons of the AVT system in basal non-breeding males along the brain. G. omarorum and B. gauderio showed similar AVT somata sizes and comparable distributions of AVT somata and fibers. Interestingly, AVT fibers project to areas related to the control of social behavior and electromotor displays in both species. We found that no gross anatomical differences in the organization of the AVT system account for functional differences between species, which rather shall depend on the pattern of activation of neurons embedded in the same basic anatomical organization of the AVT system.

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.

Dieta do peixe elétrico Gymnorhamphichthys petiti Géry & Vu-Tân-Tuê, 1964 (Rhamphichthyidae), em riachos da bacia do Rio Teles Pires, Amozônia Meridional / Diet of the knifefish Gymnorhamphichthys petiti Géry & Vu-Tân-Tuê, 1964 (Rhamphichthyidae) in streams of Teles pires river basin, Southern Amazon

Gymnorhamphichthys petiti é uma espécie de peixe elétrico que habita o fundo arenoso de riachos da bacia do rio Teles Pires, no entanto pouco se sabe a respeito de sua biologia. O objetivo foi analisar a dieta de G. petiti. As coletas foram realizadas no município de Cláudia, Mato Grosso, na bacia do Rio Teles Pires. As amostragens ocorreram nos meses de julho de 2010 e em maio e junho de 2011, em riachos de 1ª e 2ª ordem. Utilizou-se os métodos de frequência de ocorrência e volume relativo para o cálculo do Índice Alimentar (I.A.%) de 43 exemplares. O comprimento padrão variou entre 47,17 e 120,49 mm e o peso entre 0,12 e 2,04 g. Os itens alimentares encontrados foram: Nematoda, Acari, Ephemeroptera, Plecoptera, Hemiptera, Coleoptera, Trichoptera, Diptera, fragmento de insetos, ovos de insetos, sementes e areia. O item alimentar (IAi) de maior importância na dieta foi Nematoda, em razão do seu maior volume relativo. No entanto, imaturos de insetos da ordem Trichoptera, habitantes do substrato de areia apareceram em maior frequência nos estômagos, diferindo dos resultados encontrados para outras espécies de Gymnorhamphichthys. Tais resultados confirmam que G. petiti tem forte dependência de itens alimentares relacionados ao substrato arenoso.

Gymnorhamphichthys petiti is a species of electric fish that inhabits the sandy bottom of streams of Teles Pires river basin, however, little is known about the biology of this fish. Here we aim to assess the diet of G. petiti and to evaluate the importance of items present in its diet. Samples were collected in the municipality of Claudia, Mato Grosso state. Data collection occurred in July 2010, and in May and June 2011, covering streches of 150 meters of streams of 1st and 2nd order. We used Frequency of Occurrence and Relative Volume to calculate the Feeding Index (I.A.%) for 43 specimens. The standard length ranged from 47.17 to 120.49 mm and weight ranged from 0.12 to 2.04 g. The food items found were: Nematoda, Acari, Ephemeroptera, Plecoptera, Hemiptera, Coleoptera, Trichoptera, Diptera, body parts of insects, insect eggs, seeds and sand. Nematoda was the most important food item, due to its high relative volume. Immature individuals of sand-dwelling Trichoptera, however, were the most frequent item in stomachs, differing from the results for other Gymnorhamphichthys spp. These results confirm the strong dependency of G. petiti on food items present in the sandy substrate of bottoms of streams.

Two new species and a new subgenus of toothed Brachyhypopomus electric knifefishes (Gymnotiformes, Hypopomidae) from the central Amazon and considerations pertaining to the evolution of a monophasic electric organ discharge.

We describe two new, closely related species of toothed Brachyhypopomus (Hypopomidae: Gymnotiformes: Teleostei) from the central Amazon basin and create a new subgenus for them. Odontohypopomus, new subgenus of Brachyhypopomus, is diagnosed by (1) small teeth present on premaxillae; (2) medialmost two branchiostegal rays thin with blades oriented more vertically than remaining three rays; (3) background color in life (and to lesser extent in preservation) distinctly yellowish with head and sides peppered with small, widely spaced, very dark brown stellate chromatophores that greatly contrast with light background coloration; (4) a dark blotch or bar of subcutaneous pigment below the eye; (5) electric organ discharge waveform of very long duration (head-positive phase approx. 2 milliseconds or longer, head-negative phase shorter or absent) and slow pulse repetition rate (3-16 Hz). The type species of the new subgenus, Brachyhypopomus (Odontohypopomus) walteri sp. n., is diagnosed by the following additional character states: (1) subcutaneous dark pigment at base of orbit particularly prominent, (2) body semi-translucent and nearly bright yellow background coloration in life, (3) a biphasic electric organ discharge (EOD) waveform of very long duration (between 3.5 and 4 milliseconds at 25° C) with head-positive first phase significantly longer than second head-negative phase in both sexes. Brachyhypopomus (Odontohypopomus) bennetti sp. n. is diagnosed by two character states in addition to those used to diagnose the subgenus Odontohypopomus: (1) a deep electric organ, visible as large semi-transparent area, occupying approximately 14-17% body depth directly posterior to the abdominal cavity in combination with a short, but deep, caudal filament, and (2) a monophasic, head-positive EOD waveform, approximately 2.1 milliseconds in duration in both sexes. These are the only described rhamphichthyoid gymnotiforms with oral teeth, and Brachyhypopomus bennetti is the first Brachyhypopomus reported to have a monophasic (head-positive) EOD waveform. Unlike biphasic species, the waveform of its EOD is largely unaffected by tail damage from predators. Such injuries are common among specimens in our collections. This species' preference for floating meadow habitat along the major channels of the Amazon River basin may put it at particularly high risk of predation and "tail grazing."

ResumoNós descrevemos duas novas espécies proximamente relacionadas de Brachyhypopomus (Hypopomidae: Gymnotiformes: Teleostei) da porção central da bacia Amazônica e criamos um novo subgênero para elas. Odontohypopomus, novo subgênero de Brachyhypopomus, é diagnosticado por (1) apresentar dentes pequenos no pré-maxilar; (2) pela forma dos dois raios branquiostegais mais internos, com expansão laminar fina orientada mais verticalmente do que nos três raios remanescentes; (3) coloração de fundo em vida (e, em menor grau, após preservação) distintamente amarelada, com a cabeça e flancos marcados por pequenos cromatóforos marrom escuro de formato estelar e bem espaçados entre si, contrastando fortemente com a tonalidade clara de fundo; (4) uma mancha ou barra escura de pigmento subcutâneo abaixo do olho; (5) forma da onda de descarga do órgão elétrico (DOE) de duração muito longa (fase positiva com aproximadamente 2 milisegundos ou mais, fase negativa mais curta ou ausente) e uma baixa taxa de repetição de pulsos (3­16 Hz). A espécie-tipo do novo subgênero, Brachyhypopomus (Odontohypopomus) walteri sp. nov., é adicionalmente diagnosticada pelos seguintes estados de caráter: (1) pigmentação subcutânea na base da órbita particularmente conspícua; (2) corpo semi-translúcido e com coloração geral em vida amarelo forte, (3) DOE com onda bifásica e de duração muito longa (entre 3,5 e 4 milisegundos a 25° C), com a fase inicial positiva significativamente mais longa do que a segunda fase (negativa) em ambos os sexos. Brachyhypopomus (Odontohypopopmus) bennetti sp. nov. é diagnosticada por dois estados de caráter, além daqueles utilizados para diagnosticar o subgênero Odontohypopomus: (1) órgão elétrico largo em vista lateral, visível como uma grande área semitransparente ocupando aproximadamente 14­17% da altura do corpo, medida imediatamente posterior à cavidade abdominal, combinada com um filamento caudal curto e alto; e (2) DOE monofásica positiva, com duração de aproximadamente 2,1 milisegundos em ambos os sexos. Esses são os únicos GymnotiformesRhamphichthyoidea com dentes orais e Brachyhypopomus bennetti é a primeira espécie de Brachyhypopomus conhecida por apresentar uma DOE monofásica positiva. Diferentemente das espécies com DOE bifásica, a forma de onda/pulso dessa espécie não é significantemente afetada por danos ao filamento caudal decorrentes de predação. Esse tipo de dano é comum entre os espécimes examinados em nossas coleções. A ocorrência predominante dessa espécie em bancos flutuantes de macrófitas ao longo de alguns dos principais rios formadores da Bacia Amazônica pode representar um risco particularmente alto de predação e mutilação do filamento caudal.

Proximate and ultimate causes of signal diversity in the electric fish Gymnotus.

A complete understanding of animal signal evolution necessitates analyses of both the proximate (e.g. anatomical and physiological) mechanisms of signal generation and reception, and the ultimate (i.e. evolutionary) mechanisms underlying adaptation and diversification. Here we summarize the results of a synthetic study of electric diversity in the species-rich neotropical electric fish genus Gymnotus. Our study integrates two research directions. The first examines the proximate causes of diversity in the electric organ discharge (EOD) - which is the carrier of both the communication and electrolocation signal of electric fishes - via descriptions of the intrinsic properties of electrocytes, electrocyte innervation, electric organ anatomy and the neural coordination of the discharge (among other parameters). The second seeks to understand the ultimate causes of signal diversity - via a continent-wide survey of species diversity, species-level phylogenetic reconstructions and field-recorded head-to-tail EOD (ht-EOD) waveforms (a common procedure for characterizing the communication component of electric fish EODs). At the proximate level, a comparative morpho-functional survey of electric organ anatomy and the electromotive force pattern of the EOD for 11 species (representing most major clades) revealed four distinct groups of species, each corresponding to a discrete area of the phylogeny of the genus and to a distinct type of ht-EOD waveform. At the ultimate level, our analyses (which emphasize the ht-EOD) allowed us to conclude that selective forces from the abiotic environment have had minimal impact on the communication component of the EOD. In contrast, selective forces of a biotic nature - imposed by electroreceptive predators, reproductive interference from heterospecific congeners, and sexual selection - may be important sources of diversifying selection on Gymnotus signals.