Understanding daily rhythms in weakly electric fish: the role of melatonin on the electric behavior of Brachyhypopomus gauderio.

Living organisms display molecular, physiological and behavioral rhythms synchronized with natural environmental cycles. Understanding the interaction between environment, physiology and behavior requires taking into account the complexity of natural habitats and the diversity of behavioral and physiological adaptations. Brachyhypopomus gauderio is characterized by the emission of electric organ discharges (EOD), with a very stable rate modulated by social and environmental cues. The nocturnal arousal in B. gauderio coincides with a melatonin-dependent EOD rate increase. Here, we first show a daily cycle in both the EOD basal rate (EOD-BR) and EOD-BR variability of B. gauderio in nature. We approached the understanding of the role of melatonin in this natural behavior through both behavioral pharmacology and in vitro assays. We report, for the first time in gymnotiformes, a direct effect of melatonin on the pacemaker nucleus (PN) in in vitro preparation. Melatonin treatment lowered EOD-BR in freely moving fish and PN basal rate, while increasing the variability of both. These results show that melatonin plays a key role in modulating the electric behavior of B. gauderio through its effect on rate and variability, both of which must be under a tight temporal regulation to prepare the animal for the challenging nocturnal environment.

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.

Electrosensory and metabolic responses of weakly electric fish to changing water conductivity.

Weakly electric gymnotiform fishes use self-generated electric organ discharges (EODs) to navigate and communicate. The electrosensory range for these processes is a function of EOD amplitude, determined by the fish's electric organ (EO) output and the electrical conductivity of the surrounding water. Anthropogenic activity, such as deforestation, dams and industrial/agricultural runoff, are known to increase water conductivity in neotropical habitats, likely reducing the electrosensory range of these fish. We investigated whether fish modulate EO output as means of re-expanding electrosensory range after a rapid increase in water conductivity in the pulse-type Brachyhypopomus gauderio and the wave-type Eigenmannia virescens. Furthermore, because EOD production incurs significant metabolic costs, we assessed whether such compensation is associated with an increase in metabolic rate. Following the conductivity increase, B. gauderio increased EOD amplitude by 20.2±4.3% over 6 days but with no associated increase in metabolic rate, whereas the EOD amplitude of E. virescens remained constant, accompanied by an unexpected decrease in metabolic rate. Our results suggest that B. gauderio uses a compensation mechanism that requires no metabolic investment, such as impedance matching, or a physiological trade-off wherein energy is diverted from other physiological processes to increase EO output. These divergent responses between species could be the result of differences in reproductive life history or evolutionary adaptations to different aquatic habitats. Continued investigation of electrosensory responses to changing water conditions will be essential for understanding the effects of anthropogenic disturbances on gymnotiforms, and potential physiological mechanisms for adapting to a rapidly changing aquatic environment.

Unraveling the complex phylogeographic history of freshwater fishes in Lower Central America: A study of the electric fish Brachyhypopomus occidentalis.

Lower Central America (LCA) has a complex biogeographic history shaped by the rise of the Isthmus of Panama and the global climatic oscillations of the Pleistocene. These events have been crucial in structuring biodiversity in LCA, but their consequences for the distribution and partitions of genetic diversity across the region remain to be elucidated. We combined complete mitochondrial genomes and nuclear ultraconserved elements (UCEs) to study the phylogeographic history and population genetic structure of the electric fish Brachyhypopomus occidentalis in LCA. Our results are consistent with the known phylogeographic history of B. occidentalis in LCA, but we update this history in several important ways that help illuminate the phylogeographic history of freshwater fishes in the region. We provide: i) support for three waves of colonization, two of which occurred prior to the final closure of the Panama Isthmus; ii) a more precise understanding of each colonization event, with evidence for a larger footprint of the first event, as well as genetic exchange across the continental divide in subsequent events; and iii) evidence for high levels of previously unrecognized population genetic structure across LCA. This updated model of colonization and diversification of B. occidentalis consists of three waves of dispersal and colonization, which triggered the evolution of geographic breaks in both nuclear and mitochondrial genomes across LCA. These processes are tightly linked to the dynamic uplift of the Isthmus, recent volcanic activity in the region, and the sea-level oscillations of the Pleistocene. These results improve previous phylogeographic inferences regarding the distribution and diversification of freshwater fishes in LCA, and generate testable hypotheses to guide future research exploring the factors shaping biodiversity in the region.

Histochemical and immunohistochemical analysis of testicular morphology and spermatogenesis in Gymnotus carapo (Teleostei: Gymnotidae).

This work aims to study the testicular morphology and spermatogenesis of Gymnotus carapo to provide information on their reproductive biology which is useful in managing this species as a fishing resource. The testicles were isolated and fixed in 10% formalin; subsequently, they were processed for scanning electron microscopy with conventional histological technique. To analyze the cell proliferation of germline cells and Sertoli cells, immunodetection of the proliferating cell nuclear antigen (PCNA) protein was performed. In G. carapo spermatogenesis, the spermatogenic line is organized into cysts. Spermatogonia A is characterized by more bigger and solitary cells. Spermatogonia B are smaller cells; their nucleus has a larger area concerning the cytoplasm and is grouped in tubules. Spermatocytes (I-II) are smaller than spermatogonia in the prophase of meiotic division. Spermatids are cells with dense, rounded nucleus. The sperm were found in the lumen of the tubule. By immunostaining PCNA, it was possible to observe the proliferative activity of germ line cells and Sertoli cells during the cyst reorganization phase. These results are the basis for future studies focusing on the analysis compared to females of the reproductive cycle of G. carapo.

The effect of urethane and MS-222 anesthesia on the electric organ discharge of the weakly electric fish Apteronotus leptorhynchus.

Urethane and MS-222 are agents widely employed for general anesthesia, yet, besides inducing a state of unconsciousness, little is known about their neurophysiological effects. To investigate these effects, we developed an in vivo assay using the electric organ discharge (EOD) of the weakly electric fish Apteronotus leptorhynchus as a proxy for the neural output of the pacemaker nucleus. The oscillatory neural activity of this brainstem nucleus drives the fish's EOD in a one-to-one fashion. Anesthesia induced by urethane or MS-222 resulted in pronounced decreases of the EOD frequency, which lasted for up to 3 h. In addition, each of the two agents caused a manifold increase in the generation of transient modulations of the EOD known as chirps. The reduction in EOD frequency can be explained by the modulatory effect of urethane on neurotransmission, and by the blocking of voltage-gated sodium channels by MS-222, both within the circuitry controlling the neural oscillations of the pacemaker nucleus. The present study demonstrates a marked effect of urethane and MS-222 on neural activity within the central nervous system and on the associated animal's behavior. This calls for caution when conducting neurophysiological experiments under general anesthesia and interpreting their results.

Living life with an electric touch.

The electric organ discharges (EODs) produced by weakly electric fish have long been a source of scientific intrigue and inspiration. The study of these species has contributed to our understanding of the organization of fixed action patterns, as well as enriching general imaging theory by unveiling the dual impact of an agent's actions on the environment and its own sensory system during the imaging process. This Centenary Review firstly compares how weakly electric fish generate species- and sex-specific stereotyped electric fields by considering: (1) peripheral mechanisms, including the geometry, channel repertoire and innervation of the electrogenic units; (2) the organization of the electric organs (EOs); and (3) neural coordination mechanisms. Secondly, the Review discusses the threefold function of the fish-centered electric fields: (1) to generate electric signals that encode the material, geometry and distance of nearby objects, serving as a short-range sensory modality or 'electric touch'; (2) to mark emitter identity and location; and (3) to convey social messages encoded in stereotypical modulations of the electric field that might be considered as species-specific communication symbols. Finally, this Review considers a range of potential research directions that are likely to be productive in the future.

The sensory effects of light on the electric organ discharge rate of Gymnotus omarorum.

Gymnotiformes are nocturnal fishes inhabiting the root mats of floating plants. They use their electric organ discharge (EOD) to explore the environment and to communicate. Here, we show and describe tonic and phasic sensory-electromotor responses to light distinct from indirect effects depending on the light-induced endogenous circadian rhythm. In the dark, principally during the night, inter-EOD interval histograms are bimodal: the main peak corresponds to the basal rate and a secondary peak corresponds to high-frequency bouts. Light causes a twofold tonic but opposing effect on the EOD histogram: (i) decreasing the main mode and (ii) blocking the high-frequency bouts and consequently increasing the main peak at the expense of removal of the secondary one. Additionally, light evokes phasic responses whose amplitude increases with intensity but whose slow time course and poor adaptation differentiate from the so-called novelty responses evoked by abrupt changes in sensory stimuli of other modalities. We confirmed that Gymnotus omarorum tends to escape from light, suggesting that these phasic responses are probably part of a global 'light-avoidance response'. We interpret the data within an ecological context. Fish rest under the shade of aquatic plants during the day and light spots due to the sun's relative movement alert the fish to hide in shady zones to avoid macroptic predators and facilitate tracking the movement of floating plant islands by wind and/or water currents.

Structural and histochemical aspects of the Gymnotus carapo tegument (Teleostei: Gymnotiformes).

The present study aims to structurally and histochemically characterize the Gymnotus carapo tegument. 30 specimens were captured and slaughtered by spinal section with anesthesia. The observation was carried out with a stereoscopic microscope and the body surface was photographed. Fragments of the dorsal, ventral and lateral region were fixed in Bouin's solution for 12 hours and subsequently preserved in 70% alcohol. They were subsequently observed in the scanning electron microscope (SEM). The preparation for SEM was performed following the standardized protocol. Histological preparations were made, and the cuts were colored with H-E, PAS and Coomassie Blue. The images were obtained in an Olympus BX41-ENUTV-4 microscope. From the observations in SEM a plain tegument with pores of different sizes could be evidenced. The scales of the different regions of the body have different ornaments. Microscopically it was composed of a stratified non-keratinized epithelium consisting of two types of morphologically distinct cells: epidermal cells and mucous cells (PAS-Commassie Blue positive). Under the epithelium there is a layer of dense irregular connective tissue with associated chromatophores and more deeply scales. These analyzes are the basis for future studies that will focus on elucidating the events related to integumentary healing in this species.

Morphological description and molecular characterization of Ancyracanthus electrophori n. sp. (Gnathostomatoidea: Gnathostomatidae): a new nematode parasitic in the electric eel Electrophorus varii (Gymnotiformes: Gymnotidae), from the Brazilian Amazon.

A new species of Ancyracanthus, parasite of the electric eel Electrophorus varii, in the Brazilian Amazon, is described based on morphological and molecular characterization. Ancyracanthus electrophori n. sp. differs from the two congeners namely, Ancyracanthus pinnatifidus and Ancyracanthus schubarti, based on the structure of cephalic appendages, number and arrangement of caudal papillae in males, vulva very close to anus in females, eggs with smoothly mamillated shell, host taxon and geographical origin. Moreover, the new species is the first in the genus to be described with thorny cuticular rings and to be observed with the use of scanning electron microscopy (SEM). The morphology of A. pinnatifidus and A. schubarti is still poorly-known and should be revised in details; however, the separation between them and the new species was clear. Genetic characterization based on 28S rDNA and cytochrome c oxidase subunit I (cox1) mtDNA partial sequences, performed for the first time in Acyracanthus, along with phylogenetic reconstructions using both genetic markers, placed Ancyracanthus electrophori n. sp. in a suggestive basal position within Gnathostomatidae. Phylogenetic reconstructions using cox1 sequences also suggested lack of monophyly in the genera Gnathostoma and Spiroxys and, consequently, in the subfamilies Gnathostominae and Spiroxyinae. However, such results are preliminary. With the first genetic characterization and observations using SEM in Ancyracanthus, resulting in the discovery of a new species and in the expansion of the geographical occurrence of the genus to Amazonian fish, an important step towards a better understanding of these nematodes has been taken.

Proteomic characterization of spontaneously regrowing spinal cord following injury in the teleost fish Apteronotus leptorhynchus, a regeneration-competent vertebrate.

In adult mammals, spontaneous repair after spinal cord injury (SCI) is severely limited. By contrast, teleost fish successfully regenerate injured axons and produce new neurons from adult neural stem cells after SCI. The molecular mechanisms underlying this high regenerative capacity are largely unknown. The present study addresses this gap by examining the temporal dynamics of proteome changes in response to SCI in the brown ghost knifefish (Apteronotus leptorhynchus). Two-dimensional difference gel electrophoresis (2D DIGE) was combined with matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) and tandem mass spectrometry (MS/MS) to collect data during early (1 day), mid (10 days), and late (30 days) phases of regeneration following caudal amputation SCI. Forty-two unique proteins with significant differences in abundance between injured and intact control samples were identified. Correlation analysis uncovered six clusters of spots with similar expression patterns over time and strong conditional dependences, typically within functional families or between isoforms. Significantly regulated proteins were associated with axon development and regeneration; proliferation and morphogenesis; neuronal differentiation and re-establishment of neural connections; promotion of neuroprotection, redox homeostasis, and membrane repair; and metabolism or energy supply. Notably, at all three time points examined, significant regulation of proteins involved in inflammatory responses was absent.

Morphology and receptive field organization of a temporal processing region in Apteronotus albifrons.

The timing system of weakly electric fishes is vital for many behavioral processes, but the system has been relatively unexplored in Apteronotus albifrons. This paper describes the receptive fields of phase-locked neurons in the midbrain of A. albifrons, in combination with neuroanatomy and electron microscopy (EM) to delineate a phase-locked area in this fish, the magnocellular mesencephalic nucleus (MMN). The MMN was isolated electrophysiologically through the detection of phase-locked field potentials of high amplitude. Single-cell recordings were made with a sharp electrode while a phase-locked modulated stimulus was provided to the fish. Receptive field centers of phase-locked neurons in MMN were consistent with tuberous electroreceptor density maps from previous studies, but no receptive field centers were found in the posterior 50% of the body. Intracellular and extracellular labeling of MMN revealed three cell populations: giant cells with large somata (19-24 µm) and their axonal arborizations which span across the entire extent of MMN, axon terminals from spherical cells of the electrosensory lateral line lobe (ELL), and small cell somata (3-7 µm) along with their projections which extend outside the nucleus. EM revealed multiple gap junction and chemical synapses within MMN. Our results indicate that MMN is a dedicated temporal processing center in A. albifrons.

Electrocommunication signals and aggressive behavior vary among male morphs in an apteronotid fish, Compsaraia samueli.

Within-species variation in male morphology is common among vertebrates and is often characterized by dramatic differences in behavior and hormonal profiles. Males with divergent morphs also often use communication signals in a status-dependent way. Weakly electric knifefish are an excellent system for studying variation in male morphology and communication and its hormonal control. Knifefish transiently modulate the frequency of their electric organ discharge (EOD) during social encounters to produce chirps and rises. In the knifefish Compsaraia samueli, males vary extensively in jaw length. EODs and their modulations (chirps and rises) have never been investigated in this species, so it is unclear whether jaw length is related to the function of these signals. We used three behavioral assays to analyze EOD modulations in male C. samueli: (1) artificial playbacks, (2) relatively brief, live agonistic dyadic encounters, and (3) long-term overnight recordings. We also measured circulating levels of two androgens, 11-ketotestosterone and testosterone. Chirp structure varied within and across individuals in response to artificial playback, but was unrelated to jaw length. Males with longer jaws were more often dominant in dyadic interactions. Chirps and rises were correlated with and preceded attacks regardless of status, suggesting these signals function in aggression. In longer-term interactions, chirp rate declined after 1 week of pairing, but was unrelated to male morphology. Levels of circulating androgens were low and not predictive of jaw length or EOD signal parameters. These results suggest that communication signals and variation in male morphology are linked to outcomes of non-breeding agonistic contests.

Knifefish turning control and hydrodynamics during forward swimming.

Rapid turning and swimming contribute to ecologically important behaviors in fishes such as predator avoidance, prey capture, mating and the navigation of complex environments. For riverine species, such as knifefishes, turning behaviors may also be important for navigating locomotive perturbations caused by turbulent flows. Most research on fish maneuvering focuses on fish with traditional fin and body morphologies, which primarily use body bending and the pectoral fins during turning. However, it is uncertain how fishes with uncommon morphologies are able to achieve sudden and controllable turns. Here, we studied the turning performance and the turning hydrodynamics of the black ghost knifefish (Apteronotus albifrons, N=6) which has an atypical elongated ribbon fin. Fish were filmed while swimming forward at ∼2 body lengths s-1 and feeding from a fixed feeder (control) and an oscillating feeder (75 Hz) at two different amplitudes. 3D kinematic analysis of the body revealed the highest pitch angles and lowest body bending coefficients during steady swimming. Low pitch angle, high maximum yaw angles and large body bending coefficients were characteristic of small and large turns. Asynchrony in pectoral fin use was low during turning; however, ribbon fin wavelength, frequency and wave speed were greatest during large turns. Digital particle image velocimetry (DPIV) showed larger counter-rotating vortex pairs produced during turning by the ribbon fin in comparison to vortices rotating in the same direction during steady swimming. Our results highlight the ribbon fin's role in controlled rapid turning through modulation of wavelength, frequency and wave speed.

Development of the electric organ in embryos and larvae of the knifefish, Brachyhypopomus gauderio.

South American Gymnotiform knifefish possess electric organs that generate electric fields for electro-location and electro-communication. Electric organs in fish can be derived from either myogenic cells (myogenic electric organ/mEO) or neurogenic cells (neurogenic electric organ/nEO). To date, the embryonic development of EOs has remained obscure. Here we characterize the development of the mEO in the Gymnotiform bluntnose knifefish, Brachyhypopomus gauderio. We find that EO primordial cells arise during embryonic stages in the ventral edge of the tail myotome, translocate into the ventral fin and develop into syncytial electrocytes at early larval stages. We also describe a pair of thick nerve cords that flank the dorsal aorta, the location and characteristic morphology of which are reminiscent of the nEO in Apteronotid species, suggesting a common evolutionary origin of these tissues. Taken together, our findings reveal the embryonic origins of the mEO and provide a basis for elucidating the mechanisms of evolutionary diversification of electric charge generation by myogenic and neurogenic EOs.

Glutamatergic control of a pattern-generating central nucleus in a gymnotiform fish.

The activity of central pattern-generating networks (CPGs) may change under the control exerted by various neurotransmitters and modulators to adapt its behavioral outputs to different environmental demands. Although the mechanisms underlying this control have been well established in invertebrates, most of their synaptic and cellular bases are not yet well understood in vertebrates. Gymnotus omarorum, a pulse-type gymnotiform electric fish, provides a well-suited vertebrate model to investigate these mechanisms. G. omarorum emits rhythmic and stereotyped electric organ discharges (EODs), which function in both perception and communication, under the command of an electromotor CPG. This nucleus is composed of electrotonically coupled intrinsic pacemaker cells, which pace the rhythm, and bulbospinal projecting relay cells that contribute to organize the pattern of the muscle-derived effector activation that produce the EOD. Descending influences target CPG neurons to produce adaptive behavioral electromotor responses to different environmental challenges. We used electrophysiological and pharmacological techniques in brainstem slices of G. omarorum to investigate the underpinnings of the fast transmitter control of its electromotor CPG. We demonstrate that pacemaker, but not relay cells, are endowed with ionotropic and metabotropic glutamate receptor subtypes. We also show that glutamatergic control of the CPG likely involves two types of synapses contacting pacemaker cells, one type containing both α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) and N-methyl-d-aspartate (NMDA) receptors and the other one only-NMDA receptor. Fast neurotransmitter control of vertebrate CPGs seems to exploit the kinetics of the involved postsynaptic receptors to command different behavioral outputs. The prospect of common neural designs to control CPG activity in vertebrates is discussed.NEW & NOTEWORTHY Underpinnings of neuromodulation of central pattern-generating networks (CPG) have been well characterized in many species. The effects of fast neurotransmitter systems remain, however, poorly understood. This research uses in vitro electrophysiological and pharmacological techniques to show that the neurotransmitter control of a vertebrate CPG in gymnotiform fish involves the convergence of only-NMDA and AMPA-NMDA glutamatergic synapses onto neurons that pace the rhythm. These inputs may organize different behavioral outputs according to their distinct functional properties.

Paraphyly and evolutionary independent lineages in Gymnotus pantherinus (Gymnotiformes: Gymnotidae) in the Brazilian Atlantic Forest Coastal Streams.

In the Brazilian Atlantic Forest (AF), many terrestrial species with broad geographical distributions show high diversity and endemism of intraspecific lineages, as revealed by molecular genetic data. This pattern, however, is less explored in freshwater fishes. Gymnotus pantherinus is an electric fish endemic to the Brazilian coastal drainages that shows a wide distribution, ranging from the states of Bahia to Santa Catarina, an unusual pattern for AF fishes. It has been hypothesized that G. pantherinus is a species complex because distinct morphotypes were described for the species based on morphometric and meristic features. We used mitochondrial and nuclear data to test this hypothesis. Based on phylogenetic inference and multi-locus, multispecies coalescent methods, we identified six independent lineages, flagging them as candidate species. One such lineage is the recently described species G. refugio that is nested within G. pantherinus and renders it paraphyletic, showing it is a species complex. We named G. pantherinus stricto sensu the lineage that includes samples from the type locality (Santos, SP). Our results show that genetic lineages correspond only partially and far exceed the number of previously reported morphotypes. Genetic breaks in the group correspond to landscape features associated with the Serra do Mar mountain range and with riverine dynamics caused by sea level changes during the last glacial maximum. Moreover, we found evidence of river capture events affecting phylogeographic structure in the group. We uncovered an important dimension of diversity in the group and encourage further integration of genetic and phenotypic data. Such integration is a fruitful approach not only to reduce the gap between taxonomy and evolutionary history in Gymnotidae, but also to uncover the real AF biodiversity.

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.

Descending pathways generate perception of and neural responses to weak sensory input.

Natural sensory stimuli frequently consist of a fast time-varying waveform whose amplitude or contrast varies more slowly. While changes in contrast carry behaviorally relevant information necessary for sensory perception, their processing by the brain remains poorly understood to this day. Here, we investigated the mechanisms that enable neural responses to and perception of low-contrast stimuli in the electrosensory system of the weakly electric fish Apteronotus leptorhynchus. We found that fish reliably detected such stimuli via robust behavioral responses. Recordings from peripheral electrosensory neurons revealed stimulus-induced changes in firing activity (i.e., phase locking) but not in their overall firing rate. However, central electrosensory neurons receiving input from the periphery responded robustly via both phase locking and increases in firing rate. Pharmacological inactivation of feedback input onto central electrosensory neurons eliminated increases in firing rate but did not affect phase locking for central electrosensory neurons in response to low-contrast stimuli. As feedback inactivation eliminated behavioral responses to these stimuli as well, our results show that it is changes in central electrosensory neuron firing rate that are relevant for behavior, rather than phase locking. Finally, recordings from neurons projecting directly via feedback to central electrosensory neurons revealed that they provide the necessary input to cause increases in firing rate. Our results thus provide the first experimental evidence that feedback generates both neural and behavioral responses to low-contrast stimuli that are commonly found in the natural environment.

Beyond the Kármán gait: knifefish swimming in periodic and irregular vortex streets.

Neotropical freshwater fishes such as knifefishes are commonly faced with navigating intense and highly unsteady streams. However, our knowledge on locomotion in apteronotids comes from laminar flows, where the ribbon fin dominates over the pectoral fins or body bending. Here, we studied the 3D kinematics and swimming control of seven black ghost knifefish (Apteronotus albifrons) moving in laminar flows (flow speed U∞≈1-5 BL s-1) and in periodic vortex streets (U∞≈2-4 BL s-1). Two different cylinders (∼2 and ∼3 cm diameter) were used to generate the latter. Additionally, fish were exposed to an irregular wake produced by a free oscillating cylinder (∼2 cm diameter; U∞≈2 BL s-1). In laminar flows, knifefish mainly used their ribbon fin, with wave frequency, speed and acceleration increasing with U∞. In contrast, knifefish swimming behind a fixed cylinder increased the use of pectoral fins, which resulted in changes in body orientation that mimicked steady backward swimming. Meanwhile, individuals behind the oscillating cylinder presented a combination of body bending and ribbon and pectoral fin movements that counteract the out-of-phase yaw oscillations induced by the irregular shedding of vortices. We corroborated passive out-of-phase oscillations by placing a printed knifefish model just downstream of the moving cylinder, but when placed one cylinder diameter downstream, the model oscillated in phase. Thus, the wake left behind an oscillating body is more challenging than a periodic vortex shedding for an animal located downstream, which may have consequences on inter- and intra-specific interactions.