Intraspecific agonistic interactions in freely swimming mormyrid fish, Marcusenius macrolepidotus (South African form)

South African bulldogs (Marcusenius macrolepidotus, Mormyridae) generate brief (less than 1 ms) electric organ discharges (EODs), separated by much longer and highly variable inter-discharge intervals (IDIs). The diurnal and nocturnal overt behaviour and electrical activity were studied under various conditions: in isolated fish, in pairs of fish, and in a group of four fish that were kept in a "natural" large aquarium. EODs from up to four individuals were recorded simultaneously and identified. While resting during the day, isolated fish showed a broad inter-individual variability of IDI patterns, with distribution histogram modes ranging from 85.7 ms to 325.8 ms. When foraging during the day, IDI modes were shorter and less variable (36.3–48.3 ms). Behaviour patterns displayed during nocturnal agonistic encounters were retreating, parallel swimming, anti-parallel display, attack, and fleeing/chasing. High-discharge-rate (HD) displays were observed at several stages of these encounters, for example, during anti-parallel display (a period of low overt motor activity), or following attacks. IDI durations as short as 11 ms occurred during HD displays, which followed low-rate inter-HD activity almost without transition. IDI distribution histogram modes when fish showed anti-parallel display were 15.4 ms and 24.8 ms, and 30.0 ms during nocturnal non-agonistic interactions. No overt fighting was observed once a dominance relationship was established. In a large aquarium, an approaching dominant male evoked a simultaneous discharge arrest in a group of three subdominant males. Electronic Publication     

Production of aggressive electrocommunication signals to progressively realistic social stimuli in male Apteronotus leptorhynchus

Brown ghost knife fish, Apteronotus leptorhynchus, produce a continuous electric organ discharge (EOD) that they use for communication. While interacting aggressively, males also emit brief EOD modulations termed chirps. The simplicity of this behaior and its underlying neural circuitry has made it an important model system in neuroethology. Chirping is typically assayed by confining a fish in a tube (‘chirp chamber’) and presenting it with sine wave electrical stimuli that partially mimic EODs of other fish. We presented male fish with progressively more realistic social stimuli to examine whether some of the stimulus complexities during dyadic interaction influence the production of chirps. In a chirp chamber, fish chirped less to a recording of an EOD containing chirps than to a recording of an EOD alone and to sine wave stimuli. Free‐swimming fish chirped more to stimulus fish than to sine wave stimuli presented through electrodes. Fish chirped more when interacting directly than when interacting across a perforated barrier. Together, these studies demonstrate that the presence of chirps, electric field complexity, and/or non‐electric social stimuli are important in eliciting chirp production in brown ghosts.     

Electric interactions through chirping behavior in the weakly electric fish, Apteronotus leptorhynchus

The weakly electric fish Apteronotus leptorhynchus produces wave-like electric organ discharges distinguished by a high degree of regularity. Transient amplitude and frequency modulations (“chirps”) can be evoked in males by stimulation with the electric field of a conspecific. During these interactions, the males examined in this study produced six types of chirps, including two novel ones. Stimulation of a test fish with a conspecific at various distances showed that two electrically interacting fish must be within 10 cm of each other to evoke chirping behavior in the neighboring fish. The chirp rate of all but one chirp type elicited by the neighboring fish was found to be negatively correlated with the absolute value of the frequency difference between the two interacting fish, but independent of the sign of this difference. Correlation analysis of the instantaneous rates of chirp occurrence revealed two modes of interactions characterized by reciprocal stimulation and reciprocal inhibition. Further analysis of the temporal relationship between the chirps generated by the two fish during electric interactions showed that the chirps generated by one individual follow the chirps of the other with a short latency of approximately 500–1000 ms. We hypothesize that this “echo response” serves a communicatory function.     

A role of burst firings in encoding of spatiotemporally-varying stimulus

To investigate a role of burst firings of neurons in encoding of spatiotemporally-varying stimulus, we focus on electrosensory system of a weakly electric fish. Weakly electric fish generates electric field around its body using electric organ discharge and can accurately detect the location of an object using the modulation of electric field induced by the object. We developed a model of fish body by which we numerically describe the spatiotemporal patterns of electric field around the fish body. We also made neural models of electroreceptor distributed on the fish body and of electrosensory lateral-line lobe (ELL) to investigate what kinds of information of electric field distorted by an object they detect. Here we show that the spatiotemporal features of electric field around the fish body are encoded by the timing of burst firings of ELL neurons. The information of object distance is extracted by the area of synchronous firings of neurons in a higher nucleus, torus semicircularis.     

Display vigour and subsequent fight performance in the siamese fighting fish,betta splendens

The display of 24 individual male Siamese fighting fish to an unresponsive stimulus conspecific was measured, and the fish were then placed together in pairs. For 11 of the 12 pairs, the outcome of the aggressive interaction which ensued was predicted by the gill cover erection durations obtained in the pre-fight isolate tests. The implications of this result for theories of display function are discussed.     

Learning Contrast-Invariant Cancellation of Redundant Signals in Neural Systems

Cancellation of redundant information is a highly desirable feature of sensory systems, since it would potentially lead to a more efficient detection of novel information. However, biologically plausible mechanisms responsible for such selective cancellation, and especially those robust to realistic variations in the intensity of the redundant signals, are mostly unknown. In this work, we study, via in vivo experimental recordings and computational models, the behavior of a cerebellar-like circuit in the weakly electric fish which is known to perform cancellation of redundant stimuli. We experimentally observe contrast invariance in the cancellation of spatially and temporally redundant stimuli in such a system. Our model, which incorporates heterogeneously-delayed feedback, bursting dynamics and burst-induced STDP, is in agreement with our in vivo observations. In addition, the model gives insight on the activity of granule cells and parallel fibers involved in the feedback pathway, and provides a strong prediction on the parallel fiber potentiation time scale. Finally, our model predicts the existence of an optimal learning contrast around 15% contrast levels, which are commonly experienced by interacting fish.     

Effects of water conductivity on electrocommunication in the weak-electric fish Brienomyrus niger (Mormyriformes)

A characteristic electric organ discharge display in social encounters between mormyrid fish is a temporary discharge cessation. Using this response, we have investigated the useful range of electrocommunication under different water conductivity conditions in the mormyrid Brienomyrus niger. An individual fish was confined to a porous ceramic shelter tube and moved from a starting distance of 380 cm toward a similarly confined conspecific until discharge, cessation occurred. The moved fish was subsequently returned to its original, position. Water conductivity affects the peak-to-peak source voltage of the electric organ and the sensitivity of the fish's electroreceptors. Within a range of 10 to 36 000 μS/cm, the peak-to-peak amplitude of the electric organ discharge declined as a power function. At 120 μS/cm, the amplitude was 50%, and at 300μS/cm, 30% of the 10 μS/cm value. The interfish distance at which discharge cessation occurred and the associated electric field gradients were dependent on water conductivity and upon the spatial orientation of the two fish (end-to-end or parallel orientations of their shelter tubes). The respective ranges were from 135 cm and 0.02 mV/cm at 52 μS/cm (parallel orientation) to 22 cm and 0.36 mV/cm at 678 μS/cm (end-to-end orientation). When the data for both tube orientations were combined, the relationship between water conductivity (x) and the distance at which discharge cessation occurred (y) could be expressed by a power function, y=K·x^a (with K=10^2.97 and a=?0.56). When an electrically ‘silent’ fish was moved away from its conspecific, a discharge resumption in the form of a high-frequency rebound occasionally effected changes in the other fish's discharge activity at distances up to 157 cm (with an associated electric, field gradient of 0.01 mV/cm under the lowest conductivity condition).     

Aggressive behaviour and dominance relationships of the dark chub,Zacco temmincki with special reference to their individual recognition

Aggressive behaviour and dominance relationships ofZacco temmincki were observed by introducing fish into an enclosed pond. Chase (-flee), lateral display, parallel swim and butt were the principal behavioural patterns in aggressive encounters between fish, while chase, resulting in lateral display by the chased fish was the most common behavioural sequence. Initially, mutual behavioural patterns such as parallel swim and mutual lateral display were most evident among the total aggressive acts although chase became dominant three days after introduction into the pond. The dominance matrix constructed from chase-flee interactions during all observation periods contained many reverse attacks (336 out of 2,740 chases). These reverse attacks did not concentrate upon a specific period and were not site-dependent. Examination of chase-flee interactions and the subsequent behavioural pattern revealed that a chased fish reacted to the chaser either by attacking in turn, or performing lateral display etc. roughly in relation to the dominance rank of the chaser. This result implies that fish recognized each other to a great extent during aggressive encounters. It seems likely that such individual recognition was initiated during the early period when mutual behaviour was most frequent, and that some attacks against the dominance order were caused as a result of revolts rather than mistakes.     

Cutaneous electrical oscillation in a weakly electric fish, Gymnarchus niloticus

An African electric fish, Gymnarchus niloticus. ceases its electric organ discharge for a prolonged time in response to external electrical signals. During the cessation of electric organ discharges from the electric organ, a weak sinusoidal signal (approximately 0.1 mV cm(-1)) near the fish's previous discharge frequency was recorded near the body. The oscillatory potentials at all points on the body surface were synchronized and had a complex spatial distribution. The source of the potential was determined to be within the dermal tissue. Electroreceptive central neurons that responded to a moving target near the fish with normal electric organ discharges also responded to the same target when the electric organ discharge was interrupted and the potential from the skin existed. This result suggests that the fish may be able to electrolocate objects without the discharge from the electric organ.     

Body shape vs. colour associated initial divergence in the Telmatherina radiation in Lake Matano, Sulawesi, Indonesia

Highly polymorphic colouration patterns are often associated with sexual selection in fish and can be the initial cause of divergence among closely related taxa. Here we use genetic, body colour and geometric morphometric data collected on 118 fish from Lake Matano, Sulawesi, Indonesia to test if colouration is the initial cause of divergence in the radiating Telmatherina genus. Results reveal that all Telmatherina previously described in this system can be categorized into three mitochondrial lineages and that colouration is only weakly associated with early divergence. Clade-specific body shapes, however, likely adapted to microenvironments are key to the initial divergence in this system. Data also show that although colourations were not likely instrumental in seeding divergence in these fish, they appear to have developed in parallel within each clade. Our results are consistent with an emerging pattern repeated in many vertebrate radiations, whereby divergence by colouration or other display traits is preceded by specialization to environmental adaptive peaks.     

The responses of peripheral and central mechanosensory lateral line units of weakly electric fish to moving objects

Mechanosensory lateral line afferents of weakly electric fish (Eigenmannia) responded to an object which moved parallel to the long axis of the fish with phases of increased spike activity separated by phases of below spontaneous activity. Responses increased with object speed but finally may show saturation. At increasingly greater distances the responses decayed as a power function of distance. For different object velocities the exponents (mean±SD) describing this response falloff were -0.71±0.4 (20 cm/s object velocity) and-1.9±1.25 (10 cm/s). Opposite directions of object movement may cause an inversion of the main features of the response histograms. In terms of peak spike rate or total number of spikes elicited, however, primary lateral line afferents were not directionally sensitive.Central (midbrain) lateral line units of weakly electric fish (Apteronotus) showed a jittery response if an object moved by. In midbrain mechanosensory lateral line, ampullary, and tuberous units the response to a rostral-tocaudal object movement may be different from that elicited by a caudal-to-rostral object motion. Central units of Apteronotus may receive input from two or more sensory modalities. Units may be lateral line-tuberous or lateral line-ampullary. Multimodal lateral line units were OR units, i.e., the units were reliably driven by a unimodal stimulus of either modality. The receptive fields of central units demonstrate a weak somatotopic organization of lateral line input: anterior body areas project to rostral midbrain, posterior body areas project to caudal midbrain.Abbreviation EOD electric organ discharge     

Long-term Behavioral Tracking of Freely Swimming Weakly Electric Fish

Long-term behavioral tracking can capture and quantify natural animal behaviors, including those occurring infrequently. Behaviors such as exploration and social interactions can be best studied by observing unrestrained, freely behaving animals. Weakly electric fish (WEF) display readily observable exploratory and social behaviors by emitting electric organ discharge (EOD). Here, we describe three effective techniques to synchronously measure the EOD, body position, and posture of a free-swimming WEF for an extended period of time. First, we describe the construction of an experimental tank inside of an isolation chamber designed to block external sources of sensory stimuli such as light, sound, and vibration. The aquarium was partitioned to accommodate four test specimens, and automated gates remotely control the animals'' access to the central arena. Second, we describe a precise and reliable real-time EOD timing measurement method from freely swimming WEF. Signal distortions caused by the animal''s body movements are corrected by spatial averaging and temporal processing stages. Third, we describe an underwater near-infrared imaging setup to observe unperturbed nocturnal animal behaviors. Infrared light pulses were used to synchronize the timing between the video and the physiological signal over a long recording duration. Our automated tracking software measures the animal''s body position and posture reliably in an aquatic scene. In combination, these techniques enable long term observation of spontaneous behavior of freely swimming weakly electric fish in a reliable and precise manner. We believe our method can be similarly applied to the study of other aquatic animals by relating their physiological signals with exploratory or social behaviors.     

Selective infection of E. coli as a function of a specific molecular interaction

Selective infection of phage is when the bacterial infection depends on the specific molecular interaction between an antigen and a phage-displayed protein sequence such as an antibody. Engineering of the normal infection into pathways, directed by a specific protein--protein interaction, has raised several mechanistic questions. Here, we address the type of display and the affinity between the interacting pairs. The deleted phage R408d3 was used for the first time in selective infection and was shown to exhibit a superior performance compared to the VCSM13 phage. Furthermore, the affinity between the interacting pairs also affected the selective infection process and a correlation between affinity and infection efficiency was detected, thus implying that selective infection is the method of choice for selection of rare high-affinity interactions in molecular libraries.     

Electric signalling and reproductive behaviour in a mormyrid fish, the bulldog Marcusenius macrolepidotus (South African form)

Bulldog fish (Marcusenius macrolepidotus) generate short (<1 ms) electric-organ discharges (EODs), separated by much longer and highly variable interdischarge intervals (IDIs). We observed overt behaviour and electrical activity during reproductive behaviour in a male and in a female bulldog, and identified IDI patterns with putative signal functions. In contrast to Pollimyrus adspersus and Pollimyrus isidori, in which an elaborate and extended courtship precedes spawning proper, our fish started spawning almost immediately when we allowed the female to enter the males territory. The male did not construct a nest, and neither parent provided parental care. The male showed very little aggression towards the intruding female. Fish spawned in bouts near the males hiding place, and eggs were scattered by the females vigorous tail flips as she left the spawning site, only to return shortly thereafter. During spawning bouts, both fish generated highly stereotyped IDI patterns: the male generated a series of IDIs gradually decreasing from about 200 ms to about 55 ms that was abruptly terminated by a long IDI. The female generated a series of relatively regular IDIs (about 54 ms) that was followed by a marked increase in IDI duration (the probable time of spawning). Finally, a sharp decrease in IDIs to about 20 ms accompanied the females sudden escape from the spawning site. In between spawning bouts, both fish generated series of very short IDIs (high discharge rate, HD) that alternated abruptly with very low-rate inter-HD activity (especially in the male). IDIs as short as 9 ms (male) or 11 ms (female) occurred during HD displays. No visible aggression, in fact very little overt behaviour, occurred during these HD displays in both fish. Agonistic interactions between male and female, outside a reproductive context, were similar to those previously described in male pairs, including overt behavioural patterns such as parallel swimming, antiparallel display and attack, as well as HD displays. When not interacting, fish did not generate HD displays. We suggest the HD display is a communication signal in both reproductive and agonistic contexts.     

‘Communication’ in weakly electric fish, Gnathonemus petersii (Mormyridae) II. Interaction of electric organ discharge activities of two fish

The electric organ discharges (EODs) of pairs of weakly electric fish, Gnathonemus petersii, were simultaneously recorded to study the significance of the EODs as communication signals. In a 400-litre tank a larger fish (12 to 15 cm) was passively moved within a shelter tube toward a smaller specimen (6 to 9 cm), either in steps or a continuous move. The movement was stopped at that distance when at least one fish significantly lowered or ceased its EOD activity. From this ‘threshold interfish distance’ the spatial range of a ‘communication field’ was found to extend about 30 cm from the fish. At threshold distances an EOD frequency increase caused a temporary EOD activity cessation in the second fish. The spontaneous irregular EOD pattern of the fish displaying the increased EOD rate changed into a regular one with almost equal time intervals between fish pulses.     

Body Condition in Male Betta splendens Does Not Predict Their Ability to Perform Opercular Displays Under Hypoxic Conditions

Many fish, including the fighting fish Betta splendens , perform a display in which the opercula are extended away from the head and gills. Previous work has shown that opercular display rates by male B. splendens decrease under conditions of reduced dissolved oxygen (hypoxia). We tested the hypothesis that the ability to maintain opercular display rates under hypoxic conditions is related to body condition in male B. splendens . We also tested the hypothesis that females would show a greater preference for males performing this display under hypoxic conditions, when the display should be a more reliable indicator of male phenotypic quality. We found no evidence to support either hypothesis. Male opercular display rate in hypoxic conditions was unrelated to natural or experimentally induced variation in body condition. Female B. splendens showed no differential preference for the opercular display, assessed through the use of computer animated male stimuli, in either acute or chronic hypoxia. We conclude that the presence of an air-breathing organ in this species makes the opercular display an unreliable signal of male quality as measured by body condition.     

Lateralization of lateral displays in convict cichlids

We examine lateralization of lateral displays in convict cichlids, Amatitlania nigrofasciata, and show a population level preference for showing the right side. This enables contesting pairs of fish to align in a head-to-tail posture, facilitating other activities. We found individuals spent a shorter mean time in each left compared with each right lateral display. This lateralization could lead to contesting pairs using a convention to align in a predictable head-to-tail arrangement to facilitate the assessment of fighting ability. It has major implications for the common use of mirror images to study fish aggression, because the 'opponent' would never cooperate and would consistently show the incorrect side when the real fish shows the correct side. With the mirror, the 'normal' head-to-tail orientation cannot be achieved.     

An integrative model of evolutionary covariance: a symposium on body shape in fishes

A major direction of current and future biological research is to understand how multiple, interacting functional systems coordinate in producing a body that works. This understanding is complicated by the fact that organisms need to work well in multiple environments, with both predictable and unpredictable environmental perturbations. Furthermore, organismal design reflects a history of past environments and not a plan for future environments. How complex, interacting functional systems evolve, then, is a truly grand challenge. In accepting the challenge, an integrative model of evolutionary covariance is developed. The model combines quantitative genetics, functional morphology/physiology, and functional ecology. The model is used to convene scientists ranging from geneticists, to physiologists, to ecologists, to engineers to facilitate the emergence of body shape in fishes as a model system for understanding how complex, interacting functional systems develop and evolve. Body shape of fish is a complex morphology that (1) results from many developmental paths and (2) functions in many different behaviors. Understanding the coordination and evolution of the many paths from genes to body shape, body shape to function, and function to a working fish body in a dynamic environment is now possible given new technologies from genetics to engineering and new theoretical models that integrate the different levels of biological organization (from genes to ecology).     

Electric Imaging through Evolution,a Modeling Study of Commonalities and Differences

Modeling the electric field and images in electric fish contributes to a better understanding of the pre-receptor conditioning of electric images. Although the boundary element method has been very successful for calculating images and fields, complex electric organ discharges pose a challenge for active electroreception modeling. We have previously developed a direct method for calculating electric images which takes into account the structure and physiology of the electric organ as well as the geometry and resistivity of fish tissues. The present article reports a general application of our simulator for studying electric images in electric fish with heterogeneous, extended electric organs. We studied three species of Gymnotiformes, including both wave-type (Apteronotus albifrons) and pulse-type (Gymnotus obscurus and Gymnotus coropinae) fish, with electric organs of different complexity. The results are compared with the African (Gnathonemus petersii) and American (Gymnotus omarorum) electric fish studied previously. We address the following issues: 1) how to calculate equivalent source distributions based on experimental measurements, 2) how the complexity of the electric organ discharge determines the features of the electric field and 3) how the basal field determines the characteristics of electric images. Our findings allow us to generalize the hypothesis (previously posed for G. omarorum) in which the perioral region and the rest of the body play different sensory roles. While the “electrosensory fovea” appears suitable for exploring objects in detail, the rest of the body is likened to a “peripheral retina” for detecting the presence and movement of surrounding objects. We discuss the commonalities and differences between species. Compared to African species, American electric fish show a weaker field. This feature, derived from the complexity of distributed electric organs, may endow Gymnotiformes with the ability to emit site-specific signals to be detected in the short range by a conspecific and the possibility to evolve predator avoidance strategies.     

Theoretical analysis of pre-receptor image conditioning in weakly electric fish

Electroreceptive fish detect nearby objects by processing the information contained in the pattern of electric currents through the skin. The distribution of local transepidermal voltage or current density on the sensory surface of the fish's skin is the electric image of the surrounding environment. This article reports a model study of the quantitative effect of the conductance of the internal tissues and the skin on electric image generation in Gnathonemus petersii (Günther 1862). Using realistic modelling, we calculated the electric image of a metal object on a simulated fish having different combinations of internal tissues and skin conductances. An object perturbs an electric field as if it were a distribution of electric sources. The equivalent distribution of electric sources is referred to as an object's imprimence. The high conductivity of the fish body lowers the load resistance of a given object's imprimence, increasing the electric image. It also funnels the current generated by the electric organ in such a way that the field and the imprimence of objects in the vicinity of the rostral electric fovea are enhanced. Regarding skin conductance, our results show that the actual value is in the optimal range for transcutaneous voltage modulation by nearby objects. This result suggests that "voltage" is the answer to the long-standing question as to whether current or voltage is the effective stimulus for electroreceptors. Our analysis shows that the fish body should be conceived as an object that interacts with nearby objects, conditioning the electric image. The concept of imprimence can be extended to other sensory systems, facilitating the identification of features common to different perceptual systems.