Status Signaling and the Characterization of a Chirp-Like Signal in the Weakly Electric Fish \u3cem\u3eSteatogenys elegans\u3c/em\u3e

Sensory systems are critical to both exploratory and communicatory processes, the study of which is critical to our understanding of how animals perceive and respond to their environments. In weakly electric fishes the electrosensory system is utilized for both of these purposes. One type of communication, status signaling, is widespread across taxa and frequently hormonally modulated. This hormonal modulation keeps the signal honest, wherein the status of the sender and the production of the status signal itself are both hormone dependent. We investigated exploratory and communicatory strategies of the electromotor system in pulse-type gymnotiforms, with a focus on status communication in Steatogenys elegans and its hormonal modulation. S. elegans sometimes responds with brief increases in electric organ discharge rate coupled with decreases in amplitude when presented with interfering playback stimuli. This response is similar to the chirp electric organ discharge (EOD) modulation in other weakly electric fish species. Our initial work catalogued exploratory electromotor behavior in S. elegans along with three other pulse-type gymnotiforms (Hypopygus cf. lepturus, Microsternarchus bilineatus, & Brachyhypopomus sp.), with the aim of determining the electromotor repertoires of these species under solitary conditions without experimental stimulation. We then characterized the chirp in S. elegans to determine its structure and the context in which it is produced. Finally, we implanted S. elegans subjects with dihydrotestosterone (DHT) and monitored changes in chirp propensity and characteristics, in an effort to determine if the chirp is hormonally modulated. In our exploratory behavior investigations, all species exhibited faster EOD rates with a smaller range of frequencies during night (active) periods than day (quiescent) periods. Pacemaker stability did not appear to vary throughout the day, but all species except Brachyhypopomus sp. showed more rate variability at night than during the day. All species displayed stereotyped short-term EOD behaviors such as frequency rises, yet the chirp differs from these other behaviors in its rapid and large frequency increase with an equally rapid return to baseline rate, its decrease in EOD amplitude, and its short duration of just a few pulses as compared to other short-term EOD behaviors which last 10s to 100s of pulses with more gradual changes in frequency. We found that the chirp is most readily produced in response to interfering playback stimuli, and that DHT implanted subjects produced more chirps and produced them in response to a broader range of playback stimuli. Additionally, their chirps were modulated in such a way that their frequency, duration, and amplitude characteristics were exaggerated. The chirp in S. elegans appears to be similar to the chirp in other weakly electric fish species, may serve as a hormonally dependent honest communicatory signal, and is a promising model system for investigations into status communications and their hormonal control

A JAR of Chirps: The Gymnotiform Chirp Can Function as Both a Communication Signal and a Jamming Avoidance Response

The weakly electric gymnotiform fish produce a rhythmic electric organ discharge (EOD) used for communication and active electrolocation. The EOD frequency is entrained to a medullary pacemaker nucleus. During communication and exploration, this rate can be modulated by a pre-pacemaker network, resulting in specific patterns of rate modulation, including stereotyped communication signals and dynamic interactions with conspecifics known as a Jamming Avoidance Response (JAR). One well-known stereotyped signal is the chirp, a brief upward frequency sweep usually lasting less than 500 ms. The abrupt change in frequency has dramatic effects on phase precession between two signalers. We report here on chirping in Brachyhypopmus cf. sullivani, Microsternarchus cf. bilineatus Lineage C, and Steatogenys cf. elegans during conspecific playback experiments. Microsternarchus also exhibits two behaviors that include chirp-like extreme frequency modulations, EOD interruptions with hushing silence and tumultuous rises, and these are described in terms of receiver impact. These behaviors all have substantial impact on interference caused by conspecifics and may be a component of the JAR in some species. Chirps are widely used in electronic communications systems, sonar, and other man-made active sensing systems. The brevity of the chirp, and the phase disruption it causes, makes chirps effective as attention-grabbing or readiness signals. This conforms to the varied assigned functions across gymnotiforms, including pre-combat aggressive or submissive signals or during courtship and mating. The specific behavioral contexts of chirp expression vary across species, but the physical structure of the chirp makes it extremely salient to conspecifics. Chirps may be expected in a wide range of behavioral contexts where their function depends on being noticeable and salient. Further, in pulse gymnotiforms, the chirp is well structured to comprise a robust jamming signal to a conspecific receiver if specifically timed to the receiver’s EOD cycle. Microsternarchus and Steatogenys exploit this feature and include chirps in dynamic jamming avoidance behaviors. This may be an evolutionary re-use of a circuitry for a specific signal in another context. © Copyright © 2019 Field, Petersen, Alves-Gomes and Braun

Reproductive Character Displacement And Signal Ontogeny In A Sympatric Assemblage Of Electric Fish

Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/86991/1/j.1558-5646.2011.01245.x.pd

Vasotocin Actions on Electric Behavior: Interspecific, Seasonal, and Social Context-Dependent Differences

Social behavior diversity is correlated with distinctively distributed patterns of a conserved brain network, which depend on the action of neuroendocrine messengers that integrate extrinsic and intrinsic cues. Arginine vasotocin (AVT) is a key integrator underlying differences in behavior across vertebrate taxa. Weakly electric fish use their electric organ discharges (EODs) as social behavioral displays. We examined the effect of AVT on EOD rate in two species of Gymnotiformes with different social strategies: Gymnotus omarorum, territorial and highly aggressive, and Brachyhypopomus gauderio, gregarious and aggressive only between breeding males. AVT induced a long-lasting and progressive increase of EOD rate in isolated B. gauderio, partially blocked by the V1a AVT receptor antagonist (Manning compound, MC), and had no effects in G. omarorum. AVT also induced a long-lasting increase in the firing rate (prevented by MC) of the isolated medullary pacemaker nucleus (PN) of B. gauderio when tested in an in vitro preparation, indicating that the PN is the direct effector of AVT actions. AVT is involved in the seasonal, social context-dependent nocturnal increase of EOD rate that has been recently described in B. gauderio to play a role in mate selection. AVT produced the additional nocturnal increase of EOD rate in non-breeding males, whereas MC blocked it in breeding males. Also, AVT induced a larger EOD rate increase in reproductive dyads than in agonistic encounters. We demonstrated interspecific, seasonal, and context-dependent actions of AVT on the PN that contribute to the understanding of the mechanisms the brain uses to shape sociality

The Effect of male-male competition and its Underlying Regulatory Mechanisms on the Electric Signal of the Gymnotiform fish \u3cem\u3eBrachyhypopomus gauderio\u3c/em\u3e

Sexually-selected communication signals can be used by competing males to settle contests without incurring the costs of fighting. The ability to dynamically regulate the signal in a context-dependent manner can further minimize the costs of male aggressive interactions. Such is the case in the gymnotiform fish Brachyhypopomus gauderio, which, by coupling its electric organ discharge (EOD) waveform to endocrine systems with circadian, seasonal, and behavioral drivers, can regulate its signal to derive the greatest reproductive benefit. My dissertation research examined the functional role of the EOD plasticity observed in male B. gauderio and the physiological mechanisms that regulate the enhanced male EOD. To evaluate whether social competition drives the EOD changes observed during male-male interactions, I manipulated the number of males in breeding groups to create conditions that exemplified low and high competition and measured their EOD and steroid hormone levels. My results showed that social competition drives the enhancement of the EOD amplitude of male B. gauderio. In addition, changes in the EOD of males due to changes in their social environment were paralleled by changes in the levels of androgens and cortisol. I also examined the relationship between body size asymmetry, EOD waveform parameters, and aggressive physical behaviors during male-male interactions in B. gauderio, in order to understand more fully the role of EOD waveforms as reliable signals. While body size was the best determinant of dominance in male B. gauderio, EOD amplitude reliably predicted body condition, a composite of length and weight, for fish in good body condition. To further characterize the mechanisms underlying the relationship between male-male interactions and EOD plasticity, I identified the expression of the serotonin receptor 1A, a key player in the regulation of aggressive behavior, in the brains of B. gauderio. I also identified putative regulatory regions in this receptor in B. gauderio and other teleost fish, highlighting the presence of additional plasticity. In conclusion, male-male competition seems to be a strong selective driver in the evolution of the male EOD plasticity in B. gauderio via the regulatory control of steroid hormones and the serotonergic system

Dynamics of sensorimotor behavior in electrolocation and electrocommunication

Pedraja F. Dynamics of sensorimotor behavior in electrolocation and electrocommunication. Bielefeld: Universität Bielefeld; 2019.How are external sensory stimuli perceived, integrated and represented within the central nervous system? How does the nervous system generate appropriate behavioral responses based on this input and how does this behavior affect perception? The above questions have in common that they view sensory input and motor control as two sides of the sensorimotor loop. In this closed-loop system, actions inevitably generate sensory flow that can serve to organize behavior. To look, to smell, to touch, etc. are perceptual acts that depend on the interaction, coordination and interpretation of motor and sensory information through neural mechanisms. Active sensory systems are particularly amenable to the study of the reciprocal relations of motor and sensory components, as parts of closed loop control structures. A notable advantage of these sensory systems is the experimental accessibility of their sensory input, both in terms of its measurement and in terms of detailed modeling reconstructions of the input. In the case of weakly electric fish studied in this thesis, the animals sense and process environmental perturbations of a self-generated electric field. The fact that this field serves as the carrier of sensory information and at the same time is controlled by the animal, enables to precisely determine aspects of sensing that are often hard to obtain or quantify in sensory systems that do not actively generate the carrier: where, when and what an animal samples. Drawing on these benefits, my thesis focuses on the role of motor and electromotor behavior in sensorimotor integration. For this, a biophysical model for the active and passive electroreception was combined with physiological recordings and behavioral approaches. The central topics addressed are: (i) Object detection and sensorimotor learning. The sensory information obtained by the African species Gnathonemus petersii while learning a detection task was computationally reconstructed using boundary element methods (BEM). This revealed that the improved task performance was paralleled by an enhancement of the quality of the sensory information, which was mediated by changes of the electromotor patterns. The versatile manner in which the fish changed the spatial and temporal allocation of otherwise stable motor components not only improved the quality of the sensory input, but also resulted in shifts of the animals' attention towards the object. (ii) Dynamic choice of optimal behavior. Extending on the above results, I next explored how changing the distance of an object to be detected by the fish influenced the electromotor behavior. With increasing complexity (distance), the fish resorted to a new motor strategy. This consisted in first approaching a salient element in the arena, from where the fish then made a perceptually-guided decision. This interpretation is backed up by analyzing the trajectories in the context of attractors, revealing that the focus of attention was altered in a task-dependent manner. (iii) Distance estimation using a non-visual form of motion parallax. In the above experiments it is implicitly assumed that electric fish acquire spatial information like the position and distance of a target. How this is achieved dynamically has been addressed recently. Based on the properties of the electric field geometry, theoretical considerations indicated that relative movements might provide depth information. In a behavioral assay, I show that this novel form of electric parallax exists and is used across phylogenetically distant taxa of weakly electric fish (Apteronotus albifrons, Eigenmania virescens and Gnathonemus petersii). Notably, these species electrically sample the environment in temporally distinct ways (using discrete pulses or quasi-sinusoidal waves), suggesting an ubiquitous role for parallax in electric sensing. (iv) The role of multi-modal integration in socially relevant agonistic behaviour. Extending on the above results, I next addressed if passive as well as active electric sensory information can be used to evaluate more complex features of the environment. For this I turned to social interactions of the South American species Gymnotus omarorum to study if an electrical assessment of a competitor is possible. Based on modeling the sensory consequences of dyadic encounters, I showed that passive as well as active sensory information can drive agonistic interactions. This suggests that aggressive interactions may be triggered by information about contenders obtained through the active and passive electrosensory system. (v) Hierarchy as a social consequence of electric interactions. The above analysis indicated that active as well as passive electrolocation may contribute in a non-reciprocal manner to social interactions. Gymnotus omarorum then was tested in intra- and intersexual dyads in small plain arenas. A sex-independent dominant-subordinate status emerged after highly aggressive contests. Subordinates signaled their submission by retreating and emitting specific (submissive) electric signals. The emergence of a dominant-subordinate status was also observed in a larger arena after longer but milder contests with rare electric signaling of submission with a unique consequence: the persistence of dominance over time with no outcome reversion

Animal-Robot Interactions: Electrocommunication, Sensory Ecology, and Group Dynamics in a Mormyrid Weakly Electric Fish

Mormyrid weakly electric fish possess a specialized electrosensory system. During the process of active electrolocation, these animals perceive self-generated electric organ dis-charges (EOD) and are thereby able to detect objects in their nearby environment. The EOD is a short, biphasic pulse, which is simultaneously used to communicate with conspe-cifics. There are two principles according to which information exchange occurs during electrocommunication. The waveform of the EOD constitutes a relatively stable identity marker that signals species, gender, and status of an individual. In contrast, the temporal sequence of inter-discharge intervals (IDI) is highly variable and encodes context-specific information. Modifications of IDI-duration not only alter the instantaneous discharge fre-quency but also enable the generation of specific signaling patterns and interactive dis-charge sequences. One such interactive discharge behavior is the so-called echo response, during which a fish responds with a constant latency of only a few milliseconds to the EOD of a conspecific. Animals can synchronize their signaling sequences by mutually generating echoes to each other's signals over a coherent period. Although active electrolocation and electrocommunication are mediated by different types of electroreceptor organs and neural pathways, an unambiguous assignment of electromotor behavior to only one of the two functions is often problematic. In this thesis, the significance of IDI-based signaling sequences during motor and electro-motor interactions of the mormyrid fish Mormyrus rume proboscirostris were investigated. To this end, different electrical playback sequences of species-specific EODs were generated via mobile fish dummies, and the motor and electromotor responses of live fish were analyzed. In Part One of this thesis, electrocommunication strategies of the fish were analyzed, and particularly the functions of double pulses, discharge regularizations, and echo responses were examined in an adaptive context. Double pulses were classified as an aggressive mo-tivation signal, whereas regularizations may have a communicative function during the early stages of the sequential assessment of a potential opponent. In this context, discharge synchronization by means of echo responses may enable a mutual assessment for the net benefit of both contestants. Because echo responses occur in various behavioral contexts, and artificial echoes of the dummy evoked increased echoing by the fish, it was hypothesized that the echo response serves a more general purpose by enabling mutual allocation of social attention between two fish. In Part Two of this thesis, a biomimetic robotic fish was designed to investigate the senso-ry basis on which fish followed the dummy. It was shown that electrical playback signals induced following-behavior in live fish, whereas biomimetic motility patterns had no ef-fect. By subsequently reducing the mobile dummy to only the electric signaling sequence from the perspective of the fish, it could be shown that passive perception of electrical communication signals is also involved in mediating the spatial coordination of social in-teractions. This passive perception is likely mediated by the same electroreceptor organs that are used during electrocommunication. The EOD can therefore be considered to be an essential social stimulus that makes it possible to integrate a dummy into a group of weak-ly electric fish as an artificial conspecific. The influence of an interactively signaling mobile dummy fish on small groups of up to four individuals was investigated in Part Three of this thesis. Typical schooling behavior was a rare occurrence in this context. However, EOD-synchronizations through mutual echo responses between two fish, or between a fish and the interactive dummy, were fre-quently observed during social interactions in small groups. Motor interactions during synchronization episodes supported the hypothesis that mormyrids may use discharge synchronizations between individuals to allocate social attention, and the echo response may thus adopt a particularly useful function during communication in groups.Schwach elektrische Fisch aus der Familie der Mormyriden verfügen über ein spezialisier-tes elektrosensorisches Sinnessystem. In einem Prozess, der als aktive Elektroortung be-zeichnet wird, sind diese Tiere in der Lage, selbstgenerierte elektrische Organentladungen (EOD) wahrzunehmen, und dadurch Objekte in ihrer unmittelbaren Nähe zu detektieren. Das EOD ist ein kurzer bipolarer Puls, der gleichzeitig auch zur Kommunikation mit Artge-nossen dient. Informationsaustausch während der Elektrokommunikation basiert auf zwei verschiedenen Prinzipien: Die Wellenform des EOD stellt einen relativ konstanten Identi-tätsmarker dar, der beispielsweise Art, Geschlecht und Status eines Individuums signali-siert. Die zeitliche Abfolge der Intervalle zwischen den EODs ist hingegen höchst variabel und kodiert kontextspezifische Information. Durch Modifikation der Intervalldauer ändert sich nicht nur die Entladungsfrequenz, sondern es können auch spezifische Signalmuster und interaktive Entladungssequenzen generiert werden. Ein interaktives Entladungsver-halten stellt beispielsweise die Echoantwort dar, bei der ein Fisch mit einer konstanten Latenz von wenigen Millisekunden auf das EOD eines Artgenossen reagiert. Zwei Tiere können ihre Entladungssequenzen synchronisieren, indem sie ihre Signale über einen kohärenten Zeitraum gegenseitig mit Echos beantworten. Obwohl aktive Elektroortung und Elektrokommunikation über unterschiedliche Rezeptororgansysteme und neuronale Pfade vermittelt werden, ist eine eindeutige Zuordnung der elektromotorischen Verhal-tensäußerungen der Fische zu nur einer der beiden Funktionen oft problematisch. In der vorliegenden Arbeit wurde die Bedeutung intervallbasierter EOD-Sequenzen für motorische und elektromotorische Interaktionen des Mormyriden Mormyrus rume proboscirostris erforscht. Hierzu wurden verschiedene elektrische Playbacksequenzen artspezifischer EODs generiert und durch mobile Fischattrappen wiedergegeben. Die mo-torischen und elektromotorischen Verhaltensreaktionen der Fische wurden analysiert. Im ersten Teil der Arbeit wurden Elektrokommunikationsstrategien der Fische analysiert und die adaptive Funktion insbesondere von Doppelpulsen, Entladungsregularisierungen und Echoantworten untersucht. Doppelpulse wurden als aggressives Motivationssignal kategorisiert, wohingegen die Kommunikationsfunktion von Regularisierungen im gegen-seitigen Einschätzen zu Beginn einer kompetitiven Begegnung zu liegen scheint. Entla-dungssynchronisation durch gegenseitige Echoantworten kann dabei eine Einschätzung des Gegenübers zum Vorteil beider Parteien erleichtern. Da Echoantworten in verschiede-nen Verhaltenssituationen auftreten und artifizielle Echoantworten der Attrappe vermehrt zu Echos vonseiten der Fische führten, wurde postuliert, dass die Echoantwort eine generellere Funktion bei der Fokussierung gegenseitiger sozialer Aufmerksamkeit über-nehmen kann. Im zweiten Teil der Arbeit wurde ein biomimetischer Fischroboter konstruiert, um zu untersuchen, auf welcher sensorischen Grundlage die Fische der Attrappe folgen. Es konnte gezeigt werden, dass elektrische Playbacksignale, nicht aber biomimetische Bewe-gungsmuster, Folgeverhalten der Fische induzieren. In einem weiteren Schritt konnte durch die Reduktion der Attrappe auf die elektrischen Signalsequenzen aus der Perspektive der Versuchsfische gezeigt werden, dass passive Wahrnehmung elektrischer Kommu-nikationssignale auch bei der räumlichen Koordination sozialer Interaktionen von Bedeu-tung ist. Dies wird mutmaßlich über die gleichen Rezeptororgane vermittelt, die auch für die Elektrokommunikation verantwortlich sind. Das EOD kann daher als ein soziales Signal betrachtet werden, das es ermöglicht, eine Attrappe als künstlichen Artgenossen in eine Gruppe schwach elektrischer Fische zu integrieren. Der Einfluss einer elektrisch interaktiven mobilen Fischattrappe auf kleine Gruppen von bis zu vier Individuen wurde im dritten Teil der Arbeit getestet. Typisches Schwarmver-halten konnte in diesem Zusammenhang nur selten beobachtet werden. In kleinen Gruppen kam es während sozialer Interaktionen jedoch häufig zu EOD-Synchronisationen durch Echoantworten zwischen zwei Fischen, oder zwischen einem Fisch und der interaktiven Attrappe. Motorische Verhaltensinteraktionen im Zeitraum dieser Synchronisationen stützen die Hypothese, dass Mormyriden durch elektrische Entladungssynchronisation soziale Aufmerksamkeit zwischen Individuen herstellen können, und die Echoantwort somit besonders in Gruppen eine nützliche Kommunikationsfunktion übernehmen kann

Effects of Hypoxia on Swimming and Sensing in a Weakly Electric Fish

Low dissolved oxygen (hypoxia) can severely limit fish performance, especially aerobically expensive behaviours including swimming and acquisition of sensory information. Fishes can reduce oxygen requirements by altering these behaviours under hypoxia, but the underlying mechanisms can be difficult to quantify. We used a weakly electric fish as a model system to explore potential effects of hypoxia on swim performance and sensory information acquisition, which enabled us to non-invasively record electric signalling activity used for active acquisition of sensory information during swimming. To quantify potential effects of hypoxia, we measured critical swim speed (Ucrit) and concurrent electric signalling activity under highand low-dissolved oxygen concentrations in a hypoxia-tolerant African mormyrid fish, Marcusenius victoriae. Fish were maintained under normoxia for 6 months prior to experimental treatments, and then acclimated for 8 weeks to normoxia or hypoxia and tested under both conditions (acute: 4 h exposure). Acute hypoxia exposure resulted in a significant reduction in both Ucrit and electric signalling activity in fish not acclimated to hypoxia. However, individuals acclimated to chronic hypoxia were characterized by a higher Ucrit under both hypoxia and normoxia than fish acclimated to normoxia. Following a 6 month re-introduction to normoxia, hypoxia-acclimated individuals still showed increased performance under acute hypoxic test conditions, but not under normoxia. Our results highlight the detrimental effects of hypoxia on aerobic swim performance and sensory information acquisition, and the ability of fish to heighten aerobic performance through acclimation processes that can still influence performance even months after initial exposure