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

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

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

Sense and Sensitivity: Spatial Structure of conspecific signals during social interaction

Organisms rely on sensory systems to gather information about their environment. Localizing the source of a signal is key in guiding the behavior of the animal successfully. Localization mechanisms must cope with the challenges of representing the spatial information of weak, noisy signals. In this dissertation, I investigate the spatial dynamics of natural stimuli and explore how the electrosensory system of weakly electric fish encodes these realistic spatial signals. To do so In Chapter 2, I develop a model that examines the strength of the signal as it reaches the sensory array and simulates the responses of the receptors. The results demonstrate that beyond distances of 20 cm, the signal strength is only a fraction of the self-generated signal, often measuring less than a few percent. Chapter 2 also focuses on modeling a heterogeneous population of receptors to gain insights into the encoding of the spatial signal perceived by the fish. The findings reveal a significant decrease in signal detection beyond 40 cm, with a corresponding decrease in localization accuracy at 30 cm. Additionally, I investigate the impact of receptor density differences between the front and back on both signal detection and resolution accuracy. In Chapter 3, I analyze distinct movement patterns observed during agonistic encounters and their correlation with the estimated range of receptor sensitivity. Furthermore, I uncover that these agonistic interactions follow a classical pattern of cumulative assessment of competitors\u27 abilities. The outcome of this research is a comprehensive understanding of the spatial dynamics of social interactions and how this information is captured by the sensory system. Moreover, the research contributed to the development of a range of tools and models that will play crucial roles in future investigations of sensory processing within this system

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