Salience of multisensory feedback regulates behavioral variability

Many animal behaviors are robust to dramatic variations in morphophysiological features, both across and within individuals. The control strategies that animals use to achieve such robust behavioral performances are not known. Recent evidence suggests that animals rely on sensory feedback rather than precise tuning of neural controllers for robust control. Here we examine the structure of sensory feedback, including multisensory feedback, for robust control of animal behavior. We re-examined two recent datasets of refuge tracking responses of Eigenmannia virescens, a species of weakly electric fish. Eigenmannia rely on both the visual and electrosensory cues to track the position of a moving refuge. The datasets include experiments that varied the strength of visual and electrosensory signals. Our analyses show that increasing the salience (perceptibility) of visual or electrosensory signals resulted in more robust and precise behavioral responses. Further, we find that robust performance was enhanced by multisensory integration of simultaneous visual and electrosensory cues. These findings suggest that engineers may achieve better system performance by improving the salience of multisensory feedback rather than solely focusing on precisely tuned controllers.

Communication with self, friends and foes in active-sensing animals

ABSTRACT Animals that rely on electrolocation and echolocation for navigation and prey detection benefit from sensory systems that can operate in the dark, allowing them to exploit sensory niches with few competitors. Active sensing has been characterized as a highly specialized form of communication, whereby an echolocating or electrolocating animal serves as both the sender and receiver of sensory information. This characterization inspires a framework to explore the functions of sensory channels that communicate information with the self and with others. Overlapping communication functions create challenges for signal privacy and fidelity by leaving active-sensing animals vulnerable to eavesdropping, jamming and masking. Here, we present an overview of active-sensing systems used by weakly electric fish, bats and odontocetes, and consider their susceptibility to heterospecific and conspecific jamming signals and eavesdropping. Susceptibility to interference from signals produced by both conspecifics and prey animals reduces the fidelity of electrolocation and echolocation for prey capture and foraging. Likewise, active-sensing signals may be eavesdropped, increasing the risk of alerting prey to the threat of predation or the risk of predation to the sender, or drawing competition to productive foraging sites. The evolutionary success of electrolocating and echolocating animals suggests that they effectively counter the costs of active sensing through rich and diverse adaptive behaviors that allow them to mitigate the effects of competition for signal space and the exploitation of their signals.

The Use of Supervised Learning Models in Studying Agonistic Behavior and Communication in Weakly Electric Fish

Despite considerable advances, studying electrocommunication of weakly electric fish, particularly in pulse-type species, is challenging as very short signal epochs at variable intervals from a few hertz up to more than 100 Hz need to be assigned to individuals. In this study, we show that supervised learning approaches offer a promising tool to automate or semiautomate the workflow, and thereby allowing the analysis of much longer episodes of behavior in a reasonable amount of time. We provide a detailed workflow mainly based on open resource software. We demonstrate the usefulness by applying the approach to the analysis of dyadic interactions of Gnathonemus petersii. Coupling of the proposed methods with a boundary element modeling approach, we are thereby able to model the information gained and provided during agonistic encounters. The data indicate that the passive electrosensory input, in particular, provides sufficient information to localize a contender during the pre-contest phase, fish did not use or rely on the theoretically also available sensory information of the contest outcome-determining size difference between contenders before engaging in agonistic behavior.

Derived karyotypes in two elephantfish genera (Hyperopisus and Pollimyrus): lowest chromosome number in the family Mormyridae (Osteoglossiformes)

The African weakly electric elephantfish family Mormyridae comprises 22 genera and almost 230 species. Up-to-date cytogenetic information was available for 17 species representing 14 genera. Here we report chromosome number and morphology in Hyperopisus bebe (Lacepède, 1803) and Pollimyrus isidori (Valenciennes, 1847) collected from the White Nile system in southwestern Ethiopia. Both taxa displayed the diploid chromosome number 2n = 40, but they differed in fundamental numbers: FN = 66 in H. bebe and FN = 72 in P. isidori; previously the same diploid chromosome number 2n = 40 was reported in an undescribed species of Pollimyrus Taverne, 1971 (FN = 42) from the same region. Our results demonstrate that not only pericentric inversions, but fusions also played a substantial role in the evolution of the mormyrid karyotype structure. If the hypothesis that the karyotype structure with 2n = 50–52 and prevalence of the uni-armed chromosomes close to the ancestral condition for the family Mormyridae is correct, the most derived karyotype structures are found in the Mormyrus Linnaeus, 1758 species with 2n = 50 and the highest number of bi-armed elements in their compliments compared to all other mormyrids and in Pollimyrus isidori with the highest number of bi-armed elements among the mormyrids with 2n = 40.

Convergent mosaic brain evolution is associated with the evolution of novel electrosensory systems in teleost fishes

Brain region size generally scales allometrically with total brain size, but mosaic shifts in brain region size independent of brain size have been found in several lineages and may be related to the evolution of behavioral novelty. African weakly electric fishes (Mormyroidea) evolved a mosaically enlarged cerebellum and hindbrain, yet the relationship to their behaviorally novel electrosensory system remains unclear. We addressed this by studying South American weakly electric fishes (Gymnotiformes) and weakly electric catfishes (Synodontis spp.), which evolved varying aspects of electrosensory systems, independent of mormyroids. If the mormyroid mosaic increases are related to evolving an electrosensory system, we should find similar mosaic shifts in gymnotiforms and Synodontis. Using micro-computed tomography scans, we quantified brain region scaling for multiple electrogenic, electroreceptive, and non-electrosensing species. We found mosaic increases in cerebellum in all three electrogenic lineages relative to non-electric lineages and mosaic increases in torus semicircularis and hindbrain associated with the evolution of electrogenesis and electroreceptor type. These results show that evolving novel electrosensory systems is repeatedly and independently associated with changes in the sizes of individual brain regions independent of brain size, which suggests that selection can impact structural brain composition to favor specific regions involved in novel behaviors.

Electric signal synchronization as a behavioural strategy to generate social attention in small groups of mormyrid weakly electric fish and a mobile fish robot

African weakly electric fish communicate at night by constantly emitting and perceiving brief electrical signals (electric organ discharges, EOD) at variable inter-discharge intervals (IDI). While the waveform of single EODs contains information about the sender’s identity, the variable IDI patterns convey information about its current motivational and behavioural state. Pairs of fish can synchronize their EODs to each other via echo responses, and we have previously formulated a ‘social attention hypothesis’ stating that fish use echo responses to address specific individuals and establish brief dyadic communication frameworks within a group. Here, we employed a mobile fish robot to investigate the behaviour of small groups of up to four Mormyrus rume and characterized the social situations during which synchronizations occurred. An EOD-emitting robot reliably evoked social following behaviour, which was strongest in smaller groups and declined with increasing group size. We did not find significant differences in motor behaviour of M. rume with either an interactive playback (echo response) or a random control playback by the robot. Still, the robot reliably elicited mutual synchronizations with other fish. Synchronizations mostly occurred during relatively close social interactions, usually when the fish that initiated synchronization approached either the robot or another fish from a distance. The results support our social attention hypothesis and suggest that electric signal synchronization might facilitate the exchange of social information during a wide range of social behaviours from aggressive territorial displays to shoaling and even cooperative hunting in some mormyrids.