Species differences in group size and electrosensory interference in weakly electric fishes: Implications for electrosensory processing

Abstract

In animals with active sensory systems, group size can have dramatic effects on the sensory information available to individuals. In “wave-type” weakly electric fishes there is a categorical difference in sensory processing between solitary fish and fish in groups: when conspecifics are within about 1 m of each other, the electric fields mix and produce interference patterns that are detected by electroreceptors on each individual. Neural circuits in these animals must therefore process two streams of information—salient signals from prey items and predators and social signals from nearby conspecifics. We investigated the parameters of social signals in two genera of sympatric weakly electric fishes, Apteronotus and Sternopygus, in natural habitats of the Napo River valley in Ecuador and in laboratory settings. Apteronotus were most commonly found in pairs along the Napo River (47% of observations; maximum group size 4) and produced electrosensory interference at rates of 20–300 Hz. In contrast, Sternopygus were alone in 80% of observations (maximum group size 2) in the same region of Ecuador. Similar patterns were observed in laboratory experiments: Apteronotus were in groups and preferentially approached conspecific-like signals in an electrotaxis experiment whereas Sternopygus tended to be solitary and did not approach conspecific-like electrosensory signals. These results demonstrate categorical differences in social electrosensory-related activation of central nervous system circuits that may be related to the evolution of the jamming avoidance response that is used in Apteronotus but not Sternopygus to increase the frequency of electrosensory interference patterns.

Introduction

Many animal species have evolved “active sensory” systems in which individuals probe their environment with autogenous signals [42]. These adaptations allow animals to exploit niches that would be difficult, or perhaps impossible, to use with passive sensing systems alone. However, these animals are subject to additional sources of sensory interference, particularly from the simultaneously generated signals of nearby conspecifics. Indeed there is often a categorical difference in the sensory milieu between when individuals are alone versus when they are in groups. The size and density of the groups and the specific properties of the signals being used by group members determine the sensory interference experienced by the animals. The question arises if and how these animals modulate their social and sensing behaviors to avoid detrimental interference.

In “wave-type” weakly electric fish, each individual continuously produces a quasi-sinusoidal electric organ discharge (EOD) at a nearly constant frequency. When two or more individuals come into close proximity, the electric fields interact and produce amplitude and phase modulations, collectively known as “beats” [24]. These beats occur at rates equal to the frequency difference (Df) between the EOD signals of nearby fish: if one fish produces an EOD of 700 Hz and a nearby fish one of 705 Hz, then the beat rate will be 5 Hz. The frequency of these beats is encoded in the patterns of activity of tuberous electroreceptors. Tuberous electroreceptors are specialized organs in the skin of the fish that are tuned to detect features of species-specific electric signals [24]. There is a direct relation between the beat rate and the patterns of resulting neural activity so that, for example, a 5 Hz beat rate induces oscillatory brain activity at 5 Hz, and a 40 Hz beat rate induces activity at 40 Hz. In some species, 5 Hz beat rates have profound deleterious effects on electrolocation of objects [2], [23], [24] whereas 40 Hz beat rates may actually enhance certain features of electrosensory perception [46].

These electrosensory beats only occur when fish are in groups of two or more individuals. Thus, social interactions between nearby fish determine the global pattern of electrosensory stimulation and brain activation that these fish experience. “Global” indicates that almost the entire receptor array is simultaneously stimulated, as is the case for the retina when there is a change in ambient lighting [7], [18]. In some genera, including Eigenmannia and Apteronotus, fish can change the frequency of their EOD depending on the beat rate. In this behavior, which is known as the jamming avoidance response (JAR), fish can change their electric signal frequency to avoid deleterious beat rates of less than 10 Hz [4], [5], [32]. The combination of social behavior and the JAR behavior largely determines the global electrosensory signals that these fish experience [18]. For Eigenmannia, fish in groups typically generate beat rates in the gamma frequency range, between 20 and 80 Hz [52].

The frequency range of the beat experienced by a fish depends largely on whether a nearby conspecific is of the same or of the opposite-sex, since males and females differ in EOD frequency, even though their frequency ranges usually overlap. In Sternopygus, and Apteronotus albifrons the males produce the lower-frequency EODs [15], [27], [28], [29], whereas in Apteronotus leptorhynchus the males produce the higher frequency EODs [22], [33]. Therefore, low-frequency beats usually occur in same-sex groupings and high-frequency beats occur in opposite-sex groupings in these species. Further, each genus exhibits distinct behavioral and neural solutions to electrosensory jamming by conspecifics. The JAR in Apteronotus appears to be simpler than in Eigenmannia [25], and Sternopygus do not exhibit JAR behaviors despite the presence of neural circuits similar to those in the other two genera [5], [39], [46]. Rather, Sternopygus has a specialized class of neurons in the electrosensory lateral line lobe (ELL) that appears to confer immunity to this sort of detrimental interference [37], [38].

Building on a previous study of group size and electrosensory interference in Eigenmannia [52], we set out to better understand the relations between social behavior, the JAR, and electrosensory processing. We examined the patterns of electrosensory signals produced by Apteronotus and Sternopygus in natural habitats (Napo River valley, Ecuador) and in laboratory experiments. First, we looked at the natural distribution of fish to determine group sizes, electric signal frequencies, and beat rates. We also used a naturalistic laboratory setting where fish grouping preferences were observed over several consecutive days. Finally, we conducted electrotaxis experiments in the laboratory to determine if electrosensory information alone may contribute to the observed group sizes.