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Behavioural Brain Research Species Differences in Group Size And Behavioural Brain Research 207 (2010) 368–376 Contents lists available at ScienceDirect Behavioural Brain Research journal homepage: www.elsevier.com/locate/bbr Research report Species differences in group size and electrosensory interference in weakly electric fishes: Implications for electrosensory processing a, b c d d a,c Sarah A. Stamper ∗, Erika Carrera-G , Eric W. Tan , Vincent Fugère , Rüdiger Krahe , Eric S. Fortune a Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD, USA b Pontificia Católica del Ecuador, Quito, Ecuador c Department of Neuroscience, Johns Hopkins University, Baltimore, MD, USA d Department of Biology, McGill University, Montreal, QC, Canada article info abstract Article history: In animals with active sensory systems, group size can have dramatic effects on the sensory information Received 13 August 2009 available to individuals. In “wave-type” weakly electric fishes there is a categorical difference in sensory Received in revised form 1 October 2009 processing between solitary fish and fish in groups: when conspecifics are within about 1 m of each other, Accepted 16 October 2009 the electric fields mix and produce interference patterns that are detected by electroreceptors on each Available online 27 October 2009 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 Keywords: the parameters of social signals in two genera of sympatric weakly electric fishes, Apteronotus and Electrotaxis Gymnotiformes Sternopygus, in natural habitats of the Napo River valley in Ecuador and in laboratory settings. Apterono- Electrosensory tus were most commonly found in pairs along the Napo River (47% of observations; maximum group Social behavior 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. © 2009 Elsevier B.V. All rights reserved. 1. Introduction modulate their social and sensing behaviors to avoid detrimental interference. Many animal species have evolved “active sensory” systems in In “wave-type” weakly electric fish, each individual continu- which individuals probe their environment with autogenous sig- ously produces a quasi-sinusoidal electric organ discharge (EOD) at nals [42]. These adaptations allow animals to exploit niches that a nearly constant frequency. When two or more individuals come would be difficult, or perhaps impossible, to use with passive sens- into close proximity, the electric fields interact and produce ampli- ing systems alone. However, these animals are subject to additional tude and phase modulations, collectively known as “beats” [24]. sources of sensory interference, particularly from the simultane- These beats occur at rates equal to the frequency difference (Df) ously generated signals of nearby conspecifics. Indeed there is often between the EOD signals of nearby fish: if one fish produces an a categorical difference in the sensory milieu between when indi- EOD of 700 Hz and a nearby fish one of 705 Hz, then the beat rate viduals are alone versus when they are in groups. The size and will be 5 Hz. The frequency of these beats is encoded in the patterns density of the groups and the specific properties of the signals being of activity of tuberous electroreceptors. Tuberous electroreceptors used by group members determine the sensory interference experi- are specialized organs in the skin of the fish that are tuned to enced by the animals. The question arises if and how these animals 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 oscil- latory brain activity at 5 Hz, and a 40 Hz beat rate induces activity Abbreviations: Df, frequency difference; EOD, electric organ discharge; JAR, jam- at 40 Hz. In some species, 5 Hz beat rates have profound deleteri- ming avoidance response. ous effects on electrolocation of objects [2,23,24] whereas 40 Hz ∗ Corresponding author at: 3400 North Charles Street, Baltimore, MD 21218, USA. Tel.: +1 410 516 7367; fax: +1 410 516 4478. beat rates may actually enhance certain features of electrosensory E-mail address: [email protected] (S.A. Stamper). perception [46]. 0166-4328/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.bbr.2009.10.023 S.A. Stamper et al. / Behavioural Brain Research 207 (2010) 368–376 369 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 light- ing [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 combi- nation 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 fre- quency, 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 lep- torhynchus the males produce the higher frequency EODs [22,33]. Therefore, low-frequency beats usually occur in same-sex group- ings 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 Eigenman- nia [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 natu- ralistic laboratory setting where fish grouping preferences were observed over several consecutive days. Finally, we conducted electrotaxis experiments in the laboratory to determine if elec- trosensory information alone may contribute to the observed group sizes. Fig. 1. (A) Map of Ecuador showing study site locations (red). Field recordings were 2. Materials and methods made over a three-year period in Sacha Lodge, Panacocha,˜ and Estación Yasuní. (B) A sonogram of a recording showing EOD frequency over time for three species of All of the procedures used in this work were approved by the institutional ani- electric fish: Apteronotus (green), Sternopygus (blue) and Eigenmannia (red). The fre- mal care and use committees of the Johns Hopkins University and McGill University quency range of each species is color-coded on the Y-axis (left). In this sample, there and follow the recommendations of Hitschfeld et al. [26]. Field studies were con- was one Sternopygus, three individual Eigenmannia, and one Apteronotus. The funda- ducted with approval of the Ministerio del Ambiente, the owners of Sacha Lodge, mental frequency (F) of each fish is indicated (arrow) as well as all visible harmonics and the Pontificia Universidad Católica del Ecuador. For laboratory studies, adult A. (H). (C) A Venn diagram showing the distribution of species across 819 samples that leptorhynchus, and Sternopygus macrurus were purchased from various commercial contained at least one Eigenmannia (E), Apteronotus (A) or Sternopygus (S). In many cases, multiple species of fish were present, including 77 samples where all three vendors and maintained at 25–29 ◦C in laboratory tanks. species of fish were present in the recording. The sizes of the regions of the Venn dia- gram are mathematical
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