Carl D. Hopkins

Electric Communication: Functions in the Social Behavior of Eigenmannia Virescens

Eigenmannia virescens was observed in aquaria in Guyana, South America, during the non-breeding and breeding seasons. Agonistic behavior was described and correlated with electrical activity. Variations in the electric discharges play important roles in agonistic behavior as displays given during attack and retreat. Although descriptions of sexual behavior are not complete, certain electrical signals also appear to be used in courtship. The role of electrical signals in agonistic behavior of Eigemnannia were studied by (1) an analysis of the behavior of fish in dominant and subordinate roles, (2) an analysis of the simultaneous occurrence of electrical displays and motor actions, (3) an analysis of preceding actions of one fish and following actions of the other fish, and (4) analysis of responses to artificial electrical stimuli. These studies indicate that at least three classes of electric signals are important in communication among Eigenmannia: the normal discharge, Interruptions, and Rises. The normal discharge. The normal discharge of Eigenmannia virescens is species-distinctive in the area where this study was conducted. Playback of recorded signals and presentation of sinusoidal electrical stimuli, indicates that the normal discharge particularly the fundamental frequency of the normal discharge (240 to 600 Hz)- is used in species recognition. Males and females overlap extensively in their discharge frequency, and males do not appear to distinguish the electric discharges of males from those of females. Interruptions. Interruptions are brief cessations of the electric discharge. They are most often 20 to 40 msec in duration during agonistic interactions whereas they are often 60 to 80 msec when given by males during interactions with females during the breeding season. Interruptions are usually given in bouts where a bout is any group of Interruptions separated by less than 1.5 seconds. Interruptions are given almost exclusively by dominant fish. They are given at the same time as Attacks, Threats, and No Action, but rarely during Retreat. Bouts with many Interruptions are more likely to be associated with Attacks, and less likely with No Action, than are bouts containing only a few Interruptions. Interruptions correlate with motivation to Attack, and the number of Interruptions in a bout correlates with the probability of attack. Interruptions in one fish are followed by Retreat and No Action in the other fish, thus they appear to be an effective threat display. Interruptions with long durations are given at high repetition rates by male Eigenmannia in the presence of females during the breeding season, thus they may play a role in courtship. Rises. A Rise is an increase in discharge frequency followed by a decrease to the resting frequency. Rises lasting less than two seconds (Short Rises) are often given by dominant fish in agonistic interactions, most often at the same time as Attacks or Threats. They are given rarely. Long Rises (longer than two seconds) are given predominantly by subordinate fish in agonistic interactions. They are given simultaneous with Retreat and No Action and are thus an indicator of submissive behavior. Long Rises in one fish are followed by Attacks, Threats, Approaches, and by No Action in the other. During the breeding season, females, in the presence of males, often give long series of frequency modulations of unknown significance.

Sex Differences in Electric Signaling in an Electric Fish

The electric discharge of Sternopygus macrurus is distinctly different from the discharges of ten sympatric species of electric fish in Guyana, South America. Sternopygus is the first known example of a fish with sexually different electric discharges. Males and females differ in the steady-state frequency of their discharges, and males produce variations in their discharge during courtship. Playback experiments demonstrate that species and sex differences in electric discharges have communicative significance.

AFLPs RESOLVE PHYLOGENY AND REVEAL MITOCHONDRIAL INTROGRESSION WITHIN A SPECIES FLOCK OF AFRICAN ELECTRIC FISH (MORMYROIDEA: TELEOSTEI)

Abstract Estimating species phylogeny from a single gene tree can be especially problematic for studies of species flocks in which diversification has been rapid. Here we compare a phylogenetic hypothesis derived from cytochrome b (cyt b) sequences with another based on amplified fragment length polymorphisms (AFLP) for 60 specimens of a monophyletic riverine species flock of mormyrid electric fishes collected in Gabon, west-central Africa. We analyze the aligned cyt b sequences by Wagner parsimony and AFLP data generated from 10 primer combinations using neighbor-joining from a Nei-Li distance matrix, Wagner parsimony, and Dollo parsimony. The different analysis methods yield AFLP tree topologies with few conflicting nodes. Recovered basal relationships in the group are similar between cyt b and AFLP analyses, but differ substantially at many of the more derived nodes. More of the clades recovered with the AFLP characters are consistent with the morphological characters used to designate operational taxonomic units in this group. These results support our hypothesis that the mitochondrial gene tree differs from the overall species phylogeny due at least in part to mitochondrial introgession among lineages. Mapping the two forms of electric organ found in this group onto the AFLP tree suggests that posteriorly innervated electrocytes with nonpenetrating stalks have independently evolved from anteriorly innervated, penetrating-stalk electrocytes at least three times.

Sexual signal evolution outpaces ecological divergence during electric fish species radiation.

Natural selection arising from resource competition and environmental heterogeneity can drive adaptive radiation. Ecological opportunity facilitates this process, resulting in rapid divergence of ecological traits in many celebrated radiations. In other cases, sexual selection is thought to fuel divergence in mating signals ahead of ecological divergence. Comparing divergence rates between naturally and sexually selected traits can offer insights into processes underlying species radiations, but to date such comparisons have been largely qualitative. Here, we quantitatively compare divergence rates for four traits in African mormyrid fishes, which use an electrical communication system with few extrinsic constraints on divergence. We demonstrate rapid signal evolution in the Paramormyrops species flock compared to divergence in morphology, size, and trophic ecology. This disparity in the tempo of trait evolution suggests that sexual selection is an important early driver of species radiation in these mormyrids. We also found slight divergence in ecological traits among closely related species, consistent with a supporting role for natural selection in Paramormyrops diversification. Our results highlight the potential for sexual selection to drive explosive signal divergence when innovations in communication open new opportunities in signal space, suggesting that opportunity can catalyze species radiations through sexual selection, as well as natural selection.

Evolution of electric communication channels of mormyrids

Summary1.Field studies in the Ivindo River district of Gabon, West Africa, yielded information on the ecology and the electric discharge characteristics of 23 species of mormyrid fishes. The electric organ discharge (EOD) acts as an electric signature that defines the properties of an electric communication and electrolocation channel. Correlations between the properties of this signature and the ecological and social conditions of the fish in their natural environment suggest that signature properties are under natural selection, much as are social communication displays.2.EOD duration is reduced in those species that aggregate in dense schools. Those with long-duration discharges are widely spaced in stream habitats. EOD waveforms are usually species-specific. EODs are highly divergent within some genera, but convergence to the same EOD pattern is also found among schooling species. Species producing monophasic EODs inhabit rivers rather than small streams. A river habitat is evenly represented by fish species with EODs at all frequencies in the available spectrum. Stream habitats are represented mainly by species with shortduration pulses that emphasize the high-frequency end of the available spectrum.

Evolutionary designs for electric signals and electroreceptors in gymnotoid fishes of Surinam

Summary1.Field collections of gymnotoid electric fish in coastal Surinam streams; 23 March–6 April, 1976, yielded 11 species belonging to two families (Rhamphichthyidae and Gymnotidae). Electric organ discharges (EODs) were recorded and power spectra were generated by Fourier analysis. Each species could be classified as either wave or pulse type. Although EODs varied from species to species, individuals had species-typical discharges. EODs appear to function in electrolocation and electric communication. Coexisting pulse fish diverged in either pulse spectrum or pulse repetition rate. Although each species showed ecological preferences for one habitat or another, no general correlation was found between EOD form and habitat type (Fig. 1).2.Three species of coexisting Hypopomus showed widely differing EOD durations. Peak spectral energies were nonoverlapping (Fig. 4a).3.Electrophysiologic studies of the electroreceptors in Hypopomus species revealed five types of electroreceptors. Two types of units appear to act as EOD filters, responding maximally to spectral frequencies characteristic of the peak power of the species-specific EOD (Fig. 7).4.Relationships between EOD rate and spectrum are discussed with reference to their roles in communication and in electrolocation. A theory for the evolution of EOD wave forms is presented (Fig. 9).

Acoustic communication in an electric fish, Pollimyrus isidori (Mormyridae)

SummaryIt has been known since von Frischs work in the 1930s that mormyrid electric fishes are quite sensitive to sound. We now describe a repertoire of natural sounds produced by the mormyrid,Pollimyrus isidori, during breeding and aggression; reception of communication sounds is probably a major function for mormyrid audition.1.In aquaria,Pollimyrus isidori produce ‘grunts’, ‘moans’, ‘growls’, ‘pops’ and ‘hoots’ at various phases during nesting, courtship, and territory defense.2.All five sounds are produced primarily at night. Territorial males produce grunts, moans and growls during courtship. Vocalizing is stimulated by the presence of a gravid female on the males territory and decreases with the onset of spawning. Hoots and pops are given during agonistic behavior.3.Grunts are bursts of acoustic pulses, stereotyped for an individual, with the potential as individual signatures.4.The electric organ is silent during grunts and moans and is discharged at a reduced rate during growls.5.The courtship and spawning ofPollimyrus isidori is described.

DISCOVERY AND PHYLOGENETIC ANALYSIS OF A RIVERINE SPECIES FLOCK OF AFRICAN ELECTRIC FISHES (MORMYRIDAE: TELEOSTEI)

Abstract The evolution of species‐specific mate recognition signals is of particular interest within speciose mono‐phyletic groups with restricted distributions (known as “species flocks”). However, the explosive nature of speciation in these clades makes difficult the reconstruction of their phylogenetic history. Here we describe a species flock of riverine mormyrid fishes from west‐central Africa in which electric signals may play a role in the reproductive isolation of sympatric species. In our recent field collections, totaling more than 1400 specimens from many localities, we recognize 38 forms that are distinct in their morphologies and electric organ discharge (EOD) characteristics. Of these 38, only four clearly correspond to described species. Here we treat these forms as operational taxonomic units (OTUs) in a phylogenetic analysis of cytochrome b sequence data from a sample of 86 specimens. We examined support in the molecular data for the monophyly of these 38 OTUs considered together, the monophyly of each phenotypically delimited OTU considered individually, and for relationships among OTUs congruent with those inferred from the distribution of morphological and EOD character states. Trees obtained by both maximum‐parsimony and maximum‐likelihood analyses, rooted with sequence data from outgroup taxa, provide evidence for the monophyly of these 38 OTUs with respect to other mormyrid fishes. The small genetic distances between many distinct forms suggest their recent divergence. However, in many instances the cytochrome b tree topology fails to support the monophyly of individual OTUs and close relationships between OTUs that are similar in morphology and EOD characteristics. In other cases, individuals from distinct OTUs share identical or nearly identical haplotypes. Close examination of these cases suggests that unnatural OTU definition is not the sole cause of this pattern, and we infer an incongruence between the mitochondrial gene tree and the organismal phylogeny caused by incomplete mitochondrial lineage sorting and/or introgression across forms. The apparently rapid diversification in this clade of riverine electric fishes and the problems associated with recovering a meaningful species‐level phylogeny from mitochondrial data parallel findings in other species flocks. Selection on EOD waveforms as mate recognition signals may be involved in the radiation of these fishes. This is the first description of a freshwater fish species flock from a riverine, as opposed to a lacustrine, environment.

Shifts in frequency tuning of electroreceptors in androgen-treated mormyrid fish

SummarySeveral species of mormyrid electric fish have a sex difference in the pulse waveform of their electric organ discharge (EOD). Field studies in Gabon, West Africa have shown for one such species,Brienomyrus brachyistius (triphasic), that the sexually mature male EOD differs in shape and is nearly twice the duration of the EODs of females and juveniles. Fourier analysis reveals that differences in EOD duration correlate with those in the EOD power spectrum which has a peak at 0.3 kHz in males and 1.3 kHz in females and juveniles. We find a corresponding sex difference in the frequency tuning of at least one class of electroreceptors known as Knollenorgans. The average ‘best’ or ‘characteristic’ frequency of Knollenorgans is lower in males compared to females and juveniles. This correlates with a lower peak in the power spectrum of the males pulse. When females are treated with gonadal androgens, their EODs increase 2–3 fold in duration, and the power spectra of their pulses are correspondingly lowered to match that of mature males. The average best frequency of Knollenorgans decreases by nearly 1 kHz which matches the downward shift of their EODs power spectrum.For a second species ofBrienomyrus (sp. 2) which is commercially imported from Nigeria, we have not detected a sex difference in the power spectrum or duration of the EOD. The power spectrum peaks at about 4.2 kHz in males, females, and juveniles. Androgens, however, do cause a coincident downward shift in the average peak of the EOD power spectrum (from 4.2 to 1.3 kHz) and the average best frequency of Knollenorgans (from 2.3 to 1.4 kHz).Specimens ofBrienomyrus (sp. 2) that have been electrically silenced by surgical means are tuned, on the average, only 0.2 kHz higher than control animals. Silenced animals that have been treated with androgens are tuned, on the average, 0.2 kHz below controls. The results suggest that electroreceptor tuning is only partially modifiable during androgen treatment if the electroreceptors arenot being stimulated by an external electrical stimulus, i.e. the animals own EOD. Since androgen treatment has a dramatic effect on receptor tuningonly in intact fish, it seems likely that retuning isnot due to a direct action of androgens on receptors, but rather due to the action of the principal electrical stimulus upon the receptors, i.e. the EOD. The implications of such results for the development of species and sex differences in electro-receptor tuning is discussed.

Androgen Correlates of Socially Induced Changes in the Electric Organ Discharge Waveform of a Mormyrid Fish

Weakly electric fish from the family Mormyridae produce pulsatile electric organ discharges (EODs) for use in communication. For many species, male EODs are seasonally longer in duration than those of females, and among males, there are also individual differences in EOD duration. While EOD elongation can be induced by the administration of exogenous androgens, androgen levels have never before been assessed under natural or seminatural conditions. By simulating the conditions occurring during the breeding season in the laboratory, we provide evidence of a sex difference in EOD duration as well as document levels of circulating androgens in males. In this study, we analyzed the nature of social influences on male EOD duration and plasma androgen levels in Brienomyrus brachyistius. Individual males, first housed with a single female and then placed into social groups consisting of three males and three females, showed status-dependent changes in EOD duration. Top-ranking males experienced a relatively large increase in EOD duration. Second-ranking males experienced a more modest increase, and low-ranking males experienced a decrease in EOD duration. These changes were paralleled by differences in circulating levels of plasma 11-ketotestosterone (11-KT), but not testosterone, suggesting that the changes in EOD duration may have been mediated by changes in plasma 11-KT levels. Thus, it appears that EOD duration is an accurate indicator of male status, which is under social and hormonal control.