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Ostariophysi: Gymnotiformes: Electrophorus) The Untold Story of the Caudal Skeleton in the Electric Eel (Ostariophysi: Gymnotiformes: Electrophorus) Carlos David de Santana1,2*, Richard P. Vari1, Wolmar B. Wosiacki2 1 Division of Fishes, Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, D. C., United States of America, 2 Setor de Ictiologia, Museu Paraense Emilio Goeldi, Bele´m, Para´, Brazil Abstract Alternative hypotheses had been advanced as to the components forming the elongate fin coursing along the ventral margin of much of the body and tail from behind the abdominal region to the posterior margin of the tail in the Electric Eel, Electrophorus electricus. Although the original species description indicated that this fin was a composite of the caudal fin plus the elongate anal fin characteristic of other genera of the Gymnotiformes, subsequent researchers proposed that the posterior region of the fin was formed by the extension of the anal fin posteriorly to the tip of the tail, thereby forming a ‘‘false caudal fin.’’ Examination of ontogenetic series of the genus reveal that Electrophorus possesses a true caudal fin formed of a terminal centrum, hypural plate and a low number of caudal-fin rays. The confluence of the two fins is proposed as an additional autapomorphy for the genus. Under all alternative proposed hypotheses of relationships within the order Gymnotiformes, the presence of a caudal fin in Electrophorus optimized as being independent of the occurence of the morphologically equivalent structure in the Apteronotidae. Possible functional advantages to the presence of a caudal fin in the genus are discussed. Citation: de Santana CD, Vari RP, Wosiacki WB (2013) The Untold Story of the Caudal Skeleton in the Electric Eel (Ostariophysi: Gymnotiformes: Electrophorus). PLoS ONE 8(7): e68719. doi:10.1371/journal.pone.0068719 Editor: Jacob Engelmann, Universita¨t Bielefeld, Germany Received February 21, 2013; Accepted June 1, 2013; Published July 24, 2013 This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Funding: Funding for the research was provided to RPV and CDS by the Herbert R. and Evelyn Axelrod Chair in Systematic Ichthyology of the National Museum of Natural History, Smithsonian Institution, and to WBW by Conselho Nacional de Pesquisa (CNPq). CDS was supported by a Posdoctoral Fellowship from the CNPq/Cieˆncia sem Fronteiras (245622/2012-8). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction been the subject of study by physiologists and are well known in popular lore [11]. The order Gymnotiformes includes 33 genera and more than Electrophorus was erected by Gill [12] to include the Electric Eel, 200 extant species of Neotropical electric fishes plus one fossil Gymnotus electricus Linnaeus [13]. The description by Linneaus [13] form from the Late Miocene of Bolivia [1,2]. Gymnotiforms was based on what was for the period a very detailed account and inhabit freshwaters across the expanse from northern Argentina accompanying illustration by Gronovius [14] of a specimen to southern Mexico in settings ranging from shallow, slow- probably originating in Suriname. Ichthyofaunal sampling over flowing streams to deep rivers, with subsets of several families the following two and one-half centuries documented that specialized for life in rapids and other high energy settings [3–6]. Electrophorus has a broad distribution in low- and mid-elevation Species of gymnotiforms range in body size from miniatures of settings across the vast expanse encompassed by the Amazon and 50 mm total length such as Hypopygus minissimus [7] to the over Orinoco basins and additionally through the river systems of 2.5 m total length of Electrophorus electricus [8]; a 50 times range northern Brazil and the Guianas between the mouths of those two notable in itself, but particularly striking in a lineage of circa only major drainages [15,16]. 200 species. Various autapomorphies unique within the Ostariophysi Arguably one of the most noteworthy characteristics of all distinguish Electrophorus [17], with one of the most prominent gymnotiforms is their ability to produce electric organ discharges being the presence of three hypaxial electric organs (the Main, (EODs) which serve dual purposes - communication and Hunter and Sach organs) versus a single hypaxial organ in adults exploration of the surrounding environment. Two alternative of other gymnotiforms [1]. Electrophorus also has a highly forms of such discharges occur among these electric fishes: pulse vascularized oral respiratory organ with multiple folds that greatly EODs (via myogenic organs) and wave EODs (via myogenic or increase its surface area [1,9]; an elaboration unique to the genus neurogenic organs). Electrophorus is unique within the Gymnoti- among Neotropical electric fishes and critical for respiration in this formes in having a third form of discharge of up to 600 volts obligatory air breather. The Electric Eel, moreover, differs from all used for hunting and self-defense [9,10]. Such powerful other gymnotiforms in the elongate fin extending along the ventral discharges are dramatically apparent to anyone in contact with, surface of the body and tail from posterior of the abdominal cavity or in close proximity, to these fishes in the water during a to the end of tail (Fig. 1; [18]). Other gymnotiforms conversely discharge. These shocks were reported by naturalists commenc- have the lengthy anal fin terminating further anteriorly along the ing early in the European exploration of the Neotropics, have tail. PLOS ONE | www.plosone.org 1 July 2013 | Volume 8 | Issue 7 | e68719 Caudal Skeleton in the Electric Eel Figure 1. Lateral view of Electrophorus electricus, MPEG 25422, 1000 mm TL. Continuous compound fin along ventral surface of body and posteroventral portion of tail shown in upper figure and close up of compound anal-caudal fin at tip of tail in lower figure. doi:10.1371/journal.pone.0068719.g001 Alternative hypotheses have been advanced concerning the Results and Discussion components of the elongate fin coursing along the ventral surface of the body and tail of Electrophorus. Linnaeus [13] originally The Caudal Skeleton in Electrophorus postulated that the anal fin of Gymnotus electricus (the Electrophorus Well over two centuries ago, Linnaeus [13]: 427 commented electricus of this paper) was posteriorly continuous with the rays of that Gymnotus electricus had ‘‘Pinna caudali obtufiffima anali annexa’’ the caudal-fin, i.e., the caudal fin is present. Subsequent authors ( = the caudal fin very obtuse and joined to the anal). Information ascribed to the alternative concept of the absence of a caudal fin in in that account indicated that his statement was most likely derived the genus. Intriguingly, the details of the unusual tail along the from a detailed description and illustration of a specimen of the ventral and posterior margins of the body in Electrophorus have not species by Gronovius [14] rather than based on the examination of been the subject of analysis to evaluate the two alternative material of G. electricus. This concept of conjoined anal and caudal hypotheses – that the fin at the posterior of the tail is a true caudal fins in what was later termed Electrophorus electricus (hereafter fin versus that the terminal portion of the elongate fin in the genus Electrophorus) then vanished without comment from the scientific is a posterior extension of the anal fin to form a false caudal fin. literature for more than 200 years. The alternative accepted We herein address that question and evaluate the results within the scenario was that the anal fin extended posteriorly to the end of context of the divergent hypotheses of intraordinal phylogenetic tail in Electrophorus and formed what has been termed a false caudal relationships in the Gymnotiformes. fin [1,17,20–25]. An assumption that the terminal portion of the elongate fin in Electrophorus was a false, rather than true, caudal fin Materials and Methods may have been, in part, based on the absence of the caudal fin in Gymnotus, a genus showing a number of derived characters with Specimens were examined at, or borrowed from, the following Electrophorus, with those two genera now forming the Gymnotidae. institutions: AMNH, American Museum of Natural History, New Comments as to a possible contrary arrangement were limited to York; AUM, Auburn University Museum, Auburn; ANSP, remarks by Meunier & Kirschbaum [26,27]. Academy of Natural Sciences of Drexel University, Philadelphia; Meunier & Kirschbaum [26]: 216 briefly mentioned the FMNH, Field Museum of Natural History, Chicago; INHS, possible presence of a caudal fin in Electrophorus as an alternative Illinois Natural History Survey, Champaign; KU, University of to the prevailing concept of an elongate anal fin extending Kansas, Lawrence; MBUCV, Museo de Biologia de la Uni- posteriorly to the terminus of the tail. Soon thereafter Meunier & versidad Central de Venezuela, Caracas; MCZ, Museum of Kirschbaum [27]: 149 speculated again on the presence of a Comparative Zoology, Harvard University, Cambridge; MNRJ, caudal skeleton in the genus, stating that ‘‘…the last vertebra is Museu Nacional, Rio de Janeiro; MPEG, Museu Paraense terminated by a small cartilage, which serves to support some Emı´lio Goeldi, Bele´m; MZUSP, Museu de Zoologia da lepidotrichia.’’ That observation notwithstanding, those authors Universidade de Sa˜o Paulo, Sa˜o Paulo; UF, Florida Museum did not explicitly interpret the cartilaginous element in question as of Natural History, Gainesville; NRM, Swedish Museum of a caudal skeleton, perhaps due to the absence of an ontogenetic Natural History, Stockholm; and USNM, National Museum of series of the species. In so far as they commented on the presence Natural History, Smithsonian Institution, Washington.
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