Electric Fishes of the Genus Sternarchorhynchus
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Zoological Journal of the Linnean Society, 2010, 159, 223–371. With 77 figures Electric fishes of the genus Sternarchorhynchus (Teleostei, Ostariophysi, Gymnotiformes); phylogenetic and revisionary studies CARLOS DAVID DE SANTANA† and RICHARD P. VARI FLS* Division of Fishes, Department of Vertebrate Zoology, MRC-159, National Museum of Natural History, PO Box 37012, Smithsonian Institution, Washington, D.C. 20013-7012, USA Received 6 May 2008; accepted for publication 6 March 2009 Analysis of 88 characters of external and internal body systems yielded a phylogenetic reconstruction of the Neotropical electric knifefish genus Sternarchorhynchus (Apteronotidae; Gymnotiformes). The results support a hypothesis of Sternarchorhynchus as the sister group to Platyurosternarchus. A series of synapomorphies, many involving major innovations of the neurocranium, jaws, suspensorium, and associated systems that permit an unusual mode of grasp-suction feeding, support the monophyly of both genera. Synapomorphies largely resolve relationships within Sternarchorhynchus with basal nodes strongly supported by characters pertinent to prey capture and initial processing of food items. These possible key innovations may provide Sternarchorhynchus with a competitive advantage over other clades of the Apteronotidae and account for the species diversity of the genus in Neotropical rivers. Adaptive radiation in Sternarchorhynchus was analysed. Habitat preference transitions repeatedly occurred in the genus between deep-river channel dwelling species and rheophilic species with preferences for higher energy setting including rapids and swift-flowing fluviatile settings. Twenty-two species of Sternarchorhynchus are described as new based on samples that originated in the smaller rivers draining into the Golfo de Paria, the Marowijne and Essequibo River basins, the Río Orinoco and in particular the Amazon River basin. The 32 species in Sternarchorhynchus make it the most speciose genus in the Apteronotidae. No claim to original US government works. Journal compilation © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 223–371. doi: 10.1111/j.1096-3642.2009.00588.x ADDITIONAL KEYWORDS: adaptive radiation – Apteronotidae – cladistics – convergence – key innovation – new species – osteology – South America. INTRODUCTION through the rivers of the Guianas (Planquette, Keith & Le Bail, 1996; Meunier, 2004) and the Amazon Electric knifefishes of the genus Sternarchorhynchus basin (Goulding, Leal Carvalho & Ferreira, 1988; are tube-snouted, elongate, distinctly laterally com- Cox-Fernandes, 1999) to the upper Rio Paraná in the pressed fishes with a broad range in many Atlantic Río de La Plata basin (Britski, Silimon & Lopes, 1999; drainages of South America. Sternarchorhynchus Campos-da-Paz, 2000). The genus is unknown from ranges from the Río Orinoco basin in Venezuela and the trans-Andean and Caribbean versant portions of Colombia (Mojica, 1999; Lasso et al., 2004a, b) south South America, the rivers of north-eastern and south- eastern Brazil that drain directly into the Atlantic Ocean, all portions of the Río de La Plata basin *Corresponding author. E-mail: [email protected] †Current address: Programa de Pós-graduação em Genética. exclusive of the upper Rio Paraná system, and the Conservação e Biologia Evolutiva, Instituto Nacional de entirety of the southern reaches of the continent. Pesquisas da Amazônia, Av. André Araújo, 2936 Manaus, Sternarchorhynchus species are moderate-sized AM, 69060-001, Brazil; and Laboratório de Fisiologia predators (150 to 540 mm maximum total length) of Comportamental e Evolutiva, Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo, 2936 Manaus, benthic invertebrates (Goulding et al., 1988; Marrero AM, 69060-001, Brazil. & Taphorn, 1991). Their electrogenic abilities No claim to original US government works. 223 Journal compilation © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 159, 223–371 224 C. D. DE SANTANA and R. P. VARI facilitate the location and capture of prey in soft mud Cox-Fernandes et al., 2002). Although these elabora- and within the interstices between leaf litter and tions of the lower jaw and associated dentition occur other detritus (Marrero & Winemiller, 1993; Cramp- only in mature males, they are absent in some con- ton & Albert, 2006). Similarly they hunt for and specific males of comparable body sizes with well- capture aquatic insects, especially of the Chironomi- developed testes. Presence versus absence of these dae, Ephemeroptera, and Trichpotera, in small spaces modifications potentially reflects a social hierarchy in the river bottom and the tunnels and spaces in wherein the jaw and dentition elaborations are compacted clay nodules (Marrero, 1987; Marrero, limited to alpha males. Alternatively, variability in Castillo & Machado-Allison, 1987; Marrero & Wine- the expression of these features may reflect season- miller, 1993). Correlated modifications of the bones, ality in the manifestation of the modifications of the musculature, and other soft tissues of the jaws, and lower jaw and associated dentition. suspensorium in the highly restructured, tube-like As in other gymnotiforms, the species of Sternar- snouts, and anterior portions of the neurocranium chorhynchus generate and receive weak electrical allow extraction of prey items from these constricted signals that function in electrocommunication and refuges (Aguilera, 1986). These restructurings permit electrolocation. Electrocommunication serves to what has been termed ‘grasp-suction’ or ‘suction signal species identity and aspects of behaviour, assisted by mechanical grasping’. Morphological whereas electrolocation permits the detection of adaptations permitting this highly specialized feeding organisms and objects in the surrounding aquatic mode are unique to Sternarchorhynchus and the system via distortions of the electric field generated African mormyriform genus Campylomormyrus by the individual [see Carr & Maler, 1986 and Albert amongst orders of fishes entirely restricted to fresh- & Crampton (2005) for discussions of the adaptations waters (Marrero & Winemiller, 1993; Winemiller & associated with these functions]. Members of Sterna- Adite, 1997). rchorhynchus generate at least four types of electric A diversity of secondary sexually dimorphic fea- organ discharges (EODs). These periodic (wave-type) tures characterize genera in the Apteronotidae, with signals are interspecifically variable with discharges these modifications most prominent in the morphol- ranging between 944 and 1922 Hz and considerable ogy of the snout and jaws (Cox-Fernandes, 1998). overlap in distance ranges between congeners Amongst these are the hypermorphic growth of the (Crampton & Albert, 2006: 688–689, figs 23.10–11). snout in males of some species of Apteronotus (Cox- Some Sternarchorhynchus species have a unique Fernandes, Lundberg & Riginos, 2002; Albert & EOD modulation pattern (active phase coupling) pos- Crampton, 2009) and the elaboration of the anterior sibly associated with information exchange between portion of the jaws and dentition in Sternarchogiton potential mates (Langner & Scheich, 1978; (de Santana & Crampton, 2007). Many species of Gottschalk & Scheich, 1979); however, the degree to Sternarchorhynchus are characterized by secondary which these unusual EOD patterns are universal sexual dimorphism of multiple body systems. Non- across the genus is unknown. cephalic sexually dimorphic features of some species Species of Sternarchorhynchus dwell in diverse of Sternarchorhynchus involve pigmentation and habitats, with many members of the genus resident in more often the location of the anus and urogenital the deep-water benthos of the larger rivers. In these pore. More dramatic are the sexually dimorphic habitats, the species of Sternarchorhynchus consti- attributes involving the snout and jaws. Mature tute a significant portion of the fish biomass (Lopez- males of Sternarchorhynchus mormyrus have a wider Rojas, Lundberg & Marsh, 1984; Lundberg et al., snout than conspecific females of comparable body 1987; Marrero & Taphorn, 1991). Jointly with other sizes, whereas the distinct fleshy dorsomedian ridge deep-water species of the Apteronotidae, they are on the snout is limited to the males of Sternarcho- preyed upon extensively by several catfish species of rhynchus kokraimoro. Some species in the genus dem- large body sizes (Marrero & Taphorn, 1991; Barbarino onstrate sexually dimorphic differences in the degree Duque & Winemiller, 2003). Some species of Sterna- of curvature of the elongate snout. Most striking of rchorhynchus are adapted for life in smaller rivers the sexually dimorphic features in Sternarchorhyn- and tributary streams where they often inhabit high- chus are the lengthened and transversely widened energy settings such as rapids and/or pools at the anterior portions of the dentaries in some larger base of waterfalls (e.g. Sternarchorhynchus severii, males of ten species. This expanded region is rounded Sternarchorhynchus caboclo; de Santana & Nogueira, in the transverse plane and dorsally forms a bulbous 2006: 90). structure crowned with a patch of variably enlarged Impoundments across the range of Sternarchorhyn- teeth. Such enlarged dentition may be brought into chus drowned many of the rapids and waterfalls that play by males in confrontations during breeding con- are preferred habitats for many species of the genus tests (Marrero & Taphorn, 1991; Kirschbaum, 1995;