Acessibilidade / Reportar erro

The brain of Brycon orbignyanus (Valenciennes, 1850) (Teleostei: Characiformes: Bryconidae): gross morphology and phylogenetic considerations

ABSTRACT

The brain of Brycon orbignyanus is described as a model for future studies of the gross morphology of the central nervous system in Characiformes. The study of brain gross morphology of 48 distinct taxa of Characiformes, one of Cypriniformes, two of Siluriformes and two of Gymnotiformes, allowed us to propose, for the first time, six putative brain synapomorphies for the Characiformes and also two possibly unique gross brain morphology characters for the Siluriformes. A detailed protocol for the extraction of the brain in Characiformes is also provided.

Keywords:
Comparative morphology; Encephalon; Ostariophysi; Otophysi; Putative synapomorphies

RESUMO

O encéfalo de Brycon orbignyanus é descrito como um modelo para futuros estudos da anatomia externa do Sistema Nervoso Central de Characiformes. O estudo da morfologia externa de 48 táxons distintos de Characiformes, um de Cypriniformes, dois de Siluriformes e dois de Gymnotiformes, permitiu-nos propor, pela primeira vez, seis prováveis sinapomorfias encefálicas e também duas possíveis características encefálicas para Siluriformes. Um protocolo detalhado para a dissecção e extração do encéfalo de Characiformes é também apresentado.

Introduction

During the last two centuries, diagnoses of fish taxa and hypotheses of their evolutionary relationships were almost exclusively based on osteological attributes (see Wiley & Johnson, 2010Wiley E. O. & G. D. Johnson. 2010. A teleost classification based on monophyletic groups. Pp. 123-182. In: Nelson J. S., H.-P. Schultze & M. V. H. Wilson (Eds.). Origin and phylogenetic interrelationships of teleosts. München, Verlag Dr. Friedrich Pfeil.; Datovo & Vari, 2014Datovo A. & R. P. Vari. 2014. The adductor mandibulae muscle complex in lower teleostean fishes (Osteichthyes: Actinopterygii): comparative anatomy, synonymy, and phylogenetic implications. Zoological Journal of the Linnean Society, 171: 554-622.). This extensive exploration of osteological features in bony fishes was really efficient in the delimitation of major Teleostei clades; notwithstanding, this almost exclusive focus on osteological features resulted in the "relatively minor attention" to other anatomical systems (Datovo & Vari, 2014Datovo A. & R. P. Vari. 2014. The adductor mandibulae muscle complex in lower teleostean fishes (Osteichthyes: Actinopterygii): comparative anatomy, synonymy, and phylogenetic implications. Zoological Journal of the Linnean Society, 171: 554-622.), and very few studies have even tried to describe and analyze other major anatomical systems in fishes, such as the neuroanatomy, which according to Datovo & Vari (2014Datovo A. & R. P. Vari. 2014. The adductor mandibulae muscle complex in lower teleostean fishes (Osteichthyes: Actinopterygii): comparative anatomy, synonymy, and phylogenetic implications. Zoological Journal of the Linnean Society, 171: 554-622.), based mostly on Wiley & Johnson (2010Wiley E. O. & G. D. Johnson. 2010. A teleost classification based on monophyletic groups. Pp. 123-182. In: Nelson J. S., H.-P. Schultze & M. V. H. Wilson (Eds.). Origin and phylogenetic interrelationships of teleosts. München, Verlag Dr. Friedrich Pfeil.), represents approximately 1% of the synapomorphies currently recognized for teleosteans fishes.

Studies of comparative brain anatomy of teleosts focusing on phylogenetic relationships are scarce, and the first to combine brain features and cladistic methods was Northcutt (1984Northcutt, R. G. 1984. Evolution of the vertebrate central nervous system: patterns and processes. American Zoologist, 24: 701-716., 1985Northcutt, R. G. 1985. Brain phylogeny: speculations on pattern and cause. Pp. 351-378. In:Cohen, M. J. & F. Strumwasser (Eds.). Comparative neurobiology: modes of communication in the nervous system. New York, Wiley.), who has shown that cladistics analytical tools could be used to find out the patterns resulting from the evolution of vertebrate brains (Abrahão & Pupo, 2014Abrahão, V. P. & F. M. R. S. Pupo. 2014. Técnica de dissecção do neurocrânio de Siluriformes para estudo do encéfalo. Boletim da Sociedade Brasileira de Ictiologia, 112: 21-26.; Striedter, 2005Striedter, G. F. 2005. Principles of brain evolution. Irvine, Sinauer Associates, 363p.). Previous to Northcutt's (1984Northcutt, R. G. 1984. Evolution of the vertebrate central nervous system: patterns and processes. American Zoologist, 24: 701-716., 1985Northcutt, R. G. 1985. Brain phylogeny: speculations on pattern and cause. Pp. 351-378. In:Cohen, M. J. & F. Strumwasser (Eds.). Comparative neurobiology: modes of communication in the nervous system. New York, Wiley.) publications, studies of fish brain anatomy were focused on the relationship between ecological attributes and brain gross morphology, or simple descriptions - either total or partial - of chondrichthyan and teleostean brains (Ewart, 1888Ewart, J. C. 1888. On the cranial nerves of Elasmobranch fishes: preliminary communication. Proceedings of the Royal Society of London, 45: 524-537.; Herrick, 1899Herrick, C. J. 1899. The cranial and first spinal nerves of Menidia , a contribution upon the nerves components of the bony fishes. Unpublished Ph.D. Dissertation, Archives of Neurology and Psychopathology, New York, 298p., 1901Herrick, C. J. 1901. The cranial nerves and cutaneous sense organs of the North American siluroid fishes. Journal of Comparative Neurology, 11: 177-249.; Evans, 1931Evans, H. M. 1931. A comparative study of the brains in British cyprinoids in relation to their habits of feeding, with special reference to the anatomy of the medulla oblongata. Proceedings of the Royal Society of London B, 757: 233-257., 1940Evans, H. M. 1940. Brain and body of fish: a study of brain pattern in relation to hunting and feeding in fish. Philadelphia, The Blakiston Company, 152p.; Miller & Evans, 1965Miller, R. J. & H. E. Evans. 1965. External morphology of the brain and lips in catostomid fishes. Copeia, 1965: 467-487.; Nieuwenhuys, 1967Nieuwenhuys, R. 1967. Comparative anatomy of the cerebellum. Pp. 1-93. In: Fox, C. A. & R. L. Snider (Eds.). The cerebellum. Progress in Brain Research . Amsterdam, Elsevier.).

Despite the scarcity of neuroanatomical features in phylogenetic analyses, a few neuroanatomical characters were found to be synapomorphic for some lineages of Teleostei. Some examples include the anterior brain position in relation to the cranial cavity in Gadiformes: Melanonoidei (Howes, 1993Howes, G. J. 1993. Anatomy of the Melanonidae (Teleostei: Gadiformes), with comments on its phylogenetic relationships. Bulletin of British Museum (Natural History), Zoology, 59: 11-31.); the olfactory sensory epithelium arranged in sensory islets and absence of the saccus vasculosus in the Cyprinodontiformes and Atheriniformes (Yamamoto, 1982Yamamoto, M. 1982. Comparative morphology of the peripheral olfactory organ in teleosts. Pp. 39-59. In: Hara, T. J. (Ed.). Chemoreception in fishes. Developments in Aquaculture and Fisheries Science. New York, Elsevier.; Parenti, 1993Parenti, L. R. 1993. Relationships of atherinomorph fishes (Teleostei). Bulletin of Marine Science, 52: 170-196., 2005Parenti, L. R. 2005. The phylogeny of atherinomorphs: evolution of a novel fish reproductive system. Pp. 13-30. In: Uribe, M. C. & H. J. Grier (Eds.). Viviparous fishes. Homstead, New Life Publication.); and the large dorsal telencephalon of the anterior portion of central nucleus and small medial portion, together with the absence of accessory optic tract and nucleus (except for the Sternopygidae), in addition to ampullary organs organized in rosettes in Gymnotiformes (Albert et al., 1998Albert, J. S., M. J. Lannoo & T. Turi. 1998. Testing hypotheses of neural evolution in gymnotiform electric fishes using phylogenetic character data. Evolution, 52: 1760-1780.; Wiley & Johnson, 2010Wiley E. O. & G. D. Johnson. 2010. A teleost classification based on monophyletic groups. Pp. 123-182. In: Nelson J. S., H.-P. Schultze & M. V. H. Wilson (Eds.). Origin and phylogenetic interrelationships of teleosts. München, Verlag Dr. Friedrich Pfeil.).

Characiformes contains approximately 2,100 valid living species, occurring mostly in the freshwaters of the Neotropical region (19 families) and less so in the African Sub-Saharan region of Africa (four families) (Reis et al., 2003Reis, R. E., S. O. Kullander & C. J. Ferraris (Eds.). 2003. Check list of the Freshwater fishes of South and Central America. Porto Alegre, Edipucrs , 729p.; Oliveira et al., 2011Oliveira, C., G. S. Avelino, K. T. Abe, T. C. Mariguela, R. C. Benine, G. Ortí, R. P. Vari & R. M. C. Castro. 2011. Phylogenetic relationships within the speciose family Characidae (Teleostei: Ostariophysi: Characiformes) based on multilocus analysis and extensive ingroup sampling. BMC Evolutionary Biology, 11: 1-25.). As with other teleostean groups, the clades within the Characiformes are diagnosed and have their evolutionary interrelationships hypothesized almost exclusively with osteological characters (Fink & Fink, 1981Fink, S. V. & W. L. Fink. 1981. Interrelationships of the ostariophysan fishes (Teleostei). Zoological Journal of Linnean Society, 72: 297-353., 1996Fink, S. V . & W. L. Fink. 1996. Interrelationships of the Ostariophysi. Pp. 209-249. In: Stiassny, M. L. J., L. R. Parenti & G. D. Johnson. Interrelationships of fishes. San Diego, Academic Press.). The great diversity of lifestyles found in Characiformes is most probably reflected in the organization of their central nervous system (see Nieuwenhuys et al., 1998Nieuwenhuys, R., H. J. ten Donkelaar & C. Nicholson (Eds.). 1998. The Central Nervous System of vertebrates. Berlin, Springer-Verlag, XL, 2214p.), thus, we hypothesize that the study of the brain gross morphology of characiforms can provide important insights into their biology, ecology, behavior, evolution and phylogenetic relationships, as pointed by Lisney & Collin (2006Lisney, T. J. & S. P. Collin. 2006. Brain morphology in large pelagic fishes: a comparison between sharks and teleosts. Journal of Fish Biology, 68: 532-554.) for the Animal Kingdom, and their diversity of brain morphologies as a whole.

Among the Otophysi (composed by the Orders Cypriniformes, Characiformes, Siluriformes and Gymnotiformes), the study of the brain gross morphology has recently been addressed for gymnotiforms (Albert et al., 1998Albert, J. S., M. J. Lannoo & T. Turi. 1998. Testing hypotheses of neural evolution in gymnotiform electric fishes using phylogenetic character data. Evolution, 52: 1760-1780.; Albert, 2001Albert, J. S. 2001. Species, diversity and phylogenetic systematics of American Knifefishes (Gymnotiformes, Teleostei). Miscellaneous Publications, Museum of Zoology, University of Michigan, 190: 1-129.), in addition to the siluriforms Callichthyidae and Pseudopimelodidae (Abrahão & Shibatta, 2015Abrahão, V. P . & O. A. Shibatta. 2015. Gross morphology of the brain of Pseudopimelodus bufonius (Valenciennes, 1840) (Siluriformes: Pseudopimelodidae). Neotropical Ichthyology, 13, 255-264.), the Callichthyidae which was the subject of a Master's dissertation (Pupo, 2011Pupo, F. M. R. S. 2011. Anatomia comparada da morfologia externa do sistema nervoso central da família Callichthyidae (Teleostei: Ostariophysi: Siluriformes) e suas implicações filogenéticas. Unpublished M. Sc. Dissertation. Universidade Federal do Rio de Janeiro, Rio de Janeiro, 97 p.) and the Characiformes studied in a Doctoral thesis (Pereira, 2014Pereira, T. N. A. 2014. Anatomia encefálica comparada de Characiformes (Teleostei: Ostariophysi). Unpublished Ph. D. Dissertation. Universidade de São Paulo, Ribeirão Preto, 279 p.), both unpublished at this moment. These Otophysi brain studies have unequivocally shown that the central nervous system can be an important source of phylogenetically informative morphological characters, although relatively unexplored. Bearing that in mind, we have chosen Brycon orbignyanus , a member of the putative generalized and phylogenetically basal family Bryconidae (Roberts, 1969Roberts, T. 1969. Osteology and relationships of characoid fishes, particularly the genera Hepsetus , Salminus , Hoplias , Ctenolucius, and Acestrorhynchus . Proceedings of the California Academy of Sciences, 36: 391-500.; Mirande, 2009Mirande, J. M. 2009. Weighted parsimony phylogeny of the family Characidae (Teleostei: Characiformes). Cladistics, 25: 574- 613., 2010Mirande, J. M. 2010. Phylogeny of the family Characidae (Teleostei: Characiformes): from characters to taxonomy. Neotropical Ichthyology, 8: 385-568.; Oliveira et al., 2011Oliveira, C., G. S. Avelino, K. T. Abe, T. C. Mariguela, R. C. Benine, G. Ortí, R. P. Vari & R. M. C. Castro. 2011. Phylogenetic relationships within the speciose family Characidae (Teleostei: Ostariophysi: Characiformes) based on multilocus analysis and extensive ingroup sampling. BMC Evolutionary Biology, 11: 1-25.), to be described as an example of a generalized Characiformes brain.

Material and Methods

Specimen preparation and brain dissection. The examined specimens belong to the following institution fish collections: LBP (Laboratório de Biologia e Genética de Peixes, Universidade Estadual Paulista "Júlio de Mesquita Filho"); LIRP (Laboratório de Ictiologia de Ribeirão Preto, Universidade de São Paulo); MZUSP (Museu de Zoologia da Universidade de São Paulo); and UNT (Laboratório de Sistemática Ictiológica da Universidade Federal do Tocantins). The complete list of examined specimens is summarized in Table 1.

Table 1
Material examined in the present study. Asterisk represents type species of genus; SL = Standard length; HL = Head length.

All specimens examined in the present study were adults to avoid the potentially confusing effects of developmental changes (Huber & Rylander, 1992Huber, R & M. K. Rylander. 1992. Brain morphology and turbidity preference in Notropis and related genera (Cyprinidae, Teleostei). Environmental Biology of Fishes, 33: 153-165.). Standard length (SL) and head length (HL) were taken point to point with digital calipers on the left side of the specimens. Specimens were stained following the musculature dissection technique proposed by Datovo & Bockmann (2010Datovo, A. & F. A. Bockmann. 2010. Dorsolateral head muscles of the catfish families Nematogenyidae and Trichomycteridae (Siluriformes: Loricarioidei): comparative anatomy and phylogenetic analysis. NeotropicalIchthyology,8: 193-246.), which allows a better visualization of cranial bones and its sutures in prepared specimens without any undesirable changes caused to their brains. The brains were then removed from the braincase using a protocol specifically developed and described below for bony fishes with laterally compressed skulls, like the characiforms.

Brain dissection protocol. To extract the brain of characiform fishes, the following dissection procedure was applied on both sides of the specimens heads:

To remove the lateral bones, branchial-basket and eyes, first scrape the epidermal layer (skin) on the opercle, orbital, facial, maxilla, premaxilla and dentary bones - scraping the epidermal layer (skin) and fat (e.g. Anostomoidea) of the neurocranium roof allows a better visualization of the cranial sutures. Remove the eyeball and associated musculature (Musculus rectus superior , Musculus rectus externus , Musculus rectus inferior , Musculus rectus internus , Musculus obliquus superior and Musculus obliquus inferior ), making a severing incision in the proximal region of eyeball muscles, as well as in the pedunculi bulbi (anterior portion of nervus opticus ). Cut free the maxillary, premaxillary and dentary bones. During the process, remove the anterior portion of the olfactory epithelium, located nearby the maxillary and premaxillary bones.

Remove the epaxial musculature located near the Weberian Apparatus and supraneural bones. Make an incision on the mid-posterior surface portion of the supraoccipital bone, and proceed to the first dorsal-fin ray removing the epaxial musculature until reaching the neural tube.

To completely disjoint and remove the cranial roof, first cut open the mesethmoid sutures with adjacent bones and remove it; then cut lengthwise the soft tissue of the frontal fontanel (the Erythrinidae and Lebiasinidae both have a completely ossified fontanel and thus bone will be cut instead of soft connective tissue); proceed backwards separating the paired parietal and supraoccipital bones, and then remove them totally. At this point the posterior portion of the brain corpus cerebelii and rhombencephalon should be visible. Cut free the pterotic and sphenotic bones, taking into account that both bones encase the lateral sides of the brain, making their inadequate removal prone to damage the brain. At the end of the aforementioned dissecting steps the brain should be almost completely exposed laterally and dorsally, and intact.

To completely extract the brain from the neurocranium, begin by making a severing incision on the posterior portion of medulla spinalis , posterior to the root the nervus vagus near and anterior to the vertical passing through the middle of the Weberian Apparatus and posterior to the imaginary line on the ventral surface of the insertion of the complex of the spino-occipitales nerves; the subsequent cuts of the cranial nerves must proceed in the following postero-anteriorly sequence, to avoid breaking inadvertently the anterior cranial nerves: sever the efferent (n. X) of lobus vagi ; the slim nervus abducens (n. VI) on the floor of the neurocranium; nerves from octavolateralis area (nervus trigeminus - n. V, nervus facialis - n. VII, nervus octavus - n. VIII, nervus linea lateralis anterior - nlla and nervus linea lateralis posterior - nllp); the nervus opticus (n. II) at the middle portion of the nervus passing through the floor of neurocranium where the chiasma opticum is located, and finally the nervus olfactorius (n. I). When the described procedure is complete, the brain should be completely free from the neurocranium.

Illustration and description. Brain illustrations were made using a pen tablet digital interface and image editing softwares applied to digital photographs made with a stereomicroscope and an attached digital camera. Colors in all illustrations are entirely arbitrary, not corresponding to the real colors of the anatomical structures illustrated. Brain descriptions were based on Meek & Nieuwenhuys (1998Nieuwenhuys, R., H. J. ten Donkelaar & C. Nicholson (Eds.). 1998. The Central Nervous System of vertebrates. Berlin, Springer-Verlag, XL, 2214p.) and Striedter (2005Striedter, G. F. 2005. Principles of brain evolution. Irvine, Sinauer Associates, 363p.), with a single modification: fish brains descriptions usually follow the posteroanterior direction (e.g. , Meek & Nieuwenhuys, 1998Meek, J. & R. Nieuwenhuys. 1998. Holosteans and teleosts Pp. 759-937. In:Nieuwenhuys, R., H. J. ten Donkelaar & C. Nicholson (Eds.). The central nervous system of vertebrates. Berlin, Springer-Verlag.), but herein we chose to follow Striedter (2005Striedter, G. F. 2005. Principles of brain evolution. Irvine, Sinauer Associates, 363p.) in adopting the anteroposterior direction, the most commonly used for vertebrates as a whole (see Bauchot et al., 1989Bauchot, R., J. Ridet & M. Bauchot. 1989. The brain organization of butterflyfishes. Environmental Biology of Fishes, 25: 205-219.; Striedter, 2005Striedter, G. F. 2005. Principles of brain evolution. Irvine, Sinauer Associates, 363p.; Eastman & Lannoo, 2007Eastman, J. T. & M. J. Lannoo. 2007. Brain and sense organ anatomy and histology of two species of phyletically basal non-Antarctic thornfishes of the Antarctic suborder Notothenioidei (Perciformes: Bovichtidae). Journal of Morphology, 268: 485-503., 2008Eastman, J. T . & M. J. Lannoo. 2008. Brain and sense organ anatomy and histology of the Falkland Islands mullet, Eleginops maclovinus (Eleginopidae), the sister group of the Antarctic notothenioid fishes (Perciformes: Notothenioidei). Journal of Morphology, 269: 84-103. for fishes; ten Donkelaar, 1998aten Donkelaar, H. J. 1998a. Anurans. Pp. 1151-1314. In: Nieuwenhuys, R., H. J. ten Donkelaar & C. Nicholson (Eds.). The central nervous system of vertebrates. Berlin, Springer-Verlag. for amphibians; ten Donkelaar, 1998bten Donkelaar, H. J. 1998b. Reptiles. Pp. 1315-1524. In: Nieuwenhuys, R., H. J. ten Donkelaar & C. Nicholson (Eds.). The central nervous system of vertebrates. Berlin, Springer-Verlag. for reptiles and Walsh & Milner, 2011Walsh, S. & A. Milner. 2011. Evolution of the avian brain and senses. Pp. 282-305. In: Dyke, G. & G. Kaiser. Living dinosaurs: The evolutionary history of modern birds. Chichester. John Wiley & Sons Publisher. for avians). For illustration and description purposes, the brains were divided into telencephalon , mesencephalon , diencephalon , rhombencephalon and medulla spinalis (Fig. 1).

The anatomical brain nomenclature follows Meek & Nieuwenhuys (1998Nieuwenhuys, R., H. J. ten Donkelaar & C. Nicholson (Eds.). 1998. The Central Nervous System of vertebrates. Berlin, Springer-Verlag, XL, 2214p.) and Striedter (2005Striedter, G. F. 2005. Principles of brain evolution. Irvine, Sinauer Associates, 363p.); bone nomenclature follows Weitzman (1962Weitzman, S. H. 1962. The osteology of Brycon meeki , a generalized characid fish, with an osteological definition of the family. Stanford Ichthyological Bulletin, 8: 1-77.), with the modifications proposed by Castro & Vari (2004Castro, R. M. C. & R. P. Vari. 2004. Detritivores of the South American fish family Prochilodontidae (Teleostei: Ostariophysi: Characiformes): a phylogenetic and revisionary study. Smithsonian Contributions to Zoology, 622: 1-189.) and musculature terminology follows Datovo & Vari (2013Datovo, A . & R. P. Vari. 2013. The jaw adductor muscle complex in teleostean fishes: evolution, homologies and revised nomenclature (Osteichthyes: Actinopterygii). PloS One, 8:4.; 2014Datovo A. & R. P. Vari. 2014. The adductor mandibulae muscle complex in lower teleostean fishes (Osteichthyes: Actinopterygii): comparative anatomy, synonymy, and phylogenetic implications. Zoological Journal of the Linnean Society, 171: 554-622.).

Fig. 1
Brain of Brycon orbignyanus (Characiformes: Bryconidae), LIRP 6309, 175.5 mm SL. Main encephalic divisons (Telencephalon , Diencephalon , Mesencephalon , Rhombencephalon + Medulla oblongata and Medulla spinalis ) in different colors. a. dorsal; b. lateral and c. ventral views.

Results

Brain gross morphology of Brycon orbignyanus (Figs. 1 and 2). The brain limits established for Brycon orbignyanus and also applied to other Characiformes examined in the present study are: the anterior portions of the bulbus olfactorius anteriorly, usually ending at the oval olfactory epithelium and the insertion of the complex of the spino -occipitales nerves on the ventral surface of the medulla spinalis , posteriorly. The encephalon is slightly elongate and narrow; slightly wider in its middle portion near the mesencephalon (tectum opticus ) and diencephalon . The brain occupies the cranial cavity almost entirely, from the region near the mesethmoid and lateral ethmoid to the region anterior to the third neural arch, not contacting the Weberian apparatus.

Fig. 2
Brain of Brycon orbignyanus (Characiformes: Bryconidae), LIRP 6309, 175.5 mm SL. a. dorsal; b. lateral and c. ventral views. Apt = Area postrema; Bol = bulbus olfactorius; Ch = chiasma opticum; Cocb = corpus cerebelli; Dien = diencephalon; Eg = eminentia granularis; Hyp = hypophysis; Hyt = hypothalamus; Lih = lobus inferior hypothalami; LobX = lobus vagi; Mo = medulla oblongata; Ms = medulla spinalis; Pob = nervus tractus olfactorius; Sv = saccus vasculosus; Tect = tectum opticum;; Telen = Telencephalon Tl = Torus lateralis; Tv = tela ventriculi; Cranial Nerves: nI = nervus olfactorius; nII = nervus opticus; nIII = nervus oculomotorius; nIV = nervus trochlearis; nV = nervus trigeminus; nVI = nervus abducens; nVII = nervus fascialis; nVIII = nervus octavus; nLLa = nervus lineae lateralis anterior; nLLp = nervus lineae lateralis posterior; nIX = nervus glossopharyngeus; nX = nervus vagus and; nSo = nervus spino-occipitales.

The olfactory epithelium is not considered as part of the telencephalon properly. In Brycon orbignyanus it is oval with a narrow support rod surrounded by 25 to 30 lamellae similar in size. The most rostral component of the telencephalon is the bulbus olfactorius . In B. orbignyanus , each nervus tractus olfactorius is composed of a slender and relatively elongated olfactory peduncle with a terminal expansion. The olfactory bulb is oval and elongate, narrower proximally and enlarged distally. The nervus tractus olfactorius is inserted directly on the ventral surface of the telencephalon .

The telencephalon is divided in two distinct parts: a conspicuous and well-developed area dorsale on its dorsal surface, and a small narrow area ventrale on its ventral surface, both parts widely and closely interconnected.

The diencephalon is well developed, located between the telencephalon and rhombencephalon , and composed of the following parts: the epithalamus and a pineal gland, both of which are inconspicuous and easily lost during dissection and located on the dorsal surface, but not in contact with the telencephalon and corpus cerebelli ; an oval and extremely reduced saccus vasculosus ; a vertically developed hypothalamus that is seen as a slight prominence on the ventral surface of the diencephalon , in ventral and lateral views; an oval lobus inferior hypothalami , kidney-shaped in ventral view and smaller than the hypothalamus ; and an oval small hypophysis stalked on the hypothalamus .

The thalamus dorsalis arises from grooves between the tecta optici and the telencephalon , being moderately developed along their extension and thicker than the olfactory tract. The chiasma opticum is located anteriorly to the posterior telencephalon margin.

The mesencephalon is composed of the tecta optici , tegmentum , torus longitudinalis , and the torus lateralis . The tecta optici are well developed, divided in two symmetrical rounded halves that equal to approximately one-third of the brain length; the tegmentum is small and totally covered by the tectum opticus , both in dorsal and lateral views and inconspicuous; the torus longitudinalis is totally inconspicuous (visible only in stained histological sections) located between the tecta optici , near the telencephalon complex; the torus lateralis is reduced and located in front of the lobus inferior hypothalami and the anterior portion of tectum opticum , with undefined limits, both in lateral and ventral views.

The rhombencephalon comprises the associated cerebellar complex and medullary areas; the crista cerebellaris region is almost inconspicuous, being just a slight prominence, when visible; the eminentia granularis is connected exclusively to the medial region of the corpus cerebelli ; the corpus cerebelli is spherical and smaller than the tectum opticum , being the dorsalmost structure of the brain; the lobus vagi is moderately developed and shaped like lateral wings attached to the basis of the corpus cerebelli ; the lobus facialis is inconspicuous and of very difficult visualization.

The medulla spinalis is cylindrical throughout its length, except for its anterior portion, near the corpus cerebelli , where it is flattened and cone-shaped, in dorsal view; the area postrema, usually is approximately trapeze-shaped in dorsal view, but its precise delimitation is possible only in stained histological preparations; the ventriculi quarti region is a semicircular area in dorsal view, with a slight concavity that abuts the corpus cerebelli posterior margin.

The cranial nerves are: rostrally, the nervus olfactorius (nI), ending in the bulbus olfactorius ; the moderately thick nervus opticus (nII), ending in the eyeball; the nervus oculomotorius (nIII), arising from the base of the midbrain crista cerebellaris region; followed by the moderately thick nervus trochlearis (nIV) innervating the eye extrinsic muscle (Meek & Nieuwenhuys, 1998Nieuwenhuys, R., H. J. ten Donkelaar & C. Nicholson (Eds.). 1998. The Central Nervous System of vertebrates. Berlin, Springer-Verlag, XL, 2214p.); and the posteriormost nervus trigeminus (nV), extremely slender, with ramifications not amenable to observation by us. Also in the midbrain section, arising laterally from the base of the rhombencephalon , are the anteriormost nervus fascialis (nVII), followed by the nervus octavus (nVIII), nervus linea lateralis anterior (nlla), nervus glossopharyngeus (nIX), nervus linea lateralis posterior (nllp), and the posteriormost nervus vagus (nX). Also arising from the rhombencephalon , although from its ventral surface, is the nervus abducens (nVI) (Meek & Nieuwenhuys, 1998Nieuwenhuys, R., H. J. ten Donkelaar & C. Nicholson (Eds.). 1998. The Central Nervous System of vertebrates. Berlin, Springer-Verlag, XL, 2214p.). The posteriormost nerve is the nervus spino -occipitalis , arising from the medullary base, wide at its origin and progressively narrow distally. It is probably not a real cranial nerve, but a ganglion located between the ear and the eye, being the anteriormost part of a prominent line of neuromasts that extends from head to tail (Ghysen & Dambly-Chaudière, 2004Ghysen, A. & C. Dambly-Chaudière. 2004. Development of the zebrafish lateral line. Current Opinion in Neurobiology, 14: 67-73.).

Gross brain morphology in other characiforms. Some features related to the forebrain (telencephalon and diencephalon ) rhombencephalon (corpus cerebelli ) and the tecta optici are conserved in the examined taxa, thus allowing us to compare and perceive their variation within 48 taxa of Characiformes and five other non-characiform otophysan taxa herein studied (Table 1). The following similar areas of the gross brain morphologies across all the examined taxa have been considered as clearly perceived and homologous areas: 1) presence or absence of the lobus facialis ; 2) degree of development of the lobus vagi , corpus cerebelli and tecta optici ; 3) width of rhombencephalon ; and 4) external morphology of area postrema (see Discussion).

The telencephalon (pallium ) is the most variable brain area in terms of size and shape, as observed in several other actinopterygian taxa (see Northcutt, 1981Northcutt, R. G. 1981. Evolution of the telencephalon in nonmammals. Annual Review of Neurosciences, 4: 301-350.), due to the formation of a highly differentiated superficial layer of gray matter after the eversion of pallium (Northcutt, 1981Northcutt, R. G. 1981. Evolution of the telencephalon in nonmammals. Annual Review of Neurosciences, 4: 301-350.), as we have also observed both in Characiformes and outgroup taxa, making almost impossible to identify a generalized morphological pattern for the area. The corpus cerebelli together with the telencephalon are the most variable parts of the actinopterygian brains regarding their size and shape (Nieuwenhuys, 1982Nieuwenhuys, R. 1982. An overview of the organization of the brain of Actinopterygian fishes. American Zoologist, 22: 287-310.) and present a unique additional structure known as eminentia granularis in teleosteans (Nieuwenhuys, 1967Nieuwenhuys, R. 1967. Comparative anatomy of the cerebellum. Pp. 1-93. In: Fox, C. A. & R. L. Snider (Eds.). The cerebellum. Progress in Brain Research . Amsterdam, Elsevier.), as observed in characiforms.

On the other hand, in Characiformes the rhombencephalon is moderately developed, (i.e. length and height) with a modest corpus cerebelli , different from the rhombencephalon observed by us in the Cypriniformes, Siluriformes and Gymnotiformes taxa, which present comparatively larger corpus cerebelli .

The area postrema region on the dorsal surface of rhombencephalon presents a unique shape in all the characiform taxa examined, usually with a slight depression, quite different from its shape in the comparative taxa of Cypriniformes, Siluriformes and Gymnotiformes examined (Figs. 2-5).

In the present study, we have observed a considerable diversity in the corpus cerebelli of the Characiformes, always much reduced when compared to the corpus cerebelli of the examined Gymnotiformes and Siluriformes.

The tecta optici form the roof of the midbrain in teleostean fishes and are considered the main visual center in fishes (Northmore, 2011Northmore, D. 2011. Optic tectum. Pp. 131-142. In: Farrell, A. (Ed.). Encyclopedia of Fish Physiology: from genome to environment. Amsterdam, Elsevier.). In the examined taxa, it showed an enormous variation of its relative size, probably related to the relative importance of vision in the various taxa. Nevertheless, several authors affirmed that, in vertebrates, the relative size of parts of vision apparatus is totally correlated to size of the image on retina and visual information reaching the brain (Garamszegi et al., 2002Garamszegi, L. Z, A. P. Møller & J. Erritzøe. 2002. Coevolving avian eye size and brain size in relation to prey capture and nocturnality. Proceedings of the Royal Society of London B, 269: 961-967.; Howland et al., 2004Howland, H. C., S. Merola & J. R. Basarab. 2004. The allometry and scaling of the size of vertebrate eyes. Vision Research, 44: 2043-2065.). According to our results, Characiformes and Cypriniformes usually present normally developed and similar optic structures, differing mostly in size, while the examined Siluriformes and Gymnotiformes taxa possess much reduced optic structures.

The lobus vagi is inconspicuous or almost absent in almost all Characiformes examined. When visible, the lobus vagi is shaped as small lateral wings emerging from the rhombencephalon base, as in Brycon orbygnianus (Figs. 1 and 2), except in the Chilodontidae which have a large lobus vagi , very similar in shape and size to the one found in our representative taxon of the Cypriniformes.

Remarkably the lobus facialis in the Characiformes is barely observable, clearly different from the conspicuous structure found in all the Cypriniformes, Siluriformes and Gymnotiformes examined.

In addition, we also propose herein two apparently exclusive brain features of the Siluriformes among all the examined taxa, but we consider that more studies must be done to establish their real phylogenetic signals, increasing the number of taxa representing this order (Figs. 1-3and 5): (1) olfactory rosette elongate and well developed (Fig. 6c) vs . the olfactory rosette approximately circular and moderately developed in Characiformes, Cypriniformes and Gymnotiformes (Fig. 6a, b and d); and (2) 60 olfactory lamellae present vs . a comparatively reduced number of lamellae, not surpassing 30, in the representatives of the Cypriniformes (16 lamellae), Characiformes (25-30 lamellae), and Gymnotiformes (15 lamellae) (Fig. 6a-d). Taking into account the well-known fact that the Cypriniformes and Characiformes are usually primarily diurnal and visually oriented, whereas the Siluriformes and Gymnotiformes are primarily nocturnal and/or inhabitants of very turbid waters, being oriented mainly by the senses of smell and tact in the case of siluriforms (see Caprio, 1978Caprio, J. 1978. Olfaction and taste in the channel catfish: an electrophysiological study of the responses to amino acids and derivatives. Journal of Comparative Physiology, 123: 357-371.), and almost exclusively by electroreception, in the case of gymnotiforms (Albert et al., 1998Albert, J. S., M. J. Lannoo & T. Turi. 1998. Testing hypotheses of neural evolution in gymnotiform electric fishes using phylogenetic character data. Evolution, 52: 1760-1780.; Albert, 2001Albert, J. S. 2001. Species, diversity and phylogenetic systematics of American Knifefishes (Gymnotiformes, Teleostei). Miscellaneous Publications, Museum of Zoology, University of Michigan, 190: 1-129.), it is to be expected the presence of more complex and developed olfactory rosettes in the Siluriformes.

Fig. 3
Brain of Cyprinus carpio (Cypriniformes: Cyprinidae), LIRP 8923, 72.3 mm SL. a. dorsal; b. lateral and c. ventral views. Apt = Area postrema; Bol = bulbus olfactorius; Ch = chiasma opticum; Cocb = corpus cerebelli; Dien = diencephalon; Eg = eminentia granularis; Hyp = hypophysis; Hyt = hypothalamus; Lih = lobus inferior hypothalami; LobVII = lobus facialis; LobX = lobus vagi; Mo = medulla oblongata; Ms = medulla spinalis; Pob = nervus tractus olfactorius; Tect = tectum opticum; Telen = Telencephalon; Tl = Torus lateralis; Tv = tela ventriculi. Cranial Nerves: nI = nervus olfactorius; nII = nervus opticus; nIII = nervus oculomotorius; nIV = nervus trochlearis; nV = nervus trigeminus; nVI = nervus abducens; nVII = nervus fascialis; nVIII = nervus octavus; nlla = nervus lineae lateralis anterior; nllp = nervus lineae lateralis posterior; nIX = nervus glossopharyngeus; nX = nervus vagus and; nSo = nervus spino-occipitales.

Fig. 4
Brain of Diplomystes mesembrinus (Siluriformes: Diplomystidae), LBP 449, 72.62 mm SL. a. dorsal; b. lateral and c. ventral views. Apt = Area postrema; Bol = bulbus olfactorius; Ch = chiasma opticum; Cocb = corpus cerebelli; Dien = diencephalon; Eg = eminentia granularis; Hyp = hypophysis; Hyt = hypothalamus; Lih = lobus inferior hypothalami; LobVII = lobus facialis; LobX = lobus vagi; Mo = medulla oblongata; Ms = medulla spinalis; Pob = nervus tractus olfactorius; Tect = tectum opticum; Telen = Telencephalon; Tl = Torus lateralis; Tv = tela ventriculi. Cranial Nerves: nI = nervus olfactorius; nII = nervus opticus; nIII = nervus oculomotorius; nIV = nervus trochlearis; nV = nervus trigeminus; nVI = nervus abducens; nVII = nervus fascialis; nVIII = nervus octavus; nlla = nervus lineae lateralis anterior; nllp = nervus lineae lateralis posterior; nIX = nervus glossopharyngeus; nX = nervus vagus and; nSo = nervus spino-occipitales.

Fig. 5
Brain of Gymnotus carapo (Gymnotiformes: Gymnotidae), LIRP 7767, 129.0 mm SL. a. dorsal; b. lateral and c. ventral views. Apt = Area postrema; Bol = bulbus olfactorius; Ch = chiasma opticum; Cocb = corpus cerebelli; Dien = diencephalon; Eg = eminentia granularis; ELL = electrosensory lateral line lobus; Hl = lateral nucleus of hypotalhamus; Hyp = hypophysis; LobX = lobus vagi; Mo = medulla oblongata; Ms = medulla spinalis; ndl = lateral portion of nucleus diffusus; nE = nucleus electrosensorius; Sv = saccus vasculosus; Tect = tectum opticum; Tv = tela ventriculi; Vcocb = valvula cerebellum. Cranial Nerves: nI = nervus olfactorius; nII = nervus opticus; nV = nervus trigeminus; nVI = nervus abducens; nVII = nervus fascialis; nVIII = nervus octavus; nlla = nervus lineae lateralis anterior; nllp = nervus lineae lateralis posterior; nIX = nervus glossopharyngeus; nX = nervus vagus.

Fig. 6
Olfactory epithelium of representatives of Otophysi. a. Cyprinus carpio (Cypriniformes); b. Brycon orbignyanus (Characiformes); c. Pimelodus maculatus (Siluriformes) and; Sternopygus macrurus (Gymnotiformes). Scale bars = 1 mm.

Discussion

As pointed by Striedter (2005Striedter, G. F. 2005. Principles of brain evolution. Irvine, Sinauer Associates, 363p.), even homologous brain regions differ in size, shape, position, cytoarchitecture, histochemistry, connections, and/or function across the major vertebrates groups. Striedter (2005Striedter, G. F. 2005. Principles of brain evolution. Irvine, Sinauer Associates, 363p.), nevertheless, also pointed that the forebrain, corpus cerebelli and tectum opticum are conserved homologous regions of vertebrate brains. Thus, it is not unexpected that we have found the same unequivocally identifiable and conserved homologous regions in the brains of representatives of the 22 families of Characiformes analyzed in this study.

Due to the taxonomic diversity and ecological plasticity of characiform fishes, combined with our aim to make available a first description of the external brain morphology of a characiform, we chose a representative of this order possessing putatively generalized and ancestral-like external brain morphology, since the external brain form of Brycon probably resembles that of the ancestral of all characiforms. Taking these considerations together with the availability of specimens for the inevitable and destructive brain removals, we have opted to use specimens of Brycon . Among the 48 taxa of Characiformes examined by us (Table 1), B. orbignyanus possess the external brain morphology more similar to the representative of the Cypriniformes, the sister order of all remaining Otophysi, especially regarding their respective olfactory bulbs, telencephalon and corpus cerebelli (Figs. 1-3). Also, in many significant past papers the genus Brycon was considered "primitive", "generalized" or phylogenetically basal in the Neotropical Characiformes, or at least in relation to the Characidae, sharing several osteological features with basal African groups (see Weitzman, 1962Weitzman, S. H. 1962. The osteology of Brycon meeki , a generalized characid fish, with an osteological definition of the family. Stanford Ichthyological Bulletin, 8: 1-77.; Buckup, 1998Buckup, P. A. 1998. Relationships of the Characidiinae and phylogeny of characiform fishes (Teleostei: Ostariophysi). Pp. 123-144. In: Malabarba, L. R., R. E. Reis; R. P. Vari, Z. M. S. Lucena & C. A. S. Lucena. (Eds). Phylogeny and classification of Neotropical fishes. Porto Alegre, Edipucrs.; Mirande, 2009Mirande, J. M. 2009. Weighted parsimony phylogeny of the family Characidae (Teleostei: Characiformes). Cladistics, 25: 574- 613., 2010Mirande, J. M. 2010. Phylogeny of the family Characidae (Teleostei: Characiformes): from characters to taxonomy. Neotropical Ichthyology, 8: 385-568.; Malabarba & Weitzman, 2003Malabarba, L. R. & S. H. Weitzman. 2003. Description of a new genus with six new species from Southern Brazil, Uruguay and Argentina, with a discussion of a putative characid clade (Teleostei: Characiformes: Characidae). Comunicações do Museu de Ciências e Tecnologia, PUCRS, Série Zoologia, 16: 67-151. and Oliveira et al., 2011Oliveira, C., G. S. Avelino, K. T. Abe, T. C. Mariguela, R. C. Benine, G. Ortí, R. P. Vari & R. M. C. Castro. 2011. Phylogenetic relationships within the speciose family Characidae (Teleostei: Ostariophysi: Characiformes) based on multilocus analysis and extensive ingroup sampling. BMC Evolutionary Biology, 11: 1-25.).

The use of B. orbignyanus external brain morphology as a surrogate of the hypothetical ancestral external brain morphology of the Characiformes should be done warily, since ours is a preliminary analysis encompassing just part of the many known taxa of Characiformes. Notwithstanding the presence of conserved homologous regions in the brains of all taxa of Characiformes, variation found in the characiform brain gross morphology allows us to consider their brain as a rich source of phylogenetically useful characters.

Bearing that in mind, we herein propose six putative synapomorphic brain features for the Characiformes, not found in the examined Cypriniformes, Siluriformes and Gymnotiformes (Figs. 3-5, respectively): (1) area postrema shaped as an inverted triangle, wider anteriorly and narrowing posteriorly (Figs. 1-2) vs . area postrema equally narrow throughout its full length, with inconspicuous limits in the Cypriniformes, Siluriformes and Gymnotiformes (Figs. 3-5, respectively); (2) width of the rhombencephalon not exceeding the width of the midbrain, both in dorsal and ventral views (Figs. 1-2) vs . rhombencephalon wider than midbrain due to the larger size of the corpus cerebelli in the Cypriniformes, Siluriformes and Gymnotiformes (Figs. 3-5, respectively); (3) lobus vagi less developed (except in the Chilodontidae) (Figs. 1-2) vs . lobus vagi well-developed in the Cypriniformes, Siluriformes and Gymnotiformes (Figs. 3-5, respectively); (4) lobus facialis inconspicuous; when visible, a small oval structure attached to the basis of the corpus cerebellaris (Figs. 1-2) vs . lobus facialis well-developed and visible in Cypriniformes and Siluriformes (Figs. 3-4, respectively), and developed but completely hidden by the uniquely large corpus cerebellaris in the Gymnotiformes (Fig. 5); (5) corpus cerebelli rounded, and elongate vertically (Figs. 1-2) vs . corpus cerebelli horizontally elongate in the Siluriformes and Gymnotiformes (Figs. 4 and 5, respectively) and moderately developed and dorsally pointed in the Cypriniformes (Fig. 3); (6) tectum opticum horizontally elongate, in contact with the anterior margin of the corpus cerebelli except in Stygichthys typhlops (a blind troglobitic species) (Figs. 1-2) vs . tectum opticum in the Cypriniformes vertically elongate and not in contact with the anterior margin of the corpus cerebelli , and relatively reduced in Siluriformes and Gymnotiformes (Figs. 3-5).

Conclusions

The initial premise in our comparative study of the brain gross morphology of the Characiformes reflected the commonly held belief that the Central Nervous System in fishes was highly conserved throughout their evolution (e.g. , Northcutt, 1984Northcutt, R. G. 1984. Evolution of the vertebrate central nervous system: patterns and processes. American Zoologist, 24: 701-716., 2002Northcutt, R. G. 2002. Understanding vertebrate brain evolution. Integrative and Comparative Biology, 42: 743-756.; Butler & Hodos, 2005Butler, A. B. & W. Hodos. 2005. Comparative vertebrate neuroanatomy: evolution and adaptation. Second edition. New Jersey, John Wiley & Sons Publisher, 715 p.). That was not what we found in our study, where the form of the brains has shown surprisingly variation among the examined taxa of Characiformes, having provided six phylogenetically useful characters. Thus, the CNS morphology in the Characiformes, as most probably also in other otophysan orders, is unquestionably worth exploring, as was the case for other non-osteological sources for morphological information (e.g. , Datovo & Castro, 2012Datovo, A . & Castro, R. M. C. 2012. Anatomy and evolution of the mandibular, hyopalatine, and opercular muscles in characiform fishes (Teleostei: Ostariophysi). Zoology (Jena), 115: 84-116.; Datovo & Vari, 2014Datovo A. & R. P. Vari. 2014. The adductor mandibulae muscle complex in lower teleostean fishes (Osteichthyes: Actinopterygii): comparative anatomy, synonymy, and phylogenetic implications. Zoological Journal of the Linnean Society, 171: 554-622.).

Acknowledgments

We are grateful to Mario de Pinna (MZUSP), Claudio de Oliveira (LBP), Paulo Lucinda (UNT-UFT) for loan of specimens for dissection. To Aléssio Datovo (MZUSP) for helping with illustrations in digital interface. To Flávio Bockmann (LIRP-USP), George Mattox (UFSCar-Sorocaba), Marcelo Britto (MNRJ-UFRJ) and Wilfred Klein (FFCLRP-USP), for the very useful criticisms and suggestions offered as members of TNAP's Doctoral Thesis (RMCC Advisor) Examination Committee. To the project "Fundos para o Fortalecimento da Conservação e Pesquisa em Coleções do Departamento de Biologia da Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto" (CNPq process nº 09/54931-0, Flávio Bockmann Coordinator) for the use of a FAXITRON digital x-ray set. TNAP was financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and RMCC was financed by Conselho Nacional Desenvolvimento Científico e Tecnológico (CNPq Proc. 307554/2010-4). This study was partially supported by the FAPESP Thematic Projects "Phylogenetic relationships in the Characidae (Ostariophysi: Characiformes) (FAPESP 04/09219-6, RMCC Coordinator and Principal Investigator), and "South America Characiformes Inventory - SACI" (FAPESP 11/50282-7, Naércio Menezes Coordinator), of which RMCC is a Principal Investigator and TNAP an Associated Investigator.

  • Abrahão, V. P. & F. M. R. S. Pupo. 2014. Técnica de dissecção do neurocrânio de Siluriformes para estudo do encéfalo. Boletim da Sociedade Brasileira de Ictiologia, 112: 21-26.
  • Abrahão, V. P . & O. A. Shibatta. 2015. Gross morphology of the brain of Pseudopimelodus bufonius (Valenciennes, 1840) (Siluriformes: Pseudopimelodidae). Neotropical Ichthyology, 13, 255-264.
  • Albert, J. S. 2001. Species, diversity and phylogenetic systematics of American Knifefishes (Gymnotiformes, Teleostei). Miscellaneous Publications, Museum of Zoology, University of Michigan, 190: 1-129.
  • Albert, J. S., M. J. Lannoo & T. Turi. 1998. Testing hypotheses of neural evolution in gymnotiform electric fishes using phylogenetic character data. Evolution, 52: 1760-1780.
  • Bauchot, R., J. Ridet & M. Bauchot. 1989. The brain organization of butterflyfishes. Environmental Biology of Fishes, 25: 205-219.
  • Buckup, P. A. 1998. Relationships of the Characidiinae and phylogeny of characiform fishes (Teleostei: Ostariophysi). Pp. 123-144. In: Malabarba, L. R., R. E. Reis; R. P. Vari, Z. M. S. Lucena & C. A. S. Lucena. (Eds). Phylogeny and classification of Neotropical fishes. Porto Alegre, Edipucrs.
  • Butler, A. B. & W. Hodos. 2005. Comparative vertebrate neuroanatomy: evolution and adaptation. Second edition. New Jersey, John Wiley & Sons Publisher, 715 p.
  • Caprio, J. 1978. Olfaction and taste in the channel catfish: an electrophysiological study of the responses to amino acids and derivatives. Journal of Comparative Physiology, 123: 357-371.
  • Castro, R. M. C. & R. P. Vari. 2004. Detritivores of the South American fish family Prochilodontidae (Teleostei: Ostariophysi: Characiformes): a phylogenetic and revisionary study. Smithsonian Contributions to Zoology, 622: 1-189.
  • Datovo, A. & F. A. Bockmann. 2010. Dorsolateral head muscles of the catfish families Nematogenyidae and Trichomycteridae (Siluriformes: Loricarioidei): comparative anatomy and phylogenetic analysis. NeotropicalIchthyology,8: 193-246.
  • Datovo, A . & Castro, R. M. C. 2012. Anatomy and evolution of the mandibular, hyopalatine, and opercular muscles in characiform fishes (Teleostei: Ostariophysi). Zoology (Jena), 115: 84-116.
  • Datovo, A . & R. P. Vari. 2013. The jaw adductor muscle complex in teleostean fishes: evolution, homologies and revised nomenclature (Osteichthyes: Actinopterygii). PloS One, 8:4.
  • Datovo A. & R. P. Vari. 2014. The adductor mandibulae muscle complex in lower teleostean fishes (Osteichthyes: Actinopterygii): comparative anatomy, synonymy, and phylogenetic implications. Zoological Journal of the Linnean Society, 171: 554-622.
  • Eastman, J. T. & M. J. Lannoo. 2007. Brain and sense organ anatomy and histology of two species of phyletically basal non-Antarctic thornfishes of the Antarctic suborder Notothenioidei (Perciformes: Bovichtidae). Journal of Morphology, 268: 485-503.
  • Eastman, J. T . & M. J. Lannoo. 2008. Brain and sense organ anatomy and histology of the Falkland Islands mullet, Eleginops maclovinus (Eleginopidae), the sister group of the Antarctic notothenioid fishes (Perciformes: Notothenioidei). Journal of Morphology, 269: 84-103.
  • Evans, H. M. 1931. A comparative study of the brains in British cyprinoids in relation to their habits of feeding, with special reference to the anatomy of the medulla oblongata. Proceedings of the Royal Society of London B, 757: 233-257.
  • Evans, H. M. 1940. Brain and body of fish: a study of brain pattern in relation to hunting and feeding in fish. Philadelphia, The Blakiston Company, 152p.
  • Ewart, J. C. 1888. On the cranial nerves of Elasmobranch fishes: preliminary communication. Proceedings of the Royal Society of London, 45: 524-537.
  • Fink, S. V. & W. L. Fink. 1981. Interrelationships of the ostariophysan fishes (Teleostei). Zoological Journal of Linnean Society, 72: 297-353.
  • Fink, S. V . & W. L. Fink. 1996. Interrelationships of the Ostariophysi. Pp. 209-249. In: Stiassny, M. L. J., L. R. Parenti & G. D. Johnson. Interrelationships of fishes. San Diego, Academic Press.
  • Garamszegi, L. Z, A. P. Møller & J. Erritzøe. 2002. Coevolving avian eye size and brain size in relation to prey capture and nocturnality. Proceedings of the Royal Society of London B, 269: 961-967.
  • Ghysen, A. & C. Dambly-Chaudière. 2004. Development of the zebrafish lateral line. Current Opinion in Neurobiology, 14: 67-73.
  • Herrick, C. J. 1899. The cranial and first spinal nerves of Menidia , a contribution upon the nerves components of the bony fishes. Unpublished Ph.D. Dissertation, Archives of Neurology and Psychopathology, New York, 298p.
  • Herrick, C. J. 1901. The cranial nerves and cutaneous sense organs of the North American siluroid fishes. Journal of Comparative Neurology, 11: 177-249.
  • Howland, H. C., S. Merola & J. R. Basarab. 2004. The allometry and scaling of the size of vertebrate eyes. Vision Research, 44: 2043-2065.
  • Howes, G. J. 1993. Anatomy of the Melanonidae (Teleostei: Gadiformes), with comments on its phylogenetic relationships. Bulletin of British Museum (Natural History), Zoology, 59: 11-31.
  • Huber, R & M. K. Rylander. 1992. Brain morphology and turbidity preference in Notropis and related genera (Cyprinidae, Teleostei). Environmental Biology of Fishes, 33: 153-165.
  • Lisney, T. J. & S. P. Collin. 2006. Brain morphology in large pelagic fishes: a comparison between sharks and teleosts. Journal of Fish Biology, 68: 532-554.
  • Malabarba, L. R. & S. H. Weitzman. 2003. Description of a new genus with six new species from Southern Brazil, Uruguay and Argentina, with a discussion of a putative characid clade (Teleostei: Characiformes: Characidae). Comunicações do Museu de Ciências e Tecnologia, PUCRS, Série Zoologia, 16: 67-151.
  • Meek, J. & R. Nieuwenhuys. 1998. Holosteans and teleosts Pp. 759-937. In:Nieuwenhuys, R., H. J. ten Donkelaar & C. Nicholson (Eds.). The central nervous system of vertebrates. Berlin, Springer-Verlag.
  • Miller, R. J. & H. E. Evans. 1965. External morphology of the brain and lips in catostomid fishes. Copeia, 1965: 467-487.
  • Mirande, J. M. 2009. Weighted parsimony phylogeny of the family Characidae (Teleostei: Characiformes). Cladistics, 25: 574- 613.
  • Mirande, J. M. 2010. Phylogeny of the family Characidae (Teleostei: Characiformes): from characters to taxonomy. Neotropical Ichthyology, 8: 385-568.
  • Nieuwenhuys, R. 1967. Comparative anatomy of the cerebellum. Pp. 1-93. In: Fox, C. A. & R. L. Snider (Eds.). The cerebellum. Progress in Brain Research . Amsterdam, Elsevier.
  • Nieuwenhuys, R. 1982. An overview of the organization of the brain of Actinopterygian fishes. American Zoologist, 22: 287-310.
  • Nieuwenhuys, R., H. J. ten Donkelaar & C. Nicholson (Eds.). 1998. The Central Nervous System of vertebrates. Berlin, Springer-Verlag, XL, 2214p.
  • Northcutt, R. G. 1981. Evolution of the telencephalon in nonmammals. Annual Review of Neurosciences, 4: 301-350.
  • Northcutt, R. G. 1984. Evolution of the vertebrate central nervous system: patterns and processes. American Zoologist, 24: 701-716.
  • Northcutt, R. G. 1985. Brain phylogeny: speculations on pattern and cause. Pp. 351-378. In:Cohen, M. J. & F. Strumwasser (Eds.). Comparative neurobiology: modes of communication in the nervous system. New York, Wiley.
  • Northcutt, R. G. 2002. Understanding vertebrate brain evolution. Integrative and Comparative Biology, 42: 743-756.
  • Northmore, D. 2011. Optic tectum. Pp. 131-142. In: Farrell, A. (Ed.). Encyclopedia of Fish Physiology: from genome to environment. Amsterdam, Elsevier.
  • Oliveira, C., G. S. Avelino, K. T. Abe, T. C. Mariguela, R. C. Benine, G. Ortí, R. P. Vari & R. M. C. Castro. 2011. Phylogenetic relationships within the speciose family Characidae (Teleostei: Ostariophysi: Characiformes) based on multilocus analysis and extensive ingroup sampling. BMC Evolutionary Biology, 11: 1-25.
  • Parenti, L. R. 1993. Relationships of atherinomorph fishes (Teleostei). Bulletin of Marine Science, 52: 170-196.
  • Parenti, L. R. 2005. The phylogeny of atherinomorphs: evolution of a novel fish reproductive system. Pp. 13-30. In: Uribe, M. C. & H. J. Grier (Eds.). Viviparous fishes. Homstead, New Life Publication.
  • Pereira, T. N. A. 2014. Anatomia encefálica comparada de Characiformes (Teleostei: Ostariophysi). Unpublished Ph. D. Dissertation. Universidade de São Paulo, Ribeirão Preto, 279 p.
  • Pupo, F. M. R. S. 2011. Anatomia comparada da morfologia externa do sistema nervoso central da família Callichthyidae (Teleostei: Ostariophysi: Siluriformes) e suas implicações filogenéticas. Unpublished M. Sc. Dissertation. Universidade Federal do Rio de Janeiro, Rio de Janeiro, 97 p.
  • Reis, R. E., S. O. Kullander & C. J. Ferraris (Eds.). 2003. Check list of the Freshwater fishes of South and Central America. Porto Alegre, Edipucrs , 729p.
  • Roberts, T. 1969. Osteology and relationships of characoid fishes, particularly the genera Hepsetus , Salminus , Hoplias , Ctenolucius, and Acestrorhynchus . Proceedings of the California Academy of Sciences, 36: 391-500.
  • Striedter, G. F. 2005. Principles of brain evolution. Irvine, Sinauer Associates, 363p.
  • Walsh, S. & A. Milner. 2011. Evolution of the avian brain and senses. Pp. 282-305. In: Dyke, G. & G. Kaiser. Living dinosaurs: The evolutionary history of modern birds. Chichester. John Wiley & Sons Publisher.
  • ten Donkelaar, H. J. 1998a. Anurans. Pp. 1151-1314. In: Nieuwenhuys, R., H. J. ten Donkelaar & C. Nicholson (Eds.). The central nervous system of vertebrates. Berlin, Springer-Verlag.
  • ten Donkelaar, H. J. 1998b. Reptiles. Pp. 1315-1524. In: Nieuwenhuys, R., H. J. ten Donkelaar & C. Nicholson (Eds.). The central nervous system of vertebrates. Berlin, Springer-Verlag.
  • Weitzman, S. H. 1962. The osteology of Brycon meeki , a generalized characid fish, with an osteological definition of the family. Stanford Ichthyological Bulletin, 8: 1-77.
  • Wiley E. O. & G. D. Johnson. 2010. A teleost classification based on monophyletic groups. Pp. 123-182. In: Nelson J. S., H.-P. Schultze & M. V. H. Wilson (Eds.). Origin and phylogenetic interrelationships of teleosts. München, Verlag Dr. Friedrich Pfeil.
  • Yamamoto, M. 1982. Comparative morphology of the peripheral olfactory organ in teleosts. Pp. 39-59. In: Hara, T. J. (Ed.). Chemoreception in fishes. Developments in Aquaculture and Fisheries Science. New York, Elsevier.

Publication Dates

  • Publication in this collection
    2016

History

  • Received
    28 Apr 2015
  • Accepted
    20 June 2016
Sociedade Brasileira de Ictiologia Neotropical Ichthyology, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá., Av. Colombo, 5790, 87020-900, Phone number: +55 44-3011-4632 - Maringá - PR - Brazil
E-mail: neoichth@nupelia.uem.br