Brain and Sense Organ Anatomy and Histology of the ... - Lannoo Lab

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BRAIN AND SENSE ORGANS OF ELEGINOPS MACLOVINUS 85 Fig. 1. Cladogram of relationships within the notothenioid suborder (Near et al., 2004), pruned to the level of family, showing the Eleginopidae as the sister group of the Antarctic clade. Original cladogram is a strict consensus of four trees resulting from maximum parsimony analysis of the complete gene 16S rRNA dataset and the analysis of this data demonstrates monophyly for the suborder (Near et al., 2004). Wedges are proportional to species diversity in each family with an updated list of species, currently numbering 131, posted at http://www.oucom. ohiou.edu/dbms-eastman. Geographic distributions also indicated, with Gon and Heemstra (1990) taken as authoritative for species with Antarctic distributions. Non-Antarctic species have distributions exclusively outside the Antarctic and Subantarctic Regions. Shading indicates clades with predominantly non-Antarctic (blue), predominantly Antarctic (green), and mixed (purple) distributions. Antifreeze glycoproteins (AFGP) characteristic of the Antarctic clade are mapped. 200 species (Jenkins and Burkhead, 1994; Boschung and Mayden, 2004; Nelson, 2006). At the opposite extreme of the habitat spectrum, about 100 perciform species of the suborder Notothenioidei dominate the cold waters of the Southern Ocean surrounding Antarctica (Eastman, 1993). In the absence of competition from most other fish groups, this polar radiation has resulted in notothenioids monopolizing species diversity (76.6%), abundance (91.6%), and biomass (91.2%) on the Antarctic shelf (Eastman, 2005). This level of dominance by a single taxonomic group is unique among piscine shelf faunas of the world. For over a decade, we have been conducting a morphological survey of notothenioid brains and sense organs to examine the effects of phyletic diversification on the structure of these systems. Because of the presence of infrastructure (established field stations and available research vessels), the phyletically derived Antarctic species are more readily available. Therefore, we began our survey with Antarctic nototheniids (Eastman and Lannoo, 1995), then progressed to artedidraconids (Eastman and Lannoo, 2003a), bathydraconids (Eastman and Lannoo, 2003b), and channichthyids (Eastman and Lannoo, 2004; Fig. 1). A recent cruise in the periphery of the Southern Ocean allowed us to collect and study phyletically basal bovichtids (Eastman and Lannoo, 2007) and eleginopids, the sister group of the Antarctic clade. The monotypic family Eleginopidae is represented by Eleginops maclovinus, locally known as mullet or róbalo. Eleginops has a non-Antarctic distribution and is common in southern South America and the Falkland Islands; this distribution may reflect an historic pattern on the South American component of the Gondwanan shelf. Unlike the Antarctic clade of notothenioids (see Fig. 1), eleginopinids did not become associated with the margins of the Antarctic plate and their subsequent evolution was little influenced by large-scale tectonic movements or by the cooling of the Southern Ocean (Eastman, 1993). As the sister group of the Antarctic clade (see Fig. 1), Eleginops is of interest in understanding notothenioid diversification because it represents the ‘‘starting point’’ for the notothenioid radiation. Eleginops maclovinus is a relatively large notothenioid reaching a maximum total length (TL) of 90 cm in the Falkland Islands (Falkland Islands Government, 2003; Brickle et al., 2005a). It has small, mobile subterminal jaws, small eyes, and small, cephalic lateral line pores (Figs. 2 and 7A). Although traditionally considered an opportunistic benthic omnivore in nearshore marine and estuarine habitats (Pequeño, 1989; Licandeo et al., 2006), recent research on a population from the Valdivia River in Chile indicates that both juveniles and adults are opportunistic carnivores capable of feeding in both marine and freshwater environments (Pavés et al., 2005). Amphipods and insects are the most abundant prey taxa in the Valdivia River, with plants and bryozoans being inadvertently consumed during feeding, as they serve as sites of refuge for crustaceans (Pavés et al., 2005). Unlike many other notothenioids, Eleginops maclovinus has a streamlined body with the free margin of the pectoral fin oblique rather than round, thus producing a higher aspect ratio (see Fig. 2). Eleginops has a relatively larger mass of Fig. 2. Live specimen of Eleginops maclovinus (SL 5 40 cm) showing general appearance and body shape. 30.28. Journal of Morphology DOI 10.1002/jmor
86 J.T. EASTMAN AND M.J. LANNOO red pectoral musculature and a greater capacity for sustained labriform swimming than other notothenioids (Fernández et al., 1999). The rapidity of its escape response is similar to eurythermal temperate non-notothenioids rather than to Antarctic notothenioids (Fernández et al., 2002) and its resting rate of oxygen consumption place it in an active category in comparison with sympatric non- Antarctic notothenioids (Vanella and Calvo, 2005). In the Falkland Islands, Eleginops is subject to an annual temperature range of 0–158C in the tidal creeks (Falkland Islands Government, 2003) and 4–118C in shelf waters (Arkhipkin et al., 2004). Other aspects of its life history distinguish Eleginops maclovinus from the stenohaline, sedentary, cold adapted Antarctic notothenioids. For example, it is one of only two euryhaline notothenioid species. Eleginops inhabits coastal waters, sounds, and tidal creeks in the Falkland Islands (Boulenger, 1900; Hart, 1946; Falkland Islands Government, 2003; Brickle et al., 2005a,b) and coastal waters, estuaries, and rivers in southern South America. Its distribution ranges from the Beagle Channel (548S) to approximately the Golfo San Matías, Argentina (408S) on the Atlantic coast (Gosztonyi, 1979) and Valparaiso, Chile (32–338S) on the Pacific coast (Gosztonyi, 1979; Pequeño, 1989; Ojeda et al., 2000). In Chile, Eleginops is dominant in both number and biomass in some estuaries, which also serve as breeding sites for adults and nursery grounds for young (Pequeño, 1981). Unlike the situation in Chile, the population of Eleginops in north central Patagonia has been observed spawning in shelf waters where bottom depths are 75–76 m, with the young then migrating to inshore waters rather than estuaries to begin their adult lives (Cousseau et al., 2004; Dr. A.E. Gosztonyi, personal communication). In the Falkland Islands, juveniles reside in creeks or sounds and adults forage in larger creeks and sounds but migrate to spawn in shelf waters 30– 100 m deep, occasionally reaching the shelf break at 250 m (Falkland Islands Government, 2003; Brickle et al., 2005a,b). Some populations of Eleginops are therefore catadromous or marginally catadromous, as defined by McDowall (1988, p. 20, 33), since most of the life cycle is spent in fresh or brackish water and the spawning migration of adults takes them to the sea or to the mouths of estuaries or sounds to breed. Populations of Eleginops maclovinus in the Beagle Channel in Argentina (Calvo et al., 1992), in southern Chile (Licandeo et al., 2006) and in the Falkland Islands (Brickle et al., 2005b) exhibit a type of sex reversal known as protandrous hermaphroditism, with males in the Falklands predominating at a TL of 10–52 cm and females at TL >53 cm. Eleginops has small pelagic eggs and the highest fecundity of any notothenioid (Brickle et al., 2005a). The larvae have never been caught Journal of Morphology DOI 10.1002/jmor and definitively identified in the Falkland Islands (Dr. Paul Brickle, personal communication). Unlike the Antarctic notothenioids, Eleginops is a rapidly growing species with a maximum age of 11 years (Brickle et al., 2005a). The status of Eleginops maclovinus as the sister group of the Antarctic notothenioids (see Fig. 1) is supported by phylogenetic analyses employing both morphological (Balushkin, 1992, 2000) and molecular data, including partial (Bargelloni et al., 2000) and complete (Near et al., 2004) mtDNA gene sequences. Antifreeze glycoproteins (AFGPs) are a key innovation and a physiological necessity that allowed Antarctic notothenioids to survive and diversify in ice-laden seawater (DeVries and Cheng, 2005). The phyletically basal bovichtids and pseudaphritids (see Fig. 1), as well as Eleginops, do not possess AFGP gene sequences in their genomes (Cheng et al., 2003), indicating that they diverged before the tectonic isolation and associated cooling of Antarctica. The split between eleginopids and the Antarctic clade, the five families with AFGPs that inhabit the cold shelf waters of the continent, is variously estimated to have occurred at 5–14 million years ago (mya) (Chen et al., 1997), 27 mya (Bargelloni et al., 2000), or 40 mya (Near, 2004). The 40 mya estimate is based on a fossil calibration of what may or may not be an extinct eleginopid (Eastman, 2005). Near (2004) discusses reasons for the discrepancies among these dates. Irrespective of its divergence time, Eleginops maclovinus has not been subjected to polar environmental conditions. Because of this, and its sister group relationship to the Antarctic clade, it is an ideal subject for studying the morphology of notothenioid nervous and sensory systems that have not had historical exposure to the unusual Antarctic thermal and light regimes experienced by the phyletically derived species living on the high latitude shelf. Since a base of information on neural and sensory morphology is available for the Antarctic notothenioids (Eastman and Lannoo, 1995, 2003a,b, 2004; Lannoo and Eastman 1995, 2000), our focus here for Eleginops is to 1) present a detailed description of the brain and cranial nerves; 2) document the anatomy and histology of the brain, olfactory apparatus, retina, and branched membranous extensions of the cephalic lateral lines; 3) examine ocular vascular structures; and 4) compare eleginopid neural and sensory morphology with that of the phyletically derived Antarctic notothenioids. MATERIALS AND METHODS Specimens and Nomenclature We collected material during the ICEFISH cruise (No. 04-04) of the RV Nathaniel B. Palmer in the South Atlantic Ocean. The cruise began in Punta Arenas, Chile on May 17, 2004 and
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