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JOURNAL OF MORPHOLOGY 269:84–103 (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)

Joseph T. Eastman 1 * and Michael J. Lannoo 2

1 Department of Biomedical Sciences, College of Osteopathic Medicine, Ohio University, Athens, Ohio 45701-2979

2 Indiana University School of Medicine – Terre Haute, Indiana State University, Terre Haute, Indiana 47809-9989

ABSTRACT The perciform notothenioid fish Eleginops

maclovinus, representing the monotypic family Eleginopidae,

has a non-Antarctic distribution in the Falkland

Islands and southern South America. It is the sister

group of the five families and 103 species of Antarctic

notothenioids that dominate the cold shelf waters of

Antarctica. Eleginops is the ideal subject for documenting

the ancestral morphology of nervous and sensory

systems that have not had historical exposure to the unusual

Antarctic thermal and light regimes, and for comparing

these systems with those of the phyletically

derived Antarctic species. We present a detailed description

of the brain and cranial nerves of Eleginops and

ask how does the neural and sensory morphology of this

non-Antarctic notothenioid differ from that seen in the

phyletically derived Antarctic notothenioids? The brain

of Eleginops is similar to those of visually oriented temperate

and tropical perciforms. The tectum is smaller

but it has well-developed olfactory and mechanoreceptive

lateral line areas and a large, caudally projecting

corpus cerebellum. Eye diameter is about twofold

smaller in Eleginops than in many Antarctic species.

Eleginops has a duplex (rod and cone) retina with single

and occasional twin cones conspicuous centrally. Ocular

vascular structures include a large choroid rete mirabile

and a small lentiform body; a falciform process and hyaloid

arteries are absent. The olfactory rosette is oval

with 50–55 lamellae, a large number for notothenioids.

The inconspicuous bony canals of the cephalic lateral

line system are simple with membranous secondary

branches that lack neuromasts. In Antarctic species, the

corpus cerebellum is the most variable brain region,

ranging in size from large and caudally projecting to

small and round. ‘‘Stalked’’ brains showing reduction in

the size of the telencephalon, tectum, and corpus cerebellum

are present in the deep-living artedidraconid

Dolloidraco longedorsalis and in most of the deep-living

members of the Bathydraconini. Eye diameter is generally

larger in Antarctic species but there is a phylogenetic

loss of cellularity in the retina, including cone photoreceptors.

Some deep-living Antarctic species have lost

most of their cones. Mechanosensation is expanded in

some species, most notably the nototheniid Pleuragramma

antarcticum, the artedidraconid genera Dolloidraco

and Pogonophryne, and the deep living members

of the bathydraconid tribe Bathydraconini. Reduction in

retinal cellularity, expansion of mechanoreception, and

stalking are the most noteworthy departures from the

morphology seen in Eleginops. These features reflect a

modest depth or deep-sea effect, and they are not

uniquely ‘‘Antarctic’’ attributes. Thus, at the level of

organ system morphology, perciform brain and sensory

systems are suitable for conditions on the Antarctic shelf,

with only minor alterations in structure in directions

exhibited by other fish groups inhabiting deep water.

Notothenioids retain a relative balance among their array

of senses that reflects their heritage as inshore perciforms.

J. Morphol. 269:84–103, 2008. Ó 2007 Wiley-Liss, Inc.

KEY WORDS: brain histology; retinal histology; cephalic

lateral line system; olfactory system

With over 10,000 species, teleost fishes of the

order Perciformes constitute 36% of known fish

and 18% of known vertebrate species (Nelson,

2006). This phyletic profusion reflects a genotype

and a body plan with an unparalleled capacity to

generate diversity in both shallow marine habitats

and in various freshwater habitats throughout the

world. For example, perciforms constitute 9 of 10

families and about 75% of the species characteristic

of tropical coral reef faunas (Bellwood and

Wainwright, 2002). In addition, perciform cichlid

stocks in East Africa have given rise to hundreds

of species in some lakes and provide classic examples

of adaptive radiations and species flocks

(Kornfield and Smith, 2000; Kocher, 2004; Seehausen,

2006). In the temperate streams of eastern

North America, darters of the percid subfamily

Etheostomatinae constitute a radiation of nearly

Contract grant sponsor: National Science Foundation; Contract

grant number: ANT 04-36190; Contract grant sponsor: National

Institutes of Health; Contract grant number: NS37600-01; Contract

grant sponsor: Indiana University School of Medicine.

*Correspondence to: J.T. Eastman, Department of Biomedical Sciences,

College of Osteopathic Medicine, Ohio University, Athens,

OH 45701-2979. E-mail: eastman@ohiou.edu

Published online 27 September 2007 in

Wiley InterScience (www.interscience.wiley.com)

DOI: 10.1002/jmor.10571

Ó 2007 WILEY-LISS, INC.


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


BRAIN AND SENSE ORGANS OF ELEGINOPS MACLOVINUS 87

ended in Cape Town, South Africa on July 17, 2004. During a

stop at Stanley (51842 0 S; 57851 0 W) in the Falkland Islands, we

captured Eleginops maclovinus (Cuvier and Valenciennes, 1830)

with a 30-m long beach seine in Fish Creek (water temperature

58C), Port Louis, East Falkland Island on May 29. These

specimens were 29–49 cm TL, 24–43 cm standard length (SL)

and most were males since they had not yet reached the length

at which transformation to females typically occurs.

In describing brain nuclei, we follow the nomenclature of

authors included in Northcutt and Davis (1983) and Davis and

Northcutt (1983) with the exception of the lateral line nerves.

What have been traditionally termed the anterior and posterior

lateral line nerves of fishes are actually ‘‘complexes’’ consisting

of several distinct cranial nerves (Northcutt, 1989; Northcutt

and Bemis, 1993). We follow Northcutt (1989) in distinguishing

the anterodorsal and anteroventral lateral line nerves as innervating

both canal and superficial neuromasts on the head.

When describing ocular structures and vasculature, we use the

nomenclature of Nicol (1989).

Histology

We fixed specimens onboard ship by transcardial perfusion of

Bouin’s fixative. After anesthetization in a solution of 3-aminobenzoic

acid ethyl ester (MS-222, Sigma), the heart and bulbus

arteriosus were exposed. Notothenioid saline solution (O’Grady

et al., 1982) was prepared, adjusted with NaCl to a concentration

of 330 mOsm/L, maintained at ambient seawater temperature,

and perfused through the ventral aorta. Saline was followed

by Bouin’s fixative. During this perfusion, the gills were

periodically irrigated with seawater of ambient temperature

(58C). Three hours after perfusion, we removed brains and

other tissues of interest and postfixed them in Bouin’s. After

several days of fixation, we transferred tissues to 70% ethanol

for storage and transport.

We subjected brains to the following protocol: dehydration in

alcohol, clearing in butanol, and embedding in paraffin according

to standard procedures (Kiernan, 1990). Embedded brains

and spinal cords were cut in a transverse plane on a rotary

microtome to produce sections 10–12-lm thick. Sections were

mounted on slides, dried, deparaffinized, stained with hematoxylin

and eosin, dehydrated, and coverslipped using Cytoseal 60

as the mounting medium. We tried the traditional neurological

stain for Nissl substance, 0.1% aqueous cresyl violet acetate, on

these brains but slides would not adequately destain, probably

because of the effects of fixation in Bouin’s solution.

We cut histological sections of the eyes of five specimens. In

examining the eyes, we took dorsoventral strips from the central

retina immediately temporal (lateral) to the optic disk. We

also took transverse sections of the ventral retina in the area of

the choroid fissure. We employed the histological protocol outlined

earlier except that CitriSolv (Fisher Scientific) was substituted

for butanol and sections were cut at 7 lm. In measuring

retinal thickness, we excluded the optic nerve fiber layer. Sections

were stained with hematoxylin and eosin, phloxine B, and

methylene blue, Gomori’s one step trichrome, or Bodian’s Protargol

for 24 h at 508C.

We counted olfactory lamellae in six specimens of Eleginops

maclovinus. We also examined transverse and longitudinal serial

histological sections of the olfactory apparatus and of the

head, with an emphasis on the membranous canals of the cephalic

lateral line system. We used the same histological techniques

outlined earlier.

Other Morphological Procedures

We examined the cephalic lateral line canal system to determine

whether or not Eleginops maclovinus has membranous

canals branching off of the bony canals. For this, we used specimens

that had been cleared and stained with alizarin red S

(Taylor, 1967) dissolved in 75% ethyl alcohol (Springer and

Johnson, 2000). The head skin was left intact to preserve the

membranous canals.

We used yellow Microfil 1 (Flow Tech, Carver, MA), a liquid

silicon rubber injection compound, to demonstrate ocular blood

vessels. We injected fish in the caudal vein with 0.3 ml of heparinized

(20 mg/ml) notothenioid saline and then returned them

to the holding tank for 15 min. After anaesthetization, we

placed the specimens ventral side-up on an iced surgical platform.

We cut the bulbus-ventricle junction and cannulated the

ventral aorta with a 34-cm length of either PE-50 tubing (0.96

mm OD) or PE-160 tubing (1.57 mm OD). We blunted the free

end on a hot plate and secured the cannula with two sutures.

The cannula was in turn connected to a 23-G or 18-G needle,

an 84-cm extension tube and a 20-ml syringe. The entire apparatus

was surrounded by ice to maintain a body temperature of

58C. We placed the syringe in either a Sage model 341B or a

KD Scientific model 100 syringe pump and began the perfusion

with notothenioid saline followed by Microfil. Flow rate was

about 0.5–1.0 ml/min. We allowed the Microfil to polymerize

while maintaining the specimen on ice for about 1 h, and then

preserved the specimen in 10% formalin with subsequent storage

in 70% ethanol.

Since Microfil did not fill hyaloid arteries at the vitreoretinal

interface in Eleginops maclovinus, another means of assessing

the presence or absence of these vessels was necessary. We

removed a block of skull containing the eyes from four Microfil

specimens and dissected away the cornea, lens, vitreous body,

and some of the vitreous membrane. We introduced a reversible

stain (a mixture of 1 part of 1% aqueous aniline blue and 10

parts of saturated aqueous picric acid) into the vitreous chamber

for 12 min. We then rinsed with water and returned the

specimen to 70% ethanol for additional dissection, examination,

and storage. If present, the hyaloid arteries stain more darkly

than the background and can be seen radiating from the falciform

artery at the optic disk.

RESULTS

Brain and Cranial Nerve Anatomy

In gross view, the brain of Eleginops maclovinus

exhibits a mixture of reduced and hypertrophied

structures (see Fig. 3). The olfactory bulbs are

large and positioned rostral to the telencephalon.

The telencephalic lobes are about twice the volume

of the olfactory bulbs and roughly half the volume

of the tectal lobes. Lobules of the telencephalon

are pronounced, with dorsodorsal, dorsomedial,

and dorsolateral nuclei prominent. The tectal lobes

(vision) are small- to medium-sized, as are the inferior

lobes (Fig. 3A). The corpus cerebellum

(motor skill) is large, dorsally expanded, and caudally

directed. The eminentia granularis and crista

cerebellares, two structures associated with

mechanoreceptive lateral line inputs, are well

developed. A decussation of the crista cerebellares

is present, bridging the fourth ventricle (Fig. 3B).

Cranial nerves exhibit proportions atypical for

perciforms but in accordance with Eleginops brain

regions. The optic nerve is the largest-diameter

cranial nerve and is pleated, but is relatively small

for a perciform brain, only slightly larger than the

olfactory nerve. The olfactory nerve is relatively

large and exhibits a prominent bulge immediately

rostral to the olfactory bulb (Fig. 3A). The anterior

dorsal and anterior ventral lateral line nerve complexes

are more than twice the diameter of the

Journal of Morphology DOI 10.1002/jmor


88 J.T. EASTMAN AND M.J. LANNOO

Fig. 3. Brain and cranial nerves of Eleginops maclovinus (SL 5 34.5 cm) in left lateral (top) and dorsal (bottom) views 34.3. To

illustrate features of the rhombencephalon in dorsal view, the drawing was made from a slightly oblique dorsocaudal angle. Therefore

structures such as the corpus of the cerebellum are not perfectly aligned in the two views of the brain. ADLL, anterodorsal lateral

line nerve complex; AVLL, anteroventral lateral line nerve complex; CC, crista cerebellaris of the rhombencephalon; CCb, corpus

division of the cerebellum; Dl, dorsolateral subdivision of the telencephalon; Dd, dorsodorsal subdivision of the telencephalon;

Dm, dorsomedial subdivision of the telencephalon; EG, eminentia granularis division of the cerebellum; IL, inferior lobe of the diencephalon;

OB, olfactory bulb; Pit, pituitary gland; PLL, posterior lateral line nerve complex; SN1, first spinal nerve; SN2, second

spinal nerve; SV, saccus vasculosus; Tec, tectum of the mesencephalon; Tel, telencephalon; I, olfactory nerve; II, optic nerve; III,

oculomotor nerve; IV, trochlear nerve; V, trigeminal nerve; VII, facial nerve; VIII, auditory/vestibular nerve; IX, glossopharyngeal

nerve; X, vagus nerve.

posterior lateral line nerve complex. The vagus

nerve is large. The octaval nerve (hearing and balance),

oculomotor, trochlear, and abducens nerves

(eye movement), as well as the spinal nerves are

proportional.

Brain and Spinal Cord Histology

Olfactory nerve and telencephalon. In gross

view, the olfactory bulbs are sessile, positioned at

the rostral base of the telencephalon. Before entering

the olfactory bulbs, the olfactory nerves exhibit

expansions. Histologically, these expansions consist

of fiber bundles interspersed centrally with

sparse groups of small cells (Fig. 4A). Cell types

characteristic of the olfactory bulbs, including glomerular

cells and the medial smaller cell layers

(not labeled), appear caudal to the olfactory nerve

expansions and rostral to the leading edge of the

telencephalon (Fig. 4B).

The rostral portion of the telencephalon is positioned

over the caudal portion of the olfactory

bulbs and consists primarily of the dorsal division,

characterized by uniform, small cells. Cell groups

present but not particularly prominent include the

dorsodorsal, dorsomedial, and dorsolateral nuclei

(Fig. 4C). At the level of the anterior commissure,

the dorsodorsal, dorsomedial, dorsolateral, and

dorsocentral nuclei are prominent, as are nuclei in

the ventral division, including the ventrodorsal,

Journal of Morphology DOI 10.1002/jmor


BRAIN AND SENSE ORGANS OF ELEGINOPS MACLOVINUS 89

Fig. 4. Brain histology (transverse sections) of Eleginops maclovinus (SL 5 24.5 cm) from olfactory bulbs (A) through rostral

spinal cord (V). Stain: Hematoxylin and eosin. Magnifications: A, B, G, 316.4; C, 316.8; D–F, R, V, 310.8; H, T, 310.3; I, 39.2; J,

L–O, 37.7; K, P, Q 38.2; S, 313.7; U, 312.3. AC, anterior commissure; CC, crista cerebellaris; CCb, corpus division of the cerebellum;

CM, mammillary bodies; CP, central posterior nucleus of the thalamus; Dc, dorsocentral nucleus of the telencephalon; dCC,

decussation of the crista cerebellaris; Dd, dorsodorsal nucleus of the telencephalon; Dl, dorsolateral nucleus of the telencephalon;

Dm, dorsomedial nucleus of the telencephalon; Dp, dorsoposterior nucleus of the telencephalon; DP, dorsal posterior nucleus of the

thalamus; E, endopeduncular nucleus; EG, eminentia granularis; G, nucleus glomerulosus; Ha, habenula; Hd, dorsal nucleus of the

diencephalon; Hv, ventral nucleus of the diencephalon; IL, inferior lobe of diencephalon; LR, lateral recess of the inferior lobe; LT,

lateral tuberal nucleus; MLF, medial longitudinal fasciculus; ND, nucleus diffusus of the inferior lobe; OB, olfactory bulb; PC, posterior

commissure; PG, nucleus preglomerulosus; Pp, preoptic nucleus; RF, reticular formation; Sps, spinal sensory nucleus; SV,

saccus vasculosus; Tec, tectum of the mesencephalon; TL, torus longitudinalis of the mesencephalon; TP, posterior tuberal nucleus;

TS, torus semicircularis of the mesencephalon; VCb, valvula cerebelli; VM, dorsal medial nucleus of the thalamus; Xs, visceral sensory

nucleus of the vagal nerve; CN I, olfactory nerve; II, optic nerve; III/IV, oculomotor/trochlear nerve complex; Vm, motor nucleus

of the trigeminal nerve.

Journal of Morphology DOI 10.1002/jmor


90 J.T. EASTMAN AND M.J. LANNOO

Figure 4.

(Continued.)

and ventroventral nuclei (not shown; Fig. 4D,E).

The anterior commissure is thick, and the white

matter associated with this fiber bundle is extensive

(Fig. 4D,E). Caudally, the dorsoposterior

nuclei are medium sized and protrude ventrally,

contributing to a top-heavy appearance (Fig. 4F).

Cells in the dorsal region are notably differentiated

by size and arrangement, and the dorsal portion

of the dorsolateral nucleus forms a discrete

lobe (Fig. 4F). In the caudal-most telencephalon,

the ventral portion of the dorsolateral nucleus

overlies the dorsoposterior nucleus (Fig. 4G).

Diencephalon. The rostral preoptic area is

small and consists of a parvocellular preoptic nucleus

(Fig. 4E,F). Farther caudally, the endopeduncular

nucleus forms a tight cluster of cells within

the preoptic region (Fig. 4G,H). At the level of the

rostral pituitary, cells of the magnocellular pre-

Journal of Morphology DOI 10.1002/jmor


BRAIN AND SENSE ORGANS OF ELEGINOPS MACLOVINUS 91

Figure 4.

(Continued.)

optic nucleus are abundant in the dorsal preoptic

area and the endopeduncular nucleus is large

(Fig. 4G). In the central diencephalic region, the

preoptic region contains both parvocellular and

magnocellular cells (Fig. 4G,H). The habenula is

medium-sized and thalamic nuclei, including the

ventromedial nucleus, are present and exhibit a

normal appearance. Cells comprising the lateral

tuberal nucleus are large and form a prominent

cluster (Fig. 4H). The pituitary is also large and

appears well organized (not shown). At the level of

the posterior commissure, narrow subependymal

expansions are present (Fig. 4I,J), thalamic nuclei,

including the dorsoposterior and centroposterior

nuclei, and hypothalamic nuclei, including the dorsal

and ventral nuclei, appear in normal positions

Journal of Morphology DOI 10.1002/jmor


92 J.T. EASTMAN AND M.J. LANNOO

and proportions. Nucleus preglomerulosus is normally

proportioned. The inferior lobes are small to

medium sized.

Farther caudally, the nucleus glomerulosus is

large and circular shaped, the posterior tuberal

nucleus crosses the midline (Fig. 4K,L). Immediately

ventral to the posterior tuberal nuclei the

mammillary bodies meet along the third ventricle.

At this level the inferior lobes are medium sized,

cells of the nucleus diffusus are small and sparse,

and the lateral recess is positioned within the lobe.

The saccus vasculosus is small. Farther caudally,

at the level of the oculomotor nerve (Fig. 4L,M),

cells within the nucleus diffusus are well organized.

Near the caudal-most inferior lobes, nucleus

diffusus cells are less well organized and the lateral

recesses become subpial (Fig. 4N).

Mesencephalon. The tectum is small and

unusually proportioned. Rostrally (Fig. 4I) the superficial

white matter, consisting of the superficial

white and gray zone, the central zone, and the

deep white zone, is proportional along the dorsal

and lateral tectal surfaces, but thickens to form a

deep neuropil ventrally. At about the mid-tectal

level, the tectum remains small and thin. The

thick appearance of the white matter is no longer

apparent, but the ventrolateral portion of the tectum

makes an acute angle (Fig. 4J). The rostral

portions of the torus longitudinales are present.

The rostral torus semicircularis is flattened

along its dorsal surface—it protrudes very little

into the tectal ventricle (Fig. 4K). Caudally, the

torus semicirculares form narrow lobes that project

deeply into the tectal ventricle (Fig. 4L–N).

Motor neurons of the oculomotor complex are

large but sparse at about the midtectal level (Fig.

4L). At the level of oculomotor nerve exit (Fig. 4M)

oculomotor nuclei are numerous. Farther caudally

(Fig. 4N) they are again less numerous but clustered,

and positioned immediately dorsal to the

medial longitudinal fasciculus.

Cerebellum. At its rostral-most level the valvula

cerebellum is single lobed, consisting of a

central molecular layer and lateral granule cell

regions (Fig. 4L). Just caudally, at the level of oculomotor

nerve exit (Fig. 4M), the valvula consists

of two large, stacked lobes, which caudally become

broader, with lobules separated dorsoventrally—a

morphology that does not appear to be artifact

and that we have not seen before (Fig. 4N). The

rostral corpus cerebellum is tall, comprising more

than 50% of the dorsal extent of the brain at the

level of the rostral rhombencephalon (Fig. 4O,P).

Farther caudally, the corpus becomes broad (Fig.

4P,Q); the eminentia granulares appear as large

lateral granule cell masses (Fig. 4Q). At the point

where it becomes a lobe, the corpus and the vestibulolateral

lobe are large and well differentiated;

the crista cerebellaris is large (Fig. 4R). As it

forms a lobe, the corpus is large, with about the

Journal of Morphology DOI 10.1002/jmor

same cross-sectional area as the brainstem proper

(Fig. 4S).

Rhombencephalon. The brainstem of Eleginops

is typically proportioned. Rostrally, neurons

of the trigeminal motor nuclei are prominent (Fig.

4O–Q). The rostral portions of the crista cerebellares

are large (Fig. 4R) and at the level of the

mid-fourth ventricle form a decussation (Fig. 4S).

At the level of the caudal rhombencephalon, the

fourth ventricle is again open dorsally, the crista

cerebellares become small, and the sensory nuclei

of the vagal nerve are present (Fig. 4T). At this

level, subependymal expansions (arrows) are

prominent and contain cell bodies and axons.

At the level of the brainstem junction with the

spinal cord, the spinal sensory nuclei are moderately

sized (Fig. 4U). Subependymal expansions

are prominent and form a septum below the central

canal. The rostral spinal cord is narrower dorsally

than it is ventrally; motor neurons are large

(Fig. 4V).

Sensory Systems

Visual system

Eye size. At 11%–13% of head length (HL) or 3%

of SL, the eye diameter of Eleginops maclovinus

(Figs. 2 and 7A) is about twofold smaller than in

many other notothenioids. For comparison, eye diameter

of the artedidraconid Dolloidraco longedorsalis

is 31–37% of HL, bathydraconids are 16–31%,

and channichthyids are 19–22% (Eastman and

Lannoo, 2003a,b, 2004).

Ocular vasculature. The generalized teleostean

eye (Walls, 1942) as well as the phyletically basal

notothenioid eye, exemplified by Bovichtus diacanthus

(Eastman, 2006; Eastman and Lannoo, 2007),

possess three ocular vascular structures supplying

the retina and ocular adnexa: the choroid rete mirabile,

the lentiform body (also a rete), and the falciform

process. In Eleginops maclovinus the embryonic

choroid fissure is closed and therefore the

falciform process is not present (Fig. 5A). There is

a well-developed choroid rete (Fig. 5B) but this

was not filled by our ventral aortic perfusions of

Microfil because the perfusate is unable to pass

distal to the capillary bed of the pseudobranch.

The ophthalmic artery, a vessel originating in the

pseudobranch, supplies the choroid rete. The eye

of Eleginops also receives blood from a second vessel,

the optic artery (60 lm diameter). This vessel,

a branch of the carotid complex, is the afferent

supply to the lentiform body and was filled by

Microfil (Fig. 5C). The lentiform body, located ventral

to the optic nerve (Fig. 5B,C), is a small complex

(1.2 mm by 0.5 mm) of two to three orders of

short, small diameter (15 lm) arterial capillaries.

Since the venous capillaries are extrinsic and part

of the general choriocapillaris network, they were

not filled by Microfil. The falciform artery (also


BRAIN AND SENSE ORGANS OF ELEGINOPS MACLOVINUS 93

Fig. 5. Ocular vascular structures and retinal histology of Eleginops maclovinus. A: After removal of cornea and lens, vitreous

chamber of left eye shows falciform artery (containing yellow Microfil) at the optic disk continuing as the main vessel to the retractor

lentis muscle. The main vessel is superficial to the site of the fused choroid fissure. Hyaloid arteries are absent at the vitreoretinal

interface. B: Removal of sclera and argentea from back of left eye displays choroid rete mirabile (unfilled) and lentiform body (filled

with Microfil). C: Enlargement of B showing detail of arterial vasculature of lentiform body. Optic artery is the afferent vessel and falciform

artery the efferent vessel. D, E: Transverse histological sections showing predominance of cone photoreceptors and layering of

central retina. Stains: D, Gomori; E, Bodian. Magnifications: A, 36.7; B, 34.5; C, 315.6; D, E, 3175. cc, choriocapillaris; cr, choroid

rete; fa, falciform artery; lb, lentiform body; mv, main vessel; oa, optic artery; ocn, oculomotor nerve; od, optic disk; on, optic nerve; r,

retina; rl, retractor lentis muscle; 1, retinal pigment epithelium; 2, outer segments of photoreceptors; 3, inner segments of photoreceptors;

4, external limiting membrane; 5, external nuclear layer; 6, internal nuclear layer; 7, ganglion cell layer; 8, optic nerve fibers.

60 lm diameter) is the efferent vessel of the lentiform

body (Fig. 5C); it enters the optic nerve and

continues into the vitreous chamber of the eye as

the main vessel (31–38 lm diameter) supplying

blood to the retractor lentis muscle (Fig. 5A). This

vessel is occasionally double. Microfil preparations

Journal of Morphology DOI 10.1002/jmor


94 J.T. EASTMAN AND M.J. LANNOO

TABLE 1. Cell counts a in the central area of the retina comparing Eleginops maclovinus with members of

other notothenioid families both non-Antarctic and Antarctic

Species

Habitat

depth b

(m)

Retinal

thickness

(lm) Cones Rods

Cones 1

rods

Ratio

cones:rods c

Cells in

internal

nuclear

layer

Ganglion

cells

Convergence

ratio (cones 1

rods:ganglion

cells) d

Bovichtidae (non-Antarctic)

Bovichtus diacanthus 1–20 200–250 13 350 363 1:27 103 8 45:1

B. variegatus 0–50 241 20 288 308 1:14 63 13 24:1

Cottoperca gobio 100–310 300 5 239 244 1:48 93 5 49:1

Eleginopidae (non-Antarctic)

Eleginops maclovinus 1–100 250–275 14 184 198 1:14 102 14 14:1

Nototheniidae (non-Antarctic)

Notothenia angustata 0–100 246 19 132 151 1:7 47 9 17:1

N. microlepidota


BRAIN AND SENSE ORGANS OF ELEGINOPS MACLOVINUS 95

Fig. 6. Retinal histology and olfactory anatomy and histology of Eleginops maclovinus. A: Enlargement of Figure 5D showing

detail of photoreceptors. Ellipsoids of cone inner segments stain red and outer segments light orange with Gomori’s trichrome. Thin

myoids of inner segments of rods are basophilic and located between cones. B: Dorsolateral view of left nasal sac, rosette, and olfactory

lamellae of a 39 cm SL specimen. Arrows indicate communications between nasal sac and dorsal and ventral accessory nasal

sacs. Anterior is to the left. C, D: Transverse section of olfactory lamellus showing nature of epithelium and large fasciculi of the olfactory

nerve in the connective tissue core of the lamellus. E, F: Olfactory epithelium on one side of lamellus showing cell types, especially

darkly stained nuclei of primary olfactory neurons in apical epithelium. Dendrites of primary olfactory neurons converge on

small fasciculi of the olfactory nerve in the basal epidermis. Stains: A,C,E, Gomori; D,F, Bodian. Magnifications: A, 31,100; B, 36.6;

C, D, 3140; E, F, 3630. b, bone of cephalic lateral line canal; bc, basal cells; cr, central raphe of olfactory rosette; ct, connective tissue;

d, dermis of head skin; dans, dorsal accessory nasal sac; e, epidermis of head skin; la, lamellae of olfactory rosette; muc, mucous

cells; n, nerves; ns, nasal sac; p, melanin pigment; pon, primary olfactory neurons; ro, rod (myoid); sc, supporting cells; sco, single

cone (ellipsoid); sk, head skin; tco, twin cone (ellipsoid); v, blood vessels; vans, ventral accessory nasal sac; 2, outer segments of rod

photoreceptors; 3, inner segments of rod photoreceptors; 4, external limiting membrane; 5, external nuclear layer.

and increase in number ontogenetically at the anterior

margin of the rosette (left portion of Fig.

6B). For example, a 15 cm SL specimen has 36–37

lamellae whereas a 43 cm SL specimen has 61–62.

Olfactory epithelium. Both sides of the lamellae

are faced with a pseudostratified columnar epithelium

(Fig. 6C,D) that is 50–65 lm thick but thins

to 25–50 lm in the non-olfactory area of the tips.

The core of the lamellae contains abundant fascicles

of olfactory nerve fibers and pigment cells

(Fig. 6C,D). This dark pigment is also grossly evident

in a surface view of the lamellae (Fig. 6B).

The olfactory epithelium lacks secondary folds and

consists of basal cells, supporting cells and,

although the entire cell is not evident, primary olfactory

neurons (Fig. 6E,F). The nuclei of these

Journal of Morphology DOI 10.1002/jmor


96 J.T. EASTMAN AND M.J. LANNOO

Fig. 7. Cephalic lateral line anatomy and histology of Eleginops maclovinus. A: Head showing small eyes and inconspicuousness

of bony lateral line canals, membranous tubules and pores. B: Lateral view of four of left infraorbital bones of alizarin-stained and

cleared specimen (SL 5 260 mm) showing the arrangement, size and degree of ossification of the bony canals. Since some of the

head skin is intact, origin of two membranous canals is evident (arrows). Membranous canals also originate from the three bony

canals on io1. Pores are not visible and situated peripherally at the ends of membranous canals. C: Transverse section of a bony infraorbital

canal includes longitudinal section of a membranous canal. The section through the bony canal is at the periphery of a

neuromast. Bone and scales stain red. D: Enlargement of longitudinal section of membranous canal from C showing location in the

dermis superficial to scales and the absence of bone and neuromasts. Stains: C,D, Gomori. Magnifications: A, 30.9; B, 33.2; C,

323; D, 370. b, bone of cephalic lateral line canal; bc, lumen of bony canal; ct, subcutaneous connective tissue; d, dermis of head

skin; e, epidermis of head skin; io, infraorbital bones; mc, membranous canal (canaliculus); n, nerve (to neuromast); nm, neuromast;

s, scale; sk, head skin.

neurons; however, are recognizable because they

are more apically located than are the nuclei of

the supporting cells (Hansen and Zielinski, 2005).

Furthermore, nuclei are larger and darker with a

denser pattern of chromatin (Fig. 6F), and their

axons are bundled together in the basal epithelium

(Fig. 6E). Mucous cells are located in the apical epithelium

(Fig. 6C,E).

Cephalic lateral line system. Since our specimens

of Eleginops maclovinus were subject to ab-

Journal of Morphology DOI 10.1002/jmor


BRAIN AND SENSE ORGANS OF ELEGINOPS MACLOVINUS 97

rasion during seining and the long transport back

to aquaria on the ship, we cannot comment definitively

on the number and distribution of superficial

neuromasts. A few are present on the dorsal

surface of the head in the interorbital and narial

areas, but they are probably not numerous. The

bony canals of the cephalic lateral line have the

typical actinopterygian pattern (Northcutt, 1989)

and specific descriptions are available for Eleginops

(Gosztonyi, 1979; Andersen, 1984). Based on

development and size, the bony canals of Eleginops

are most similar to the ‘‘simple 5 narrow’’ type in

the classification of Webb (1989). They are inconspicuous

on the surface of the head (Fig. 7A) and,

as exemplified by the infraorbital series, canal segments

are ossified with the exception of superficial

areas near their ends (Fig. 7B). In a 260 mm SL

specimen, they measure 0.7–0.9 mm diameter at

the center and 1.5–1.9 mm at the flared ends.

Some notothenioids, including Eleginops, possess

additional or secondary branches of the bony

canals in the form of membranous canals in the

dermis of the skin. These have been termed

‘‘canaliculi’’ in notothenioid systematic work (Jakubowski,

1971; Andersen, 1984; DeWitt et al., 1990).

They are straight and unbranched in Eleginops of

the size range that we examined, although it is

possible they become more complexly branched

during ontogeny as has been documented in a

number of groups including clupeids and bovichtids

(Stephens, 1985; Eastman and Lannoo, 2007).

Along the infraorbital canal, some of membranous

canals arise between and perpendicular to the

bony segments while others are continuous with

the bony canals (Fig. 7B). Membranous canals

have a lumen diameter of 0.4 mm at their origins

(Fig. 7B). The pores are situated at the ends of

membranous canals rather than between bony segments

of the main canal. Pores are small and

inconspicuous and some of those on the snout are

slit-like. Mandibular pores are 240–600 lm in diameter.

Histological transverse sections of the

region ventral to the eye show the deeply situated

bony infraorbital canal with a portion of a neuromast

as well as a longitudinal section through a

membranous canal (Fig. 7C). The latter is contained

in a meshwork of loose dermal collagen

fibers superficial to the scales and the denser basal

dermis (Fig. 7C,D). Membranous canals are lined

by a cuboidal epithelium containing numerous

mucous cells (Fig. 7D) and neuromasts are not

present.

DISCUSSION

Few Studies Have Addressed Brain

Variability in Perciforms

Perciforms are visual specialists with a welldeveloped

tectum (Demski, 2003) and, as exemplified

by coral reef fishes, their behavior and sensory

world are dominated by vision (McFarland, 1991).

Most habitats occupied by perciforms are relatively

shallow and well illuminated. Despite their speciosity

and prominence in many aquatic ecosystems,

surprisingly few surveys have focused on variability

in brain morphology among perciforms. In one

study, drawings of only three representative species

sufficiently encapsulated the variation in

brain morphology encountered in a survey of 17

species of pomacanthids (angelfishes) and 35 species

of chaetodontids (butterflyfishes), typical coral

reef fishes (Bauchot et al., 1989). As with many

perciforms, chaetodontids exhibit a telencephalon

with prominent lobation, and with tectal (visual),

corpus cerebellum (motor) and octavolateralis (auditory

and mechanoreceptive) areas well developed;

in contrast the olfactory bulbs are less robust.

In two other studies, among 189 cichlid species

from the three major African Great Lakes,

interspecific variation in brain regions is similar

among species from each of the lakes, with the

greatest variation in association areas such as the

telencephalon, followed by the regions responsible

for mechanoreception, olfaction, and vision (van

Staaden et al., 1994/95; Huber et al., 1997).

Brain and Sense Organ Morphology in

Non-Antarctic Eleginops maclovinus

Compared with Antarctic Notothenioids

Except for the shape of the corpus cerebellum, a

highly variable feature among teleosts (Meek and

Nieuwenhuys, 1998), and enhanced development

of olfactory areas, the brain of Eleginops maclovinus

is not substantially different from the brains

of the temperate and tropical perciforms mentioned

earlier. Nor is the brain of Eleginops fundamentally

different than that of the moronid Dicentrarchus

labrax (Mediterranean sea bass), another

marine perciform (Cerdá-Reverter et al., 2001a,b).

Because Eleginops is the sister group of the Antarctic

notothenioids, the neural starting point for

the notothenioid radiation appears to have been a

‘‘normal (typical)’’ perciform brain.

Our work to date has focused on the brains and

sense organs of the phyletically basal non-Antarctic

bovichtids (Eastman and Lannoo, 2007) and of

four of the five phyletically derived Antarctic families—Artedidraconidae,

Harpagiferidae, Bathydraconidae,

and Channichthyidae (Eastman and Lannoo,

2003a,b, 2004). Eleginops maclovinus provides

the final piece of the puzzle in interpreting the

neural and sensory morphology of notothenioids.

Do the brains and sense organs of Antarctic notothenioids

differ from those of their non-Antarctic

sister group? With Eleginops as the reference for

the ancestral state, we will note departures in the

anatomy and histology of the major brain divisions

and associated cranial nerves and sensory systems

in members of the Antarctic clade.

Journal of Morphology DOI 10.1002/jmor


98 J.T. EASTMAN AND M.J. LANNOO

Olfactory bulb, nerves, and olfactory lamellae.

The olfactory bulbs receive their primary olfactory

input as well as ascending input from telencephalic

regions (Meek and Nieuwenhuys, 1998,

p. 903). Compared with the phyletically basal

bovichtids, the olfactory components in Eleginops

maclovinus are larger. Thus, a well-developed olfactory

system appears to be the ancestral state

for the Antarctic clade. The proximal swelling or

expansion of the olfactory nerve, seen in Eleginops

but not in bovichtids, is also ancestral. This welldeveloped

olfactory morphology persists in many

notothenioids, most notably in members of the

nototheniid genera Dissostichus and Trematomus.

The olfactory system is reduced in one notothenioid

clade, the bathydraconid tribe Bathydraconini.

In adult notothenioids, the number of olfactory

lamellae peaks at 50–55 in Eleginops, falls off to

counts in the forties for many nototheniids and in

the twenties in many bathydraconids, and reaches

lows in the teens in some artedidraconids. In the

channichthyids, lamellar number remains high or

is secondarily enhanced at 30–50. Lamellar number

increases ontogenetically in notothenioids. It is

also highly variable among perciform species

(Yamamoto, 1982; Hansen and Zielinski, 2005).

There is no simple relationship between lamellar

number or arrangement and olfactory acuity in teleosts

since primary olfactory neurons are distributed

in various patterns, some of which are irregular,

within the olfactory epithelium (Yamamoto,

1982).

Little is known about the role of olfaction and

the other chemical senses in the lives of notothenioids.

Some species are attracted to baited traps

in the field (personal observation) and the nototheniid

Trematomus newnesi is sensitive to amphipod

extract introduced to aquarium tanks (Meyer and

Fanta, 1998). Through experimentation and computer

simulation, it has been demonstrated that

the nototheniid Trematomus bernacchii is capable

of following an odor plume, but only by combining

chemosensory with rheotactic information (Montgomery

et al., 1999).

Telencephalic lobation and complexity. The

telencephalon is a multimodal center receiving a

variety of sensory input. For example, the dorsal

medial subdivision receives auditory and gustatory

input, the dorsal lateral subdivision receives auditory,

lateral line, visual, and olfactory input

(Northcutt, 2006 for summary) and the dorsal posterior

subdivision receives substantial olfactory

projections (Northcutt, 2006). The telencephalon

also processes and integrates this complex of sensory

and sensorimotor components (Demski, 2003).

The telencephalon is well-developed and distinctly

lobulated in bovichtids and Eleginops maclovinus,

and this lobulation has been maintained in the

Antarctic clade, with a slight dimunition in size

Journal of Morphology DOI 10.1002/jmor

seen in some deep-living artedidraconids and bathydraconids

of the tribe Bathydraconini.

Diencephalon, subependymal expansions,

and saccus vasculosus. At the time of our original

descriptions (Eastman and Lannoo, 1995; Lannoo

and Eastman, 1995), subependymal expansions

were only known from notothenioids. We

have since found them in the non-notothenioid

Liparidae (Scorpaeniformes; Eastman and Lannoo,

1998), in the Muraenolepididae (Gadiformes; Eastman

and Lannoo, 2001), and in the Zoarcidae

(Perciformes; Lannoo and Eastman, 2006). Subependymal

expansions have also been found in the

telencephalon of the Mediterranean sea bass

(Cerdá-Reverter et al., 2001a).

The saccus vasculosus, a thin-walled circumventricular

organ, heavily vascularized, dense with

CSF-contacting neurons, and connected to the

hypothalamus, is also highly variable in size

among teleosts, even among closely related genera

(Meek and Nieuwenhuys, 1998, p. 895). While

both bovichtids (Eastman and Lannoo, 2007) and

Eleginops have a relatively small saccus, the saccus

is well-developed in the Antarctic clade

(Eastman and Lannoo, 1995, 2003a,b, 2004; Lannoo

and Eastman, 2000) and is best defined as

Type 3 in the classification of Tsuneki (1992).

Tectum of the mesencephalon, optic nerves,

and retinae. The midbrain tectum processes visual

information and is the primary target of the

retinal fibers. The tectum is also one of the main

sensorimotor integration centers in teleosts (Meek

and Nieuwenhuys, 1998, p. 863). It integrates visual

signals with sensory information from other

modalities to enable orientation tasks such as

object identification and localization, and coordinated

motor control (Meek and Nieuwenhuys,

1998, p. 863; Wullimann, 1998, p. 269). At the histological

level, the relative thicknesses of the six

tectal layers in notothenioids are similar to those

of other teleosts (Körtje et al., 1996). Large eyes, a

duplex retina, and a well-developed tectum are

characteristic of perciforms, including many notothenioids.

The eyes of Eleginops maclovinus are

small, but despite the seasonal absence of light,

eyes are large in most members of the Antarctic

clade. There is a phyletic trend toward loss of cellularity

in the retina, summarized for relatively

shallow living species in Table 1, but this is also

true for deep living species with rod dominated

retinae (Eastman and Lannoo, 2003a,b). This

trend is co-occurring with habitation of Antarctic

waters and, in some species, diversification into

slope waters to depths of 2,000 m. Retinae with

relatively few cones have independently evolved in

deep-dwelling species of the nototheniid genera

Dissostichus and Trematomus, the artedidraconid

Dolloidraco longedorsalis and the bathydraconids

Akarotaxis nudiceps and Vomeridens infuscipinnis.

It is noteworthy, however, that notothenioid reti-


BRAIN AND SENSE ORGANS OF ELEGINOPS MACLOVINUS 99

nae are devoid of the extreme specializations seen

in deep-sea fishes (Eastman, 1988; Pankhurst and

Montgomery, 1989) and, unlike true deep-water

non-perciforms, visual acuity in the nototheniid

Pagothenia borchgrevinki peaks at


100 J.T. EASTMAN AND M.J. LANNOO

fishes, those of artedidraconids lack taste buds.

However, as evidenced by large nerve trunks,

small nerve branches in the dermis and epidermis

and a lobed chief sensory nucleus of the trigeminal

nerve, the long barbel of Dolloidraco longedorsalis

may be sufficiently well innervated to serve as a

tactile organ, and thus supplement mechanosensory

information in detecting prey, which in this

species consists primarily of polychaetes (Eastman

and Lannoo, 2003a).

Other chemosensory systems (external

taste). External taste is not a hypertrophied sense

in perciforms or in notothenioids, at least in the

sense that the facial lobes of the brain are not

superficially prominent as in cyprinoids and gadiforms.

Because of abrasion, we could not determine

the distribution of taste buds in Eleginops

maclovinus, and nothing else is known about

them. In the nototheniid Trematomus newnesi and

the channichthyid Chaenocephalus aceratus taste

buds are present on the lips; T. newnesi also has

solitary chemosensory cells in the skin (Meyer and

Fanta, 1998; Fanta et al., 2003).

Stalking of the brain. The brains of some

members of the Antarctic clade have undergone a

reduction of the telencephalon, tectum, and corpus

cerebellum, sometimes to the extent that the brain

stem becomes ‘‘stalked,’’ revealing the underlying

axis of the brain between the telencephalon and

the tectum. This is most marked in the deep-living

artedidraconid Dolloidraco longedorsalis (Eastman

and Lannoo, 2003a) and in most of the deep-living

bathydraconid tribe Bathydraconini (Eastman and

Lannoo, 2003b). In some of these species (e.g., the

deep-living bathydraconids), expansion occurs in

mechanosensory areas.

Ocular vasculature. To satisfy the demand for

oxygen in the avascular retina, the teleostean eye

has a dual blood supply from an ophthalmic artery

derived from the pseudobranch and an optic artery

derived from the internal carotid (Nicol, 1989).

Compared with the generalized teleostean condition,

exemplified by bovichtids and to a lesser

extent by Eleginops maclovinus, there has been a

phyletic loss of vasculature in the notothenioid eye

(Eastman, 2006 for summary). For example, the

phyletically derived channichthyids have lost three

vascular structures—the choroid rete mirabile, the

lentiform body (also a rete) and the falciform process—and

the ophthalmic artery may be vestigal or

lost as well (Eastman and Lannoo, 2004). Thus,

the channichthyid retina is supplied by an optic

artery that branches at the optic disk into an

extensive series of hyaloid arteries at the vitreoretinal

interface, the densest pattern known in any

fish eye. This is not an adaptation, nor is it linked

with a special ocular function in channichthyids,

but rather it is a component of the overall cardiovascular

compensation necessary to offset the

losses of hemoglobin, myoglobin, and red blood

Journal of Morphology DOI 10.1002/jmor

cells, conditions that are also thought to be of no

adaptive value (Sidell and O’Brien, 2006).

Overview. Among the Antarctic notothenioids,

the most noteworthy departures from the ancestral

state of brain and sense organ morphology and

histology seen in Eleginops maclovinus are as follows.

These are usually, but not always, present in

the deepest living species. There is a reduction in

the cellularity of the retina but not a decrease in

eye size, and species have lost most cone photoreceptors.

Mechanosensation is expanded in some

species. The corpus cerebellum is the most variable

brain division, ranging from large and caudally

projecting to small and round. The deep-living

artedidraconids and bathydraconids have

‘‘stalked’’ brains showing reduction in the size of

the telencephalon, tectum, and corpus cerebellum.

The net result is a modest depth or deep-sea effect

also known in other fishes (these are not uniquely

‘‘Antarctic’’ attributes).

The sense organs and brain, as the notothenioids’

window on their environment, are probably

subject to strong selection pressure leading to

homoplastic similarity through parallelism and

reversals of character states. This reduces their

usefulness in phylogenetic analyses (Quickie,

1993, p. 32). The uncoupling of character state and

phylogeny is certainly evident in the retina of the

bathydraconid tribe Bathydraconini. This clade is

extremely susceptible to loss of cone photoreceptors

with habitat depth, with some lineages containing

deep and shallow-living sister species that

have and have not lost most cones, respectively

(Eastman and Lannoo, 2003b). The same is true in

the nototheniid genus Trematomus (Lannoo and

Eastman, 2000).

Differences Between Typical Perciform

and Notothenioid Habitats Require Some

Adaptations But Not Novel Sensory and

Neural Morphology

Environmental conditions on the Antarctic shelf

differ considerably from those experienced by perciforms

in other marine habitats. Water temperatures

are constantly 08C, producing an evolutionary

minimization of baseline energy costs as

reflected in a reduced scope for activity (Clarke

and Gaston, 2006; Pörtner, 2006). Many notothenioids

are inactive most of the time, with some

benthic species spending only 1.7% of each day

engaged in locomotion (North, 1996). Furthermore,

glacial erosion and isostasy have combined to produce

average shelf depths of 500 m, four times the

world average (Anderson, 1999), and the vertical

ranges of some notothenioids extend to upper slope

depths of nearly 3,000 m. These depths coupled

with extreme seasonality and ice cover at high latitudes

create a light-limited environment on the

Antarctic shelf. This is in some ways similar to the


BRAIN AND SENSE ORGANS OF ELEGINOPS MACLOVINUS 101

deep-sea (Montgomery and Pankhurst, 1997), but

is also the antithesis of a representative perciform

habitat. Deep, dark conditions, however, have not

been problematic for notothenioids, especially as

far as neural and sensory function are concerned.

A host of biochemical, organelle, and cellular adaptations,

not exhibited by the thousands of other

tropical and temperate perciform species, fine-tune

the excitable tissues of notothenioids for function

at low temperatures (Fields and Somero, 1998;

Kawall et al., 2002; Davison, 2005; DeVries and

Cheng, 2005; Macdonald and Montgomery, 2005;

Petricorena and Somero, 2007). But at the organ

system level, the morphology of the perciform

brain and sensory systems is suitable for conditions

on the Antarctic shelf, with only minor alterations

in structure in directions exhibited by other

fish groups inhabiting deep water. Unlike some of

the phyletically older primary and secondary deepsea

fishes that have evolved sensory specialties

(Montgomery and Pankhurst, 1997; Wagner, 2001,

2002), notothenioids retain a relative balance

among their array of senses. In other words, the

brains and sense organs of most notothenioids continue

to reflect their heritage as visually oriented,

inshore perciforms.

Antarctic notothenioids have colonized the low

diversity Antarctic shelf ecosystem relatively

recently (25 mya is a midrange estimate)

(Eastman, 2005). They moved into a new adaptive

zone containing few non-notothenioid fishes and it

is possible that under conditions of reduced competition

and in the absence of a true deep-sea

environment, there was no need for extreme neural

and sensory specialization. It is also possible

that the perciform genotype constrained the

extent of the response of brain and sensory systems

to life on the Antarctic shelf. Referring to

the radiations of perciform cichlids in the African

Great Lakes, Greenwood (1984, p. 149) noted that

relatively subtle morphological features are associated

with the diverse feeding habits characteristic

of this group, and concluded that ‘‘we seem to

have in these fishes evidence for an ecological revolution

brought about without a corresponding

morphological one.’’ With reference to their modest

neural and sensory diversification, the same

could be said of the overwhelming notothenioid

dominance of the high Antarctic shelf. In the case

of nervous and sensory systems, organismal diversity

is not accompanied by noteworthy organ system

diversity.

ACKNOWLEDGMENTS

We thank the captain, crew and personnel of

Raytheon Polar Services aboard the RVIB Nathaniel

B. Palmer for their excellent assistance during

this long cruise. We also thank Drs. Bruce Sidell

and Richard Eakin for collaborating on the Mircofil

and fixative perfusions during the cruise. We

are grateful to Danette Pratt for drawing and

assembling all figures. Susan Johnson Lannoo sectioned

and stained the brains, and proofread the

manuscript. Research was conducted under protocol

L01-14 as approved by the Institutional Animal

Care and Use Committee of Ohio University.

LITERATURE CITED

Anderson JB. 1999. Antarctic Marine Geology. Cambridge:

Cambridge University Press.

Andersen NC. 1984. Genera and subfamilies of the family Nototheniidae

(Pisces. Perciformes) from the Antarctic and Subantarctic.

Steenstrupia 10:1–34.

Arkhipkin AI, Grzebielec R, Sirota AM, Remeslo AV, Polishchuk

IA, Middleton DAJ. 2004. The influence of seasonal environmental

changes on ontogenetic migrations of the squid Loligo

gahi on the Falklands shelf. Fish Oceanogr 13:1–9.

Balushkin AV. 1992. Classification, phylogenetic relationships,

and origins of the families of the suborder Notothenioidei

(Perciformes). J Ichthyol 32:90–110.

Balushkin AV. 2000. Morphology, classification, and evolution of

notothenioid fishes of the Southern Ocean (Notothenioidei,

Perciformes). J Ichthyol 40 (Suppl 1):S74–S109.

Bargelloni L, Marcato S, Zane L, Patarnello T. 2000. Mitochondrial

phylogeny of notothenioids: A molecular approach to Antarctic

fish evolution and biogeography. Syst Biol 49:114–129.

Bauchot R, Ridet J-M, Bauchot ML. 1989. The brain organization

of butterflyfishes. Env Biol Fish 25:205–219.

Bellwood DR, Wainwright PC. 2002. The history and biogeography

of fishes on coral reefs. In: Sale PF, editor. Coral Reef

Fishes: Dynamics and Diversity in a Complex Ecosystem. San

Diego: Academic Press. pp 5–32.

Boschung HT Jr, Mayden RL. 2004. Fishes of Alabama. Washington:

Smithsonian Books.

Boulenger GA. 1900. A list of the fishes collected by Mr. Rupert

Vallentin in the Falkland Islands. Ann Mag Nat Hist (Ser 7)

6:52–54.

Brickle P, Arkhipkin AI, Shcherbich ZN. 2005a. Age and growth

in a temperate euryhaline notothenioid. Eleginops maclovinus

from the Falkland Islands. J Mar Biol Assoc UK 85:1217–

1221.

Brickle P, Laptikhovsky V, Arkhipkin A. 2005b. Reproductive

strategy of a primitive temperate notothenioid Eleginops

maclovinus. J Fish Biol 66:1044–1059.

Calvo J, Morriconi E, Rae GA, San Roman NA. 1992. Evidence

of protandry in a subantarctic notothenid. Eleginops maclovinus

(Cuv. & Val., 1830) from the Beagle Channel, Argentina.

J Fish Biol 40:157–164.

Cerdá-Reverter JM, Zanuy S, Muñoz-Cueto JA. 2001a.

Cytoarchitectonic study of the brain of a perciform species,

the sea bass (Dicentrarchus labrax). I. The telencephalon.

J Morphol 247:217–228.

Cerdá-Reverter JM, Zanuy S, Muñoz-Cueto JA. 2001b.

Cytoarchitectonic study of the brain of a perciform species,

the sea bass (Dicentrarchus labrax). II. The diencephalon.

J Morphol 247:229–251.

Chen L, DeVries AL, Cheng C-HC. 1997. Evolution of antifreeze

glycoprotein gene from a trypsinogen gene in Antarctic notothenioid

fish. Proc Natl Acad Sci USA 94:3811–3816.

Cheng C-HC, Chen L, Near TJ, Jin Y. 2003. Functional antifreeze

glycoprotein genes in temperate-water New Zealand

nototheniid fish infer an Antarctic evolutionary origin. Mol

Biol Evol 20:1897–1908.

Clarke A, Gaston KJ. 2006. Climate, energy and diversity. Proc

R Soc B 273:2257–2266.

Cousseau MB, Gosztonyi AE, Elías I, Ré ME. 2004. Estado

actual del conocimiento de los peces de la plataforma continental

Argentina yadyacencias. Mar Argentino Recur Pesqueros

4:17–38.

Journal of Morphology DOI 10.1002/jmor


102 J.T. EASTMAN AND M.J. LANNOO

Davis RE, Northcutt RG, editors. 1983. Fish Neurobiology, Vol.

2. Higher Brain Areas and Functions. Ann Arbor: University

of Michigan Press.

Davison W. 2005. Antarctic fish skeletal muscle and locomotion.

In: Farrell AP, Steffensen JF, editors. The Physiology of Polar

Fishes, Vol. 22. Fish Physiology. San Diego: Elsevier Academic

Press. pp 317–349.

Demski LS. 2003. In a fish’s mind’s eye: The visual pallium of

teleosts. In: Collin SP, Marshall NJ, editors. Sensory processing

in aquatic environments. New York: Springer-Verlag.

pp 404–419.

DeVries AL, Cheng C-HC. 2005. Antifreeze proteins and organismal

freezing avoidance in polar fishes. In: Farrell AP, Steffensen

JF, editors. The Physiology of Polar Fishes, Vol. 22,

Fish Physiology. San Diego: Elsevier Academic Press. pp 155–

201.

DeVries AL, Eastman JT. 1978. Lipid sacs as a buoyancy adaptation

in an Antarctic fish. Nature 271:352–353.

DeWitt HH, Heemstra PC, Gon O. 1990. Nototheniidae. In: Gon

O, Heemstra PC, editors. Fishes of the Southern Ocean. Grahamstown,

South Africa: J.L.B. Smith Institute of Ichthyology.

pp 279–331.

Eastman JT. 1988. Ocular morphology in Antarctic notothenioid

fishes. J Morphol 196:283–306.

Eastman JT. 1993. Antarctic fish biology: Evolution in a unique

environment. San Diego: Academic Press.

Eastman JT. 2005. The nature of the diversity of Antarctic

fishes. Polar Biol 28:93–107.

Eastman JT. 2006. Aspects of the morphology of phyletically basal

bovichtid fishes of the Antarctic suborder Notothenioidei

(Perciformes). Polar Biol 29:754–763.

Eastman JT, Hubold G. 1999. The fish fauna of the Ross Sea.

Antarctica. Antarct Sci 11:293–304.

Eastman JT, Lannoo MJ. 1995. Diversification of brain morphology

in Antarctic notothenioid fishes: Basic descriptions

and ecological considerations. J Morphol 223:47–83.

Eastman JT, Lannoo MJ. 1998. Morphology of the brain and

sense organs in the snailfish Paraliparis devriesi: Neural convergence

and sensory compensation on the Antarctic shelf.

J Morphol 237:213–236.

Eastman JT, Lannoo MJ. 2001. Anatomy and histology of the

brain and sense organs of the Antarctic eel cod Muraenolepis

microps (Gadiformes; Muranolepidae). J Morphol 250:34–50.

Eastman JT, Lannoo MJ. 2003a. Anatomy and histology of the

brain and sense organs of the Antarctic plunderfish Dolloidraco

longedorsalis (Perciformes: Notothenioidei: Artedidraconidae),

with comments on the brain morphology of other artedidraconids

and closely related harpagiferids. J Morphol 255:

358–377.

Eastman JT, Lannoo MJ. 2003b. Diversification of brain and

sense organ morphology in Antarctic dragonfishes (Perciformes:

Notothenioidei: Bathydraconidae). J Morphol 258:

130–150.

Eastman JT, Lannoo MJ. 2004. Brain and sense organ anatomy

and histology in hemoglobinless Antarctic icefishes (Perciformes:

Notothenioidei: Channichthyidae). J Morphol 260:

117–140.

Eastman JT, Lannoo MJ. 2007. Brain and sense organ anatomy

and histology of two species of phyletically basal non-Antarctic

thornfishes of the Antarctic suborder Notothenioidei (Perciformes:

Bovichtidae). J Morphol 268:485–503.

Falkland Islands Government. 2003. The Falkland Mullet Eleginops

maclovinus: Biology and Fishery in Falkand Islands’

Waters. Stanley, Falkland Islands: Scientific Report, Fisheries

Department, Falkland Islands Government. 64 p.

Fanta E, Donatti L, Romão S, Vianna ACC, Zaleski T. 2003.

Food detection and the morphology of some sensory organs in

the Antarctic blackfin icefish Chaenocephalus aceratus Lönnberg,

1906. In: Huiskes AHL, Gieskes WWC, Rozema J,

Schorno RML, van der Vies SM, Wolff WJ, editors. Antarctic

Biology in a Global Context. Leiden: Backhuys. pp 107–112.

Fenaughty JM. 2006. Geographical differences in the condition,

reproductive development, sex ratio and length distribution of

Antarctic toothfish (Dissostichus mawsoni) from the Ross Sea.

Antarctica (CCAMLR Subarea 88.1). CCAMLR Sci 13:27–45.

Fernández DA, Calvo J, Johnston IA. 1999. Characterisation of

the swimming muscles of two Subantarctic notothenioids. Sci

Mar 63 (Suppl 1):477–484.

Fernández DA, Calvo J, Wakeling JM, Vanella FA, Johnston IA.

2002. Escape performance in the sub-Antarctic notothenioid

fish Eleginops maclovinus. Polar Biol 25:914–920.

Fields PA, Somero GN. 1998. Hot spots in cold adaptation:

Localized increases in conformational flexibility in lactate dehydrogenase

A 4 orthologs of Antarctic notothenioid fishes.

Proc Natl Acad Sci USA 95:11476–11481.

Gon O, Heemstra PC, editors. 1990. Fishes of the Southern

Ocean. Grahamstown, South Africa: J.L.B. Smith Institute of

Ichthyology.

Gosztonyi AE. 1979. Biologia del ‘‘Robalo’’ (Eleginops maclovinus

Cuv. & Val., 1830). Buenos Aires, Argentina: Tesis Doctoral,

Universidad Nacional de Buenos Aires. 129 p.

Greenwood PH. 1984. African cichlids and evolutionary theories.

In: Echelle AA, Kornfield I, editors. Evolution of fish species

flocks. Orono: University of Maine at Orono Press.

pp 141–154.

Hansen A, Zielinski BS. 2005. Diversity in the olfactory epithelium

of bony fishes: Development, lamellar arrangement, sensory

neuron cell types and transduction components. J Neurocytol

34:183–208.

Hart TJ. 1946. Report on trawling surveys on the Patagonian

continental shelf. Discov Rep 23:223–408.

Huber R, van Staaden MJ, Kaufman LS, Liem KF. 1997. Microhabitat

use, trophic patterns, and the evolution of brain

structure in African cichlids. Brain Behav Evol 50:167–182.

Jakubowski M. 1971. Morphological features of the lateral-line

organs in members of the genus Notothenia Rich and other

genera of the family Nototheniidae (Pisces). J Ichthyol

11:493–499.

Janssen J. 1996. Use of the lateral line and tactile senses in

feeding in four Antarctic nototheniid fishes. Environ Biol Fish

47:51–64.

Jenkins RE, Burkhead NM. 1994. Freshwater fishes of Virginia.

Bethesda: American Fisheries Society.

Kawall HG, Torres JJ, Sidell BD, Somero GN. 2002. Metabolic

cold adaptation in Antarctic fishes: Evidence from enzymatic

activities of brain. Mar Biol 140:279–286.

Kiernan JA. 1990. Histological and histochemical methods:

Theory and practice, 2nd ed. Oxford: Pergamon Press.

Kocher TD. 2004. Adaptive evolution and explosive speciation:

The cichlid fish model. Nat Rev Genet 5:288–298.

Kornfield I, Smith PF. 2000. African cichlid fishes: Model systems

for evolutionary biology. Annu Rev Ecol Syst 31:163–

196.

Körtje K-H, Aich B, Lips K, Rahmann H. 1996. Cellular substructures

in the optic tectum of Antarctic and temperate

fish. J Zool (Lond) 238:333–350.

Lannoo MJ, Eastman JT. 1995. Periventricular morphology in

the diencephalon of Antarctic notothenioid teleosts. J Comp

Neurol 361:95–107.

Lannoo MJ, Eastman JT. 2000. Nervous and sensory system

correlates of an epibenthic evolutionary radiation in Antarctic

notothenioid fishes, genus Trematomus (Perciformes; Nototheniidae).

J Morphol 245:67–79.

Lannoo MJ, Eastman JT. 2006. Brain and sensory organ morphology

in Antarctic eelpouts (Perciformes: Zoarcidae: Lycodinae).

J Morphol 267:115–127.

Larsell O, Jansen J. 1972. The Comparative Anatomy and Histology

of the Cerebellum. Minneapolis: University of Minnesota

Press.

Licandeo RR, Barrientos CA, González MT. 2006. Age, growth

rates, sex change and feeding habits of notothenioid fish Eleginops

maclovinus from the central-southern Chilean coast.

Environ Biol Fish 77:51–61.

Macdonald J, Montgomery J. 2005. The nervous system. In:

Farrell AP, Steffensen JF, editors. The Physiology of Polar

Journal of Morphology DOI 10.1002/jmor


BRAIN AND SENSE ORGANS OF ELEGINOPS MACLOVINUS 103

Fishes, Vol. 22, Fish Physiology. San Diego: Elsevier Academic

Press. pp 351–383.

McCormick CA. 1989. Central lateral line mechanosensory

pathways in bony fish. In: Coombs S, Görner P, Münz H, editors.

The Mechanosensory Lateral Line: Neurobiology and

Evolution. New York: Springer-Verlag. pp 341–364.

McDowall RM. 1988. Diadromy in fishes: Migrations between

freshwater and marine environments. London: Croom Helm.

308 p.

McFarland WN. 1991. The visual world of coral reef fishes. In:

Sale PF, editor. The Ecology of Fishes on Coral Reefs. San

Diego: Academic Press. pp 16–38.

Meek J, Nieuwenhuys R. 1998. Holosteans and teleosts. In:

Nieuwenhuys R, ten Donkelaar HJ, Nicholson C, editors. The

Central Nervous System of Vertebrates, Vol. 2. Berlin and

Heidelberg: Springer-Verlag. pp 759–937.

Meyer AA, Fanta E. 1998. Morpho-functional study of chemosensory

structures of the Antarctic fish Trematomus newnesi

Boulenger, 1902 used for food detection and selection. Pes

Qantárt Bras 3:49–63.

Montgomery JC. 1997. An ontogenetic shift in the use of visual

and non-visual senses in Antarctic notothenioid fishes. In:

Battaglia B, Valencia J, Walton DWH, editors. Antarctic Communities:

Species, Structure and Survival. Cambridge: Cambridge

University Press. pp 217–220.

Montgomery JC, Bodznick D. 1994. An adaptive filter that cancels

self-induced noise in the electrosensory and lateral line

mechanosensory systems of fish. Neurosci Lett 174:145–148.

Montgomery JC, Macdonald JA. 1987. Sensory tuning of lateral

line receptors in Antarctic fish to the movements of planktonic

prey. Science 235:195–196.

Montgomery J, Pankhurst N. 1997. Sensory physiology. In:

Randall DJ, Farrell AP, editors. Deep-sea Fishes, Vol. 16,

Fish Physiology. San Diego: Academic Press. pp 325–349.

Montgomery JC, Sutherland KBW. 1997. Sensory development

of the Antarctic silverfish Pleuragramma antarcticum: A test

for the ontogenetic shift hypothesis. Polar Biol 18:112–115.

Montgomery JC, Macdonald JA, Housley GD. 1988. Lateral line

function in an antarctic fish related to the signals produced

by planktonic prey. J Comp Physiol A 163:827–833.

Montgomery JC, Pankhurst NW, Foster BA. 1989. Limitations

on visual food-location in the planktivorous Antarctic fish

Pagothenia borchgrevinki. Experientia 45:395–397.

Montgomery JC, Foster BA, Milton RC, Carr E. 1993. Spatial

and temporal variations in the diet of nototheniid fish in

McMurdo Sound. Antarctica. Polar Biol 13:429–431.

Montgomery JC, Diebel JC, Halstead MBD, Downer J. 1999.

Olfactory search tracks in the Antarctic fish Trematomus bernacchii.

Polar Biol 21:151–154.

Near TJ. 2004. Estimating divergence times of notothenioid

fishes using a fossil-calibrated molecular clock. Antarct Sci

16:37–44.

Near TJ, Pesavento JJ, Cheng C-HC. 2004. Phylogenetic investigations

of Antarctic notothenioid fishes (Perciformes: Notothenioidei)

using complete gene sequences of the mitochondrial

encoded 16S rRNA. Mol Phylogenet Evol 32:881–891.

Nelson JS. 2006. Fishes of the World, 4th ed. Hoboken: John

Wiley & Sons.

Nicol JAC. 1989. The Eyes of Fishes. Oxford: Oxford University

Press.

North AW. 1996. Locomotory activity and behaviour of the Antarctic

teleost Notothenia coriiceps. Mar Biol 126:125–132.

Northcutt RG. 1989. The phylogenetic distribution and innervation

of craniate mechanoreceptive lateral lines. In: Coombs S,

Görner P, Münz H, editors. The Mechanosensory Lateral

Line: Neurobiology and Evolution. New York: Springer-Verlag.

pp 17–78.

Northcutt RG. 2006. Connections of the lateral and medial divisions

of the goldfish telencephalic pallium. J Comp Neurol

494:903–943.

Northcutt RG, Bemis WE. 1993. Cranial nerves of the coelacanth,

Latimeria chalumnae [Osteichthyes: Sarcopterygii:

Actinistia], and comparisons with other Craniata. Brain

Behav Evol 42 (Suppl 1):1–76.

Northcutt RG, Davis RE, editors. 1983. Fish Neurobiology, Vol.

1, Brain Stem and Sense Organs. Ann Arbor: University of

Michigan Press.

O’Grady SM, Clarke A, DeVries AL. 1982. Characterization of

glycoprotein antifreeze biosynthesis in isolated hepatocytes

from Pagothenia borchgrevinki. J Exp Zool 220:179–189.

Ojeda FP, Labra FA, Muñoz AA. 2000. Biogeographic patterns

of Chilean littoral fishes. Rev Chilena Hist Nat 73:625–641.

Pankhurst NW, Montgomery JC. 1989. Visual function in four

Antarctic nototheniid fishes. J Exp Biol 142:311–324.

Pankhurst NW, Montgomery JC. 1990. Ontogeny of vision in

the Antarctic fish Pagothenia borchgrevinki (Nototheniidae).

Polar Biol 10:419–422.

Pavés H, Pequeño G, Bertrán C, Vargas L. 2005. Limnetic feeding

in Eleginops maclovinus (Valenciennes, 1930) in the Valdivia

River. Chile. Interciencia 30:120–125.

Pequeño G. 1981. Los peces de las riberas estuariales del rio

Lingue. Mehuin, Chile. Cah Biol Mar Roscoff 22:141–163.

Pequeño G. 1989. The geographical distribution and taxonomic

arrangement of South American nototheniid fishes (Osteichthyes.

Nototheniidae). Bol Soc Biol Concepción, Chile 60:183–

200.

Petricorena ZLC, Somero GN. 2007. Biochemical adaptations of

notothenioid fishes: Comparisons between cold temperate

South American and New Zealand species and Antarctic species.

Comp Biochem Physiol 147A:799–807.

Pörtner HO. 2006. Climate-dependent evolution of Antarctic

ectotherms: An integrative analysis. Deep-Sea Res II 53:

1071–1104.

Quickie DLJ. 1993. Principles and Techniques of Contemporary

Taxonomy. Glasgow: Blackie.

Seehausen O. 2006. African cichlid fish: A model system in

adaptive radiation research. Proc R Soc B 273:1987–1998.

Sidell BD, O’Brien KM. 2006. When bad things happen to good

fish: The loss of hemoglobin and myoglobin expression in Antarctic

icefishes. J Exp Biol 209:1791–1802.

Springer VG, Johnson GD. 2000. Use and advantages of ethanol

solution of alizarin red S dye for staining bone in fishes.

Copeia 1:300–301.

Stephens RR. 1985. The lateral line system of the gizzard shad.

Dorosoma cepedianum Lesueur (Pisces: Clupeidae). Copeia

3:540–556.

Taylor WR. 1967. An enzyme method of clearing and staining

small vertebrates. Proc US Nat Mus 122:1–17.

Tsuneki K. 1992. A systematic survey of the occurrence of the

hypothalamic saccus vasculosus in teleost fish. Acta Zool

73:67–77.

Vanella FA, Calvo J. 2005. Influence of temperature, habitat

and body mass on routine metabolic rates of Subantarctic teleosts.

Sci Mar 69 (Suppl 2):317–323.

van Staaden MJ, Huber R, Kaufman LS, Liem KF. 1994/95.

Brain evolution in cichlids of the African Great Lakes: brain

and body size, general patterns, and evolutionary trends.

Zool-Anal Complex Syst 98:165–178.

Wagner H-J. 2001. Brain areas in abyssal demersal fishes.

Brain Behav Evol 57:301–316.

Wagner H-J. 2002. Sensory brain areas in three families of

deep-sea fish (slickheads, eels and grenadiers): Comparison of

mesopelagic and demersal species. Mar Biol 141:807–817.

Walls GL. 1942. The vertebrate eye and its adaptive radiation.

Bloomfield Hills: Cranbrook Institute of Science Bulletin No.

19.

Webb JF. 1989. Gross morphology and evolution of the mechanoreceptive

lateral-line system in teleost fishes. Brain Behav

Evol 33:34–53.

Wullimann MF. 1998. The central nervous system. In: Evans

DH, editor. The Physiology of Fishes, 2nd ed. Boca Raton:

CRC Press. pp 245–282.

Yamamoto M. 1982. Comparative morphology of the peripheral

olfactory organ in teleosts. In: Hara TJ, editor. Chemoreception

in Fishes. Amsterdam: Elsevier. pp 39–59.

Journal of Morphology DOI 10.1002/jmor

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