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: firstname.lastname@example.org
Published online 27 September 2007 in
Wiley InterScience (www.interscience.wiley.com)
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
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
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).
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
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
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.
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
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
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
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
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
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
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
(lm) Cones Rods
ratio (cones 1
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
Eleginops maclovinus 1–100 250–275 14 184 198 1:14 102 14 14:1
Notothenia angustata 0–100 246 19 132 151 1:7 47 9 17:1
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
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
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,
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,
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
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
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
Differences Between Typical Perciform
and Notothenioid Habitats Require Some
Adaptations But Not Novel Sensory and
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,
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
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.
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