swim bladder coelacanth-axelrod

THE HISTOLOGICAL STRUCTURE OF THE

CALCIFIED LUNG OF THE FOSSIL COELACANTH

AXELRODICHTHYS ARARIPENSIS (ACTINISTIA:

MAWSONIIDAE)

by PAULO M. BRITO*� , FRANCOIS J. MEUNIER� , GAEL CLEMENT� and

DIDIER GEFFARD-KURIYAMA�*Departamento de Zoologia, Universidade do Estado do Rio de Janeiro. Rua Sao Francisco Xavier 524, Maracana, 20559-900, Rio de Janeiro, Brazil;

e-mail [email protected]

�UMR CNRS 7208 ‘BOREA’, Departement des Milieux et Peuplements aquatiques, Museum national d’Histoire natuelle, CP26, 43 rue Cuvier, 75231 Paris Cedex

05, France; e-mail [email protected]

�UMR CNRS 7207, Departement Histoire de la Terre, Museum national d’Histoire naturelle (MNHN), CP 38, 57 rue Cuvier, F-75231 Paris Cedex 05, France;

e-mails [email protected], [email protected]

Typescript received 19 July 2009; accepted in revised form 7 September 2009

Abstract: The palaeohistological study of the calcified

internal organ of Axelrodichthys araripensis Maisey, 1986, a

coelacanthiform from the Lower Cretaceous of Brazil (Crato

(Aptian) and Santana (Albian) formations of the Araripe

Basin), shows that the walls of this organ consist of osseous

blades of variable thickness separated from each other by the

matrix. This indicates that, in the living individuals, the walls

were reinforced by ossified plates, probably separated by con-

junctive tissue. This calcified sheath present in Axelrodichthys,

as well as in other fossil coelacanths, lies in ventral position

relative to the gut and its single anterior opening is located

under the opercle, suggesting a direct connection with the

pharynx or the oesophagus. The calcified organ of Axelrod-

ichthys, like that of other fossil coelacanths, is here regarded

as an ‘ossified lung’ and compared with the ‘fatty lung’ of

the extant coelacanth Latimeria. The reinforcement of the

pulmonary walls by the overlying osseous blades could be

interpreted as a means of adapting volumetric changes in the

manner of bellows, a necessary function for ventilation in

pulmonary respiration. Other functional hypotheses such as

hydrostatic and ⁄ or acoustic functions are also discussed.

Key words: calcified lung, fatty lung, palaeohistology, Axel-

rodichthys, Latimeria.

F ossil coelacanths are known since 1822, when the pal-

aeontologist G. Mantell described the genus Macropoma

from the Upper Cretaceous of Sussex, England (Agassiz

1839). Subsequently, many species have been referred to

this group of sarcopterygians, now known to have a tem-

poral range from the Devonian to the Recent (Forey and

Cloutier 1991; Forey 1998).

Among the differences between the extant coelacanth

Latimeria and most fossil, coelacanths is the presence, in

the fossils, of a visceral calcified structure currently

named in literature as ‘bladder’ (e.g. Woodward 1891).

This structure is known in the Palaeozoic genera Coel-

acanthus, Caridosuctor, Rhabdoderma, Hadronector and in

the Mesozoic genera Axelrodichthys, Mawsonia, Macrop-

oma, Undina, Coccoderma, Lybis, Laugia, Swenzia, and

Piveteauia. The Carboniferous genera Allenypterus and

Polyosteorhynchus also present a calcified bladder (Lund

and Lund 1985) (contrary to a previous assumption of

one of us (Clement 2005)). The condition (either absence

or presence of a calcified organ) is unknown in all other

coelacanth taxa. Nevertheless, it seems to be absent in the

two well-preserved Mesozoic genera Whiteia and Diplurus.

Although Whiteia is very common in the Triassic nodules

of Madagascar, none of the studied specimens show any

trace of calcified internal organ, whereas the rare genera

Piveteauia and Coelacanthus, from the same localities, do

possess such an organ. When entirely preserved, this cal-

cified organ occupies the length of the abdominal cavity,

reaching back as far as the pelvic fins (Text-fig. 1A).

Latimeria possesses a tubular, fat-filled organ (about 4 cm

in diameter and 45 cm in length in adults, usually filling

the entire length of the abdominal cavity) that is mostly

situated in a dorsal position relative to the gut but with a

direct link to the ventral side of the oesophagal. Some

anatomists have called this organ ‘lung’ or ‘fatty lung’

(Millot et al. 1978). The physiological function of the

[Palaeontology, Vol. 53, Part 6, 2010, pp. 1281–1290]

ª The Palaeontological Association doi: 10.1111/j.1475-4983.2010.01015.x 1281

calcified organ in fossil coelacanths and its homology with

the fatty lung of Latimeria remained to be proven.

To provide factual data for this long unresolved issue

(i.e. is the calcified organ of fossil coelacanths homolo-

gous to the ‘lung’ of the recent Latimeria?), we present a

histological study of the calcified organ of the fossil

Mesozoic coelacanth, Axelrodichthys araripensis.

The following interpretations, and those of previous

authors (e.g. Williamson 1849; Woodward 1891; Maisey

1986), of the role of the calcified bladders of fossil coel-

acanths should be considered cautiously as there is little

or no fossil evidence for any particular function.

MATERIAL AND METHODS

We have studied the histological structure of fossilized

‘bladder’ preserved in different specimens of Axelrodich-

thys araripensis. This species is relatively common in the

Lower Cretaceous Santana Formation of the Araripe

Basin, northeastern Brazil (Campos and Wenz 1982;

Maisey 1986), being also known from the slightly older

Crato Formation of the same Basin (Brito and Martill

1999).

To observe the histological structure of the fossils,

about 1 cm thick slices were cut in the middle of the

bladder. Then, each slice was embedded in Stratyl

(Chronolite 2060). Cross and horizontal sections (accord-

ing to the antero-posterior axis of the calcified organ)

were cut with a saw (‘Isomet’ or ‘Brot’ for the larger sam-

ples), glued on a glass slide and then ground to the

appropriate thickness. The ground sections were observed

in transmitted natural and polarized light.

The external surface of the bladder of young Axelrod-

ichthys specimens reaching less than 200 mm TL (total

length: the distance between the most anterior point of

the snout to the most posterior point of the caudal fin)

was observed using a scanning electron microscope

(SEM).

A high-resolution computerized axial tomography scan-

ning (CAT scan) of the specimen MNHN C.20 (male,

130 cm TL; for further information see Bruton and

Coutouvidis 1991) was made at the Centre Hospitalier

Intercommunal of Villeneuve-Saint-Georges (France).

Scan parameters are as following: 120 kV, 158 mA, slice

thickness = 0.8 mm, 1807 views.

High-resolution X-ray computed tomography is a non-

destructive and noninvasive technique that has the unique

ability to image a combination of bone, cartilage and soft

tissue (liver, muscles, fat, blood vessels, etc.). These CAT

images are suited to three-dimensional reconstruction.

The 3D image processing software MIMICS (Materialise’s

A

B C

TEXT -F IG . 1 . Axelrodichthys araripensis. A, Adult specimen, ‘Josa collection’ deposited at the Laboratoire de Paleontologie, MNHN,

left lateral view showing the calcified bladder (arrow head), scale bar represents 50 mm. B, juvenile specimen, UERJ-PMB33, showing

the calcified bladder somewhat distorted (arrow head), scale bar represents 40 mm. C, a very young specimen, MPSC-287, from Brito

and Martill 1999, showing the bladder (arrow head), scale bar represents 10 mm.

1282 P A L A E O N T O L O G Y , V O L U M E 5 3

Interactive Medical Image Control System) has been used

to create 3D virtual reconstructions.

To make ourselves perfectly clear, the ossified organ of

the fossil coelacanths (previously called ‘internal osseous

viscus’, ‘ossified stomach’, ‘air bladder’, ‘gas bladder’,

‘swim bladder’) will be here simply defined as a bladder,

whose definition is an inflated and hollow sac.

Institutional abbreviations. MNHN, Museum national d’Histoire

naturelle, Paris; MPSC, Museu de Paleontologia de Santana do

Cariri; UERJ, Universidade do Estado do Rio de Janeiro.

Referred material. �Axelrodichthys araripensis. MNHN ‘Josa

collection’ (adult specimen from the Santana Formation);

MPSC-287 (juvenile specimen from the Crato Formation);

UERJ-PMB33 (juvenile specimen from the Santana Forma-

tion); UERJ-PMB 143 (adult specimen from the Santana Forma-

tion). Latimeria chalumnae MNHN C. 20 (adult male caught the

19th of June 1960 at Itsoundzou, Comoro Islands, Indian Ocean,

and preserved ever since in a 7 per cent diluted formalin

solution).

Anatomical abbreviations used in the text-figures. Bo, primary

bone; G, gut; Ga, limestone matrix; GO, fatty organ; OD,

oesophagal diverticulum; Oe, oesophagus; St, stomach.

Description

The bladder of Axelrodichthys is a well-calcified structure, easily

observed in specimens preserved in lateral view (Text-fig. 1A–C).

This structure is situated in the ventral part of the body and its

anterior part turns up where it is covered by the opercle. At this

level, its anterior extremity opens by a median orifice as the

neck of a bottle and may have opened into the pharynx or com-

municated with the oesophagus as proposed by Woodward

(1891). This anterior opening seems to be the only aperture of

the calcified organ; its posterior extremity is generally more or

less pointed, but always closed (Text-fig. 1A). This bladder is

generally divided into an anterior and a posterior chamber, sepa-

rated by a constriction (Maisey 1986; Forey 1998). More than

one constriction can also occur (see Text-fig. 1A, where two

constrictions are present). In adult individuals, the walls of this

bladder comprise a series of superimposed bony plates (Text-

fig. 2A–D), as in other fossil coelacanths such as the Triassic

Piveteauia madagascarensis and the Jurassic Swenzia latimerae

(Clement 1999, 2005, 2006). Each plate is gently concave on its

internal side with the longest plates located on the peripherical

area of the organ, the smallest and thinnest ones being preserved

along the inner surface of the walls of the bladder. The thickness

of the laminae decreases regularly towards their margin, and

both surfaces of the laminae are smooth (Text-fig. 2A, B). These

features show that the wall of the calcified bladder comprises

several sheets that are spatially organized like the layers of an

onion.

In young Axelrodichthys individuals, generally <200 mm TL,

the bladder is unossified, being sometimes preserved as a com-

pact mass of diagenetic calcium phosphate (Text-fig. 1B, C). Soft

tissues composing these walls were preserved as eodiagenetic

replacement by calcium phosphate (Text-fig. 3A, B) during fos-

silization. This process is linked to early bacterial growth and

the decay of soft tissues (Martill 1988; Briggs et al. 1993; Briggs

2003). It occurs rapidly and often predates significant tissue

decay. As a consequence, high fidelity replication of tissues may

occur, especially when the replacing crystallite size is very small

(<1 lm), as it is the case here. Observed in SEM, this phos-

phatic mass reveals the spatial organization of the walls of the

bladder. They consist of several strata of fibres, with a diameter

of 10–20 lm; these fibres were probably collagenic during life.

In each sheet, the fibres are parallel to each others and their

direction changes from an angle of about 90 degrees between

two successive strata (Text-fig. 3A). The Jurassic genus Swenzia

also presents parallel striations on the superimposed bony plates

whose directions seem to have a radiating arrangement on the

plate (Clement 2005, fig. 6C; Clement 2006).

In adult specimens of Axelrodichthys, the smooth ossified lam-

inae of the fossilized ‘bladders’ are relatively well preserved

(Text-fig. 2A–D), except when some epigenetic mineralization

has occurred, but epigenized laminae are relatively scarce in the

whole organ. In the preserved laminae, the histological details

are clearly visible. The walls of the bladder are made up by layers

of primary cellular bone, separated by layers of limestone matrix

(Ga, Text-fig. 4A, C, E). The bony tissue is either pseudo-lamel-

lar or lamellar cellular bone (Text-fig. 4C, E, G). The osteocytes

are typically star shaped, with numerous cytoplasmic processes,

the main direction of which is orthogonal to the bone lamellae

(Text-fig. 4G–I). They are located between two successive lamel-

lae giving them a flat shape. Their average thickness is 15–

30 lm, and their main depth is about 3–6 lm. In some thicker

areas, the bony layers can be vascularized (Text-fig. 4D–F) and

the walls of the cavities can show remodelling bone (= secondary

bone) (Text-fig. 4F).

DISCUSSION

In 1849, Williamson (pl. 43, figs 29–30) figured accurate

drawings of horizontal and vertical sections of the ossified

bladder (·350 magnifications of the ‘internal osseous vis-

cus’) of the Cretaceous coelacanth Macropoma mantelli.

Williamson (1849, pp. 463–464) claimed that the walls of

this bladder ‘...consisted of true laminated bony tissue’ and

that ‘Except in cases of diseased ossification, the existence of

an internal thoracic or abdominal viscus, having hard

parietes of true bone, is an anomaly, which, as far as I am

aware, has hitherto presented no parallel in nature’. One

hundred and sixty years after Williamson, our histological

observations confirm that the walls of the fossil coela-

canth bladder are made of true cellular and vascularized

bone. One of the first questions to be placed is how, in

adult specimen bladders, bone could be developed from

tissues belonging to the walls of the bladder? It is gener-

ally considered that the whole swim bladder of teleosts is

B R I T O E T A L . : C A L C I F I E D L U N G O F F O S S I L C O E L A C A N T H 1283

either an evagination of the gut or that the evagination of

the endodermal tissue may invade a group of uncon-

nected mesoderm cells (coming from the splanchnople-

ura) then forming the outer layers of the bladder (Hoar

1937 in Pelster 2004); therefore, the walls of the bladder

have a double origin.

We have no available data about the embryological ori-

gin of the bladder in fossil coelacanths neither of the ‘fatty

organ’ in Latimeria. However, one may consider an anal-

ogy with the second hypothesis (e.g. double embryological

origin: endodermal for the breathing epithelium and

mesodermal for the walls in part). The presence of an ossi-

fication process of the wall of the ‘air bladder’, in physo-

stomid fish (Marshall 1962; Parmentier et al. 2008) is thus

understandable, although surprising, but not exceptional.

Besides, the mineralized structure of the so-called ‘rocker

bone’ situated at the anterior part of the swim bladder of

the carapid teleosts (Perciformes) is made by a specialized

mineralized conjunctive tissue, possibly of chondroid bone

(Parmentier et al. 2008) if not of true bone.

How can we interpret this structure in fossils?

What function performed the calcified organ in fossil

A

B

D

C

TEXT -F IG . 2 . Axelrodichthys araripensis. A, ‘Josa collection’ deposited at the Laboratoire de Paleontologie, MNHN, photograph of

right lateral view showing the posterior chamber of an ossified bladder; scale bar represents 10 mm. B, same specimen as in A,

photograph of left lateral view; scale bar represents 10 mm. C, Section of an uncrushed ossified bladder (from Clement, 1999, fig. 6);

scale bar represents 5 mm. D, Section of a more or less crushed bladder. UERJ-PMB 143; scale bar represents 5 mm.


coelacanths? We can suppose that the ossified organ was

filled either with fat for buoyancy control (like the ‘fatty

organ’ of Latimeria) or with gas for breathing function.

Could this large empty cavity protected by numerous

independent bony plates also have had other functions as

a specialized bladder for an auditory function or a sound

production?

The calcified bladder as an air bladder or a lung?

The position and shape of the bony organ in the fossil

coelacanthids suggest a homology with the anatomical

complex: vestigial lung (= oesophagal diverticulum) +

fatty organ of Latimeria. The anterior part of the ossified

organ appears to be situated somewhat more ventrally in

the body cavity than its posterior part (Maisey 1986). It is

congruent with a ventral position of the anteriormost part

of the lung (originating from the ventral side of the

oesophagus), posteriorly followed by a dorsal turn up,

leading to a dorsal position of the posterior part of the

lung in relation to the gut. The fatty organ of Latimeria,

enclosing anteriorly the vestigial lung, presents a such

dorsal turn up (Text-fig. 5A–D).

The distribution of lungs in vertebrate phylogeny sug-

gests that the latter are primitive osteichthyan structures

(Farmer and Jackson 1998), and even possibly for gnat-

hostomes because putative respiratory organs (‘lungs’)

have been reported in placoderms (Janvier et al. 2007),

that act in synergy with gills. This allows a bimodal respi-

ration (Brainerd 1994b), i.e. functional lungs + functional

gills, that results from either an increasing metabolism

activity or an increase in the body mass. Such a bimodal

respiration was described especially in lungfishes (Grigg

1965a, b; Liem 1986), and polypterids (Brainerd et al.

1989). It should be noticed that lepisosteids and amiids

(Farmer and Jackson 1998) and some rare osteo-

glossomorphs, elopomorphs, ostariophyses and esocoıdes

possess respiratory gas bladders rather than true lungs

(Graham 1997) and that these organs are dorsal (and not

ventral) evaginations of the oesophagus. Currently, it is

considered that the presence of a ventral oesophagal

diverticulum is plesiomorphic for Osteichthyes. In a gen-

eral way, this organ does not fossilize like most soft tissue

internal organs, except in fossil coelacanthids when the

walls of this oesophagus pouch are biomineralized.

The calcified organ as a specialized lung

In Latimeria, the ventral oesophagal diverticulum (Text-

fig. 5A–D; Millot et al. 1978) is considered as a vestigial

lung, the external conjunctive layer of which being

secondarily filled with oil to form the so-called ‘fatty

organ’ (Millot et al. 1978); it appears to be an adaptation,

a loss of its breathing function and an improvement of

the buoyancy of the fish for deep-water habitat, because

this species lives at a depth of several hundred metres

(Forster 1974; Fricke and Plante 1988; Forey 1998).

When preserved in an uncrushed condition, the calci-

fied lung in Axelrodichthys is usually hollow with a geode-

like lining of calcite (Text-fig. 2C). Maisey (1986) sug-

gested that the internal cavity was filled with fatty tissue

during life. However, in some of the specimens examined,

the lung has not resisted compaction during fossilization,

although a lining of calcite is still present (Text-fig. 2D).

The presence of fatty tissue within the bladder of Axelrod-

ichthys, if this assumption is correct, lets suppose that fos-

sil coelacanths had an ossified fatty organ (homologous

to the soft fatty organ of Latimeria) and probably a vesti-

gial lung (supposedly in the same position and maybe

already at same degree of reduction than in Latimeria,

although no trace of this soft vestigial lung has ever been

A

B

TEXT -F IG . 3 . Axelrodichthys araripensis, UERJ-PMB 33. A,

general view showing several strata of collagen fibres whose

orientation change from one layer to the next one. Scale bar

represents 50 lm. B, detail of the insert showing magnified

collagen fibres. The fossilization processes have preserved the

morphology of the fibres. Scale bar represents 10 lm.


recognized in fossils). An ossified organ filled with fatty

tissue should have had the same function as the fatty

organ of Latimeria that is for the hydrostatic balance.

The bladder in adult Axelrodichthys is a very well-ossi-

fied structure, formed by numerous superimposed, multi-

layered, bony plates, separated from one another by an

unossified connective tissue. This pattern suggests that

this structure had a somewhat variable volume, whereby

the large plates moved over each other to accommodate

certain volumetric changes and acting as bellows. The role

of these movable bony layers in a bladder filled with fat

would be difficult to interpret, and it makes more sense

that the bladder was filled with gas rather than oil or fat.

If so, the volumetric variation was probably linked with

elastic and muscular properties of the lung’s walls, facili-

tating the ventilation of breathing gas on the respiratory

epithelium.

Accepting that the anatomical complex (vestigial

lung + fatty organ) is homologous to the bony organ

AB

C

D

E

F

G

H I

TEXT -F IG . 4 . Axelrodichthys araripensis. Ground cross section

(transmitted natural light) in the calcified wall of the bladder. A,

section through 11 bony laminae of various thickness separated

by the limestone matrix (Ga). The upper and lower surfaces of

each lamina look regularly smooth. The sixth and ninth laminae

are very thin because of their proximity of their border. Scale

bar represents 200 lm. B, section through an epigenized bony

lamina. The various stages of the epigenesis process are very

clearly because of the concentric ridges (arrows). The osseous

organization has wholly disappeared. Scale bar represents 50 lm.

C, section shows three bony laminae (1–3) separated by the

limestone matrix (Ga). The upper and lower surfaces of each

laminae look regularly smooth. The middle lamina is faintly

epigenized. Scale bar represents 100 lm. D, section through a

bony lamina crossed by several more or less regular artefact

cracks (arrow heads). Several medial vascular canals are obvious

(arrows). Scale bar represents 50 lm. E, section through two

bony laminae: a very thick (below) and a very thin (above)

(arrow head), the latter having been cut near its margin. The

thickest lamina shows pseudo-lamellar bone and several vascular

canals and ⁄ or cavities (asterisks) (Ga = limestone matrix). Scale

bar represents 100 lm. F, enlargement of a section showing two

bony laminae, separated by a very thin layer of matrix (white

arrow head). The upper lamina is constituted of primary bone

(Bo) only. The second one shows three large vascular cavities

(white asterisks) the wall of which is constituted of secondary

bone (white and black arrows). The black arrowhead points

towards osteocytes lacunae. Scale bar represents 30 lm. G,

enlargement of a bony lamina constituted of primary bone

showing numerous osteocytes. Scale bar represents 30 lm. H,

detail of an osteocyte from the region localized by the black

asterisk in Text-figure 3E. Scale bar represents 10 lm. I, Detail

of osteocytes from the region localized in Text-figure 3F,

showing the canalicles that start from the osteocytes lacunae and

are more numerous on the lower surface of the cells (arrows).

Scale bar represents 10 lm.


of Axelrodichthys, one may suppose that these structures

in the fossil taxon should be active as an interface for

gas exchange, like the lung of extant lungfish Neocerato-

dus (Gunther 1871; Grigg 1965a, b; Thomson 1968;

Burggren and Johansen 1986) and extant polypterids

(Horn and Riggs 1973; Brainerd et al. 1989; Farmer

and Jackson 1998). It is also known that the depen-

dence upon aerial respiration, in the extant Protopterus

and Lepidosiren, increases dramatically as their body

mass increases (Liem 1986). This does not imply that

Axelrodichthys, as all other fossil coelacanths with ossi-

fied lungs, was necessarily a strictly air breather but

that in some circumstances, it could effectively use the

lung to support more intense activity. Contrary to

extant coelacanth species, Axelrodichthys lived in lagoo-

nal or epicontinental shallow marine environments and

was probably subjected to adverse conditions of shal-

lowing or hypoxia.

The lung was closely surrounded by ossified plates.

Connective tissue connexions between the external surface

of the lung and the internal side of the laminae permitted

the increase in the pulmonary volume to swallow the air

when the muscles attached to the external surface of the

laminae were contracted. The protecting bony laminae

should not have been a problem for the gas exchanges if

we assume that the folded mucous membrane was inside

the ossified body. Arteries and veins could have most

probably passed between the laminae (Text-fig. 4A, C) or

through the bony lamina itself because large vascular cav-

ities and canals have been observed within the laminae

(Text-fig. 4F).

Air respiration necessitates the differentiation of an

accurate ventilation system. In the extant Neoceratodus,

exhalation of air is effected by contraction of the smooth

muscle components of the lung, assisted by its natural

elasticity provided by elastin fibres present in both con-

nective tissue and smooth muscle (Grigg 1965a). It is

interesting to note that the Mesozoic coelacanth Diplurus,

one of the rare well-preserved coelacanths lacking a calci-

fied organ, also shows greatly elongated pleural ribs

(Schaeffer 1948). According to Schaeffer (1952, p. 48),

‘the functional significance of this elongation is obscure’. If

we postulate that fossil coelacanths had a functional lung,

we can assume that these elongate pleural ribs played the

same role as the ribs of tetrapods, i.e. the contraction of

the inter-pleural rib muscles enlarged the pulmonary cav-

ity and the reduced air pressure in the cavity causes air to

enter the lung. Such a ventilation system, homoplasic

with that of the tetrapods, could explain the absence of

calcified lung in Diplurus. The primitive actinopterygian

Polypterus uses recoil respiration (Brainerd et al. 1989).

The walls of the lungs are partly composed of a muscular

layer especially in the posterior part where it is thicker

and it could occur in ventilation function (Poll and

Dewattines 1967). This extant biological model also uses

the deformation of the stiff integument, constituted of

interlocking rhomboid scales, for sucking air into the lung

B

AG

St

GOOe

OD

D

C

TEXT -F IG . 5 . Latimeria chalumnae, specimen MNHN C.20.

External morphology of lung and diverticulum. A, drawing of

the anatomy of the lung, modified from Robineau (1987). (G,

gut; GO, fatty organ; OD, oesophagal diverticulum; Oe,

oesophagus; St, stomach). B, three-dimensional reconstruction

of the whole anatomy of the fish by means of axial computed

tomography, showing the entire gut and the oesophagal

diverticulum in the visceral cavity (arrow) in left lateral view.

Scale bar represents 20 cm. C, Detail of the oesophagal

diverticulum (arrow) and fatty organ (asterisk). Reconstruction

of the anterior anatomy of the fish in left lateral view. Scale bar

represents 10 cm. D, Detail of the oesophagal diverticulum (left

lateral view). Scale bar represents 4 cm. B–D, (Materialise

MIMICS v.12.1 software).


(Brainerd 1994a). Conversely, when the bladder of Axel-

rodichthys inflated during air inhalation, the osseous

plates could store the tension strength and released it as

an elastic energy facilitating air expulsion. So, the bony

walls of the lung in Axelrodichthys (and in other coel-

acanthids with an osseous bladder) can play the same

function as does the integument of polypterids for air

ventilation.

The calcified organ as an auditory organ

A large empty cavity protected by numerous indepen-

dent bony plates could have had an auditory function.

In fossil coelacanths, the anterior extension of the ossi-

fied organ extends under the opercle and seems to reach

the back of the head in some specimens. Such anterior

position may suggest some possible relation with the

inner ear, as in many teleosts (Tavolga 1971). The ante-

riormost part of the bladder could have joined the skull

as in clupeomorphs. Some bones (equivalent to the

Weberian apparatus) or modified vertebrae could have

connected the bladder to the inner ear as in otophysans

and gonorynchiforms (Lecointre and Nelson 1996). Fur-

thermore, both gonorynchiforms and otophysans present

a swim bladder divided into anterior and posterior

chambers, a morphology also seen in the ossified blad-

der of Axelrodichthys. More importantly, the coelacanths

present a communication, via the canalis communicans,

between the two inner ears, as seen in the ostariophy-

sans (Millot and Anthony 1965; Bernstein 2003). In

Latimeria, the canalis communicans emerges from the

vestibule, at the transition point of the saccule and lage-

nar recess, passing backward and medially to complete a

semiloop between the two inner ears. The commissure

of these two canals is obvious on the posterior side of

the skull, between the foramen magnum and the noto-

chordal canal. According to Millot and Anthony (1965),

a short median diverticule issued from the commissure

is posteriorly directed. These authors proposed a regres-

sion of the auditory apparatus on the basis of palaeon-

tological data and a possible link with the calcified

bladder of the fossil coelacanths Undina and Laugia. The

posterior wall of the skull of fossil coelacanths presents

foramina for the canalis communicans and a transverse

groove for the communicans commissure. This com-

municans commissure is even much more developed in

fossil coelacanths (especially Palaeozoic genera such as

Diplocercides) than in Latimeria. This character most

probably developed early in the evolutionary history of

coelacanths (Bernstein 2003).

In Latimeria, a membrane (‘innervated end organ’)

covering the foramen at the sacculo-lagenar orifice sug-

gests that the canalis communicans is a perilymphatic

duct rather than an endolymphatic duct as in some tele-

osts (Bernstein 2003). This membrane in Latimeria

might be responsive to very small pressure changes

between the endolymphatic cavity and the perilymphatic

duct. An auditory function of the ossified bladder is thus

possible if we assume that the canalis communicans was

linked to the ossified organ by any kind of soft tissue:

ligament, canal, anterior expansion of the epithelium of

the ossified organ or posterior expansion of the com-

municans commissure (in this latter hypothesis, the

median diverticule of the communicans commissure in

Latimeria could thus be considered as a vestigial remain

of this expansion).

Such a connection might have transmitted vibrations

from the bladder to the labyrinth of the ear. In fossils,

the wall of the bladder, composed of closely set indepen-

dent rounded plates, might have amplified the sensitivity

to the difference of external pressure as well as increased

the amplitude of the vibrations. A sound-transmitting

apparatus from the anterior part of the ossified bladder

and the canalis communicans was not necessarily very

long if we assume that the ossified bladder was anteriorly

extended, as seen in fossils, but it had to bypass the noto-

chord. However, this auditory function is highly hypo-

thetical, because no trace of Weberian-like apparatus or

of modified vertebrae have been recorded so far in fossil

coelacanths; however, a nonfossilized link cannot be

totally excluded.

The calcified organ as a sound production organ

Such a cavity, supposedly filled with gas, could also have

played a role as a resonance chamber. In this case, the

independent plates might have been shaken the ones on

the others, creating a rattle noise, the cavity having the

same function as a resonator. Some teleosts produce

sounds (Marshall 1962), generally for agonistic and ⁄ or

courtship behaviour (Tavolga 1971; Fine 1997). ‘Drums’

and ‘Croakers’ (Sciaenidae) have special muscles attached

to their swim bladder for sound production (see Schnei-

der 1962; Tavolga 1971); some catfishes also possess a

modified swim bladder for sound production (Fine et al.

1997; Fine and Ladich 2003), and they use specialized

muscles on the upper surface of an elastic bony spring to

create vibrations from the swim bladder. Moreover, cer-

tain species among the carapids are able to generate

sounds thanks to the so-called ‘rocker bone’ a specific

mineralized formation situated at the anterior part of the

swim bladder (Rose 1961; Courtenay and McKittrick

1970; Parmentier et al. 2003). Extant coelacanths seem to

have a remarkable social behaviour (Fricke et al. 1991).

Sound communications could have played a role in the

early coelacanth communities.


CONCLUSIONS

The abdominal ossified organ of fossil coelacanths and

the complex (oesophagal diverticulum + fatty organ) of

Latimeria are most probably both of pulmonary origin.

Although this homology between the ossified organ of �Axelrodichthys and the pulmonary apparatus of Latimeria

seems to be acceptable, it is impossible to determine

whether the ossified organ was filled (1) with oil (as previ-

ously assumed) + an anterior vestigial lung, (2) with

gas + an anterior vestigial lung and (3) with breathing

epithelium + ventilated air + a well-developed and func-

tional lung. Assuming that the ossified organ was filled

with gas, coelacanths would have had to inhale air at the

surface as do the extant Dipnoi. If its function is most

probably hydrostatic in the living coelacanth Latimeria, it

is quite improbable in fossil coelacanths. Actually the

Bernstein’s (2003) hypothesis of an adaptation to ground-

dwelling or deep-sea fishes to better withstand the high

water pressure is not reliable with the usually low-depth

palaeoenvironments of fossil coelacanths. Here, we favour

the air-breathing hypothesis, and then the calcified organ

is a remnant of a specialized functional lung; although

other hypotheses such as auditory, sound production and

mineral elements storage could be possible, certain of

them being able to act in synergy. Such multifunctionality

is known in some neotropical silurids: buoyancy, audi-

tion, sound production. As a matter of fact, a breathing

function of the ventral oesophagal pouch is a plesiomor-

phic character and complements the gill breathing. In the

coelacanthids with a bony bladder, the ossified walls rep-

resent a specialization to improve breathing ventilation.

Acknowledgements. We thank Marc Herbin, Marie-Madeleine

Loth, Lucio P. Machado, and Christiane Chancogne for all their

help during this project. We especially thank John G. Maisey,

Jesus Alvarado-Ortega, and an anonymous referee for their care-

fully reviewing of this manuscript as well as D. Martill for

improving the English style. P.M.B.’s research has been partially

supported by the Conselho Nacional de Desenvolvimento Cient-

ıfico e Tecnologico (CNPq), a fellowship from the Department

des Milieux et Peuplements Aquatiques – Museum national

d’Histoire naturelle, and a PROCIENCIA research grant.

Editor. Marcello Ruta

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