Soft-part anatomy of the siphuncle in Permian prolecanitid ammonoids

Soft-part anatomy of the siphuncle in Permian prolecanitid
ammonoids
KAZUSHIGE TANABE, ROYAL H. MAPES, TAKENORI SASAKI AND NEIL H. LANDMAN
Tanabe, K., Mapes, R. H., Sasaki, T. & Landman, N. H. 2000 06 15: Soft-part anatomy
of the siphuncle in Permian prolecanitid ammonoids. Lethaia, Vol. 33, pp. 83±91.
Oslo. ISSN 0024-1164.
Exceptionally well-preserved remains of phosphatized siphuncles were discovered in
four specimens of a Permian prolecanitid ammonoid Akmilleria electraensis (Plummer
and Scott) from Buck Mountain, Nevada. These structures occur as truncated segments
within the siphuncular tube. The outer surface of the siphuncle is sculptured by numerous equally spaced longitudinal ridges and furrows; the ridges represent an infolded
basement membrane of epithelial cells which corresponds to the distal ends of individual canaliculi between epithelial cells. In cross-section, the siphuncle of A. electraensis
consists of a large central vein, possibly two pairs of arteries, porous connective tissue
with reticulate hemocoelic spaces, and a thin epithelium. In the presence of two pairs
of arteries and porous connective tissue, the siphuncle of A. electraensis is more like
that of Nautilus pompilius than that of Spirula spirula, which has nine arteries and
dense connective tissue. However, Nautilus possesses relatively smaller and more numerous epithelial cells around the siphuncle than does Akmilleria. These observations
strongly suggest that the siphuncular epithelium of Akmilleria served as the saltconcentrating organ for buoyancy regulation of the living animal, just as in Nautilus
and Spirula. & Akmilleria, anatomy, Nautilus, Nevada, Permian, Prolecantid ammonoids,
siphuncle.
Kazushige Tanabe [[email protected]], Department of Earth and Planetary
Sciences, University of Tokyo, Tokyo 113-0033, Japan; Royal H. Mapes, Department of
Geological Sciences, Ohio University, Athens, Ohio 45701-2979, U.S.A.; Takenori Sasaki,
University Museum, University of Tokyo, Tokyo 113-0033, Japan; Neil H. Landman, Division of Paleontology (Invertebrates), American Museum of Natural History, Central Park
West at 79th Street, New York, New York 10023-5192, U.S.A.; 1st April, 1999; revised 7th
February, 2000.
Ammonoids are extinct chambered cephalopods that
¯ourished in Middle-Late Paleozoic and Mesozoic
seas. Despite their rich fossil record in marine deposits
of various geological settings, most of our knowledge
of their soft part anatomy has been con®ned to hard
tissues such as jaws and radula (see Lehmann 1990;
Nixon 1996; and Tanabe & Fukuda 1999, for recent
reviews).
The siphuncle is a long and narrow segmented tissue
consisting mainly of blood vessels and surrounding
epithelium. It occurs in three extant chambered
cephalopods: Nautilus (Nautilidae: Nautiloidea), Spirula (Spirulidae: Coleoidea), and Sepia (Sepiidae:
Coleoidea). In Nautilus and Spirula, the siphuncle is
housed in the siphuncular tube within the phragmocone
and is connected with the rear part of the body at the base
of the body chamber, while in Sepia it is ¯attened
underneath the cuttlebone without a mineralized wall
(AppelloÈf 1893; Bandel & Boletzky 1979; Denton &
Gilpin-Brown 1961, 1966, 1973, among others).
The siphuncular tube consisting of a mineralized or
organic hard tissue has been known to occur in
virtually all fossil cephalopods, including ammonoids.
In ammonoids, it passes through an opening in each
septum and extends from the apex of the shell to the
base of body chamber, forming the septal necksiphuncular complex (Tanabe & Landman 1996).
Many authors speculated that a soft-part element of
the siphuncle must also have been present in
ammonoids. This hypothesis has been con®rmed by
the discovery of fossilized siphuncular remains in the
Triassic ceratites from Spitsbergen (Weitschat 1986,
pl. 3, ®gs. 2±4, pl. 4, ®gs. 1, 3, 4; Weitschat & Bandel
1991, ®g. 23) and Jurassic ammonite Virgatites from
Russia (Druschits & Doguzhaeva 1981, pl. 22, ®g. 59b;
Druschits et al. 1982, pl. 4, ®g. 1e, f; Barskov 1996, ®gs.
2±8, 11). Yet, the microstructure of the siphuncle is
not preserved in these materials.
We have recently discovered better preserved
fossilized remains of siphuncular soft-tissues in early
Permian ammonoids. This paper describes their
anatomical features by comparing them with the
siphuncles of Nautilus and Spirula. We also discuss
their taxonomic and functional implications.
84
Kazushige Tanabe et al.
LETHAIA 33 (2000)
Fig. 1. Geological map of the
northwestern White Pine County,
Nevada (adopted from Hose &
Blake 1976), showing the location
of the specimens of Akmilleria
electraensis (Plummer and Scott)
examined.
Materials and methods
Well-preserved tissue remains of the siphuncles were
discovered in four specimens of the prolecanitid
ammonoid Akmilleria electraensis (Plummer and
Scott). These specimens were recovered from carbonate concretions from the Lower Permian (Wolfcampian) Arcturus Formation, Buck Mountain, White
Pine County, Nevada (Fig. 1).
Each specimen was ground and polished with a
graded series of carborundum and diamond pastes to
just above the median plane, and the polished surface
was etched with 5% acetic solution for one minute.
The etched surface was washed in distilled water,
dried, coated with platinum or carbon, and then
observed with a Hitachi Model S 4500 scanning
electron microscope. One specimen coated with
carbon was analysed by means of an X-ray energy
dispersion microanalyser attached to the SEM to
determine elemental and mineralogical compositions
of the fossilized siphuncle.
For comparison, optical and SEM observations were
made of a siphuncle in a specimen of Nautilus
pompilius Linnaeus caught in 1996 off the Bohol
Straits, Philippines. Immediately after capture, the soft
body was carefully removed from the shell and ®xed
with 5% formalin. In the laboratory, the siphuncle was
severed from the soft body and cross-sectioned into
several pieces with a razor blade. The sectioned pieces
of the siphuncle were dehydrated through a graded
series of ethanols, freeze-dried through t-butylalcohol
and then observed with SEM. Also, pieces of the
siphuncle from different positions in the phragmo-
LETHAIA 33 (2000)
Permian prolecanitid ammonoids
85
Fig. 2. SEMs of the siphuncle of Nautilus pompilius Linnaeus. UMUT RM 27811 from the Bohol Straits, Philippines. &A, B. Cross-section of
the adapical (A) and the middle (B) portion. &C. Close-up of B, showing the artery surrounded by a thick wall of connective tissue. &D.
Oblique view, showing equally spaced, numerous longitudinal ridges of canaliculi. e: epithelium, a: artery, v: vein (hemocoele), oc: outer
connective tissue layer, ic: inner connective tissue layer, ct: connective tissue.
cone were embedded in paraf®n (melting point 58 °C),
and thin cross-sections were made at intervals of 8 mm.
Selected sections were stained using Masson's trichrome method and then observed by means of an
Olympus model AHBS-515 light microscope. This
paper follows Greenwald et al. (1982) for terminology
of the microstructural elements of the siphuncle.
All the specimens utilized are housed in the
University Museum, University of Tokyo (UMUT).
Siphuncles of Nautilus and Akmilleria
Nautilus
The anatomy of the siphuncle in Recent Nautilus,
namely N. macromphalus Sowerby and N. pompilius
Linnaeus, has been described by Denton & GilpinBrown (1966, 1973), Bassot & Mortoja (1966), Greenwald et al. (1980, 1982), Fukuda et al. (1981), and
Bandel & Spaeth (1983). These studies have revealed
that the siphuncle of Nautilus is a segmented tubular
structure consisting of a wide central vein, two pairs of
arteries, porous connective tissue, and a siphuncular
epithelium on the outside. Of these anatomical
elements, the siphuncular epithelium has been investigated for its ultrastructure in relation to its function
in buoyancy regulation. The epithelium is characterized by several specialized features, such as (i) an
apical brush border with dense microvilli and wavy
apical folds on the outer surface, (ii) a feathery
appearing lamellar structure (= mitochondria-lined
infoldings) in cytoplasm, and (iii) a narrow canaliculus (= longitudinal duct of Denton & Gilpin-Brown
86
Kazushige Tanabe et al.
LETHAIA 33 (2000)
epithelial basement is formed by ®rm sheets of
connective tissue (ct) with sporadic haemocoelic
spaces. In the outer sublayer, ®bers are strati®ed
almost parallel to the bases of epithelial cells (Fig. 3B),
while in the inner sublayer they occur irregularly
among connective tissue cells (Figs 2C, 4).
(3) Inner connective tissue layer (ic): The inner
section contains the siphuncular arteries (a) (Fig. 2C)
and a large hemocoelic space partitioned reticulately
by a membranous network of connective tissue (Figs
2A±B, 4). There are two pairs of arteries throughout
the entire length of the siphuncle (Fig. 2A±B).
Occasionally the arteries possess small branches of
arterioles in the outer connective tissue layer.
(4) Siphuncular vein (v): This structure is delimited
only by a very thin layer of connective tissue (Fig. 2A,
B) in contrast to the arteries, which are surrounded by
a thick circular wall of connective tissue (Figs 2C, 3).
The diameter of the vein increases from the proximal
to the distal end of the siphuncle (Fig. 2A±B). The vein
has connections with haemocoelic space of the inner
connective tissue layer through small pores.
Fig. 3. Optical micrographs of siphuncular epithelium of N.
pompilius. &A. Intact part of the siphuncular epithelium. &B.
Damaged part of the siphuncular epithelium due to insuf®cient
®xation. Most of the cytoplasm is detached and the ridge of
basement membrane surrounding canaliculi (indicated by arrows)
is exposed. oc: outer connective tissue layer with sporadic
haemocoelic spaces.
1966) between elongated epithelial cells. This mitochondria-lined tubular system is assumed to be
responsible for the liquid transport between blood
vessels of the siphuncle and chambers of the shell
(Denton & Gilpin-Brown 1966; Greenwald et al. 1980,
1982). The structures of the other anatomical elements, however, have not been described in detail;
hence they were examined in this study prior to
elucidation of the microstructure of the ammonoid
siphuncle.
Microanatomy. ± The siphuncle has a three-layered
structure with a central vein (Figs 2±4, labels used in
the ®gures are shown in parentheses).
(1) Epithelium (e): The outermost layer is composed of a layer of columnar epithelial cells (ec) and
canaliculi (c) (Figs 2A±B, 3). The outer surface of the
epithelial cells is wavy corresponding to the longitudinal arrangement of the canaliculi, which are
spaced at almost equal intervals (Fig. 2D).
(2) Outer connective tissue layer (oc): The sub-
Canaliculi. ± The most specialized structures in the
siphuncle of Nautilus are the canaliculi (c), which are
formed by deep infoldings of the basement membrane
of siphuncular epithelial cells (Figs 3A, 4). The apical
end of each canaliculus is completely closed without
connecting directly with the inner surface of the
siphuncle, while the basal part is in communication
with the subepithelial hemocoelic space.
The number of canaliculi around the siphuncle is
extremely large, varying from approximately 240 near
the distal end to 280 near the proximal end of the
siphuncle in the specimen observed. Because epithelial
cells seem almost paired on either side of a canaliculus
(Fig. 3A), the number of epithelial cells is estimated to
be approximately 480 to 560 around the whole
siphuncle. Our observations also revealed that the
basement membrane forming the canaliculus is less
susceptible to dissolution than the cytoplasm of the
siphuncular cells. In the damaged part whose the
cytoplasm is mostly removed due to insuf®cient
®xation, the canaliculi remain intact and are exposed
on the surface (Fig. 3B). The canaliculi in these areas
exhibit a rough sculpture consisting of alternating tall
ridges and deep furrows. This observation has special
implications in reconstructing the structure of the
siphuncular epithelium in Akmilleria (see below).
Akmilleria
Notes on taphonomy. ± X-ray microanalysis of the
carbon-coated specimen (UMUT PM 27801) reveals
that the fossilized siphuncle is rich in phosphorus and
LETHAIA 33 (2000)
Permian prolecanitid ammonoids
87
Fig. 4. Schematic representation of
the cross-section of the siphuncle
in N. pompilius. a: artery, c:
canaliculus, ec: siphuncular
epithelial cell, h: haemocyte, n:
nucleus of siphuncular epithelial
cell, oc: outer connective tissue
layer. For other abbreviations, see
legend to Fig. 2.
calcium with lesser amounts of ¯uorine and sulphur
(Fig. 5); the amounts of P2O5 and CaO are 40.31% and
54.57wt%, respectively. A similar chemical composition was detected for the siphuncular tube that appears
to be primarily made of conchiolin. These data suggest
that the fossilized siphuncle and tube wall are both
made up of ¯uorapatite. These tissues were presumably phosphatized immediately after death and before
decay in the early taphonomic stage.
Microanatomy. ± The siphuncle occurs within the
siphuncular tube as truncated segments (Figs 6A, C,
7C). In life, the segments would have been connected
to form a long continuous cord-shaped structure. In
the best-preserved specimen with a phragmocone
diameter of 12 mm (UMUT PM 27800), each segment
is circular in cross-section with a diameter of
approximately 60±70% of the inner diameter of the
siphuncular tube, indicating shrinkage of 30±40%
during fossilization.
Comparative SEM observations of the siphuncles of
Nautilus and Akmilleria help elucidate the similarity
and dissimilarity of their microanatomy. The outer
surface of the siphuncle of Akmilleria is sculptured by
equally spaced, longitudinal ridges and furrows (Fig.
6A±C), as in the case of Nautilus (Figs 2A±B, 3, 4). The
ridges correspond to the distal ends of individual
canaliculi. There are approximately 30 ridges around
the siphuncle of Akmilleria in both the second whorl,
where the siphuncle diameter = 60 mm (Fig. 6C), and
Fig. 5. Energy dispersion spectrum for the fossilized siphuncular
portion of A. electraensis. UMUT PM 27801. From the Lower
Permian (Wolfcampian) Arcturus Formation, Buck Mountain,
White Pine County, Nevada.
88
Kazushige Tanabe et al.
LETHAIA 33 (2000)
Fig. 6. SEMs of the phosphatized siphuncle of A. electraensis. UMUT PM 27800. From the Lower Permian (Wolfcampian) Arcturus
Formation, Buck Mountain, White Pine County, Nevada. sc: siphuncle, sw: siphuncular wall, s: septum, cm: cameral membrane. The arrows
in A and C indicate the adoral direction. For other abbreviations, see the legends to Figs 2±4. &A, B. Exposed segment of a siphuncle in the
third whorl (A) and its close-up (B), showing numerous, equally spaced, longitudinal ridges and grooves. Each ridge represents the distal end
of canaliculus. &C, D. Exposed segment of a siphuncle in the second whorl (C) and close-up of its structure in cross-section, showing the
arteries, vein and connective tissue. The lower half of the siphuncle was lost during fossilization. &E. Close-up of D, showing a portion of an
artery surrounded by a thick connective tissue. &F. Sponge-like, porous connective tissue surrounded by a thin siphuncular epithelium.
LETHAIA 33 (2000)
Permian prolecanitid ammonoids
89
Fig. 7. SEMs of the phosphatized siphuncles of A. electraensis. UMUT PM 27802 (A, B) and PM 27803 (C, D). From the Lower Permian
(Wolfcampian) Arcturus Formation, Buck Mountain, White Pine County, Nevada. &A, B. Phosphatized remains of the siphuncle (A) and
close-up of the porous structure of the connective tissue (B). &C, D. Median-section of a segment of the siphuncle (C) and close-up of a
portion of the highly porous connective tissue (D). For abbreviations, see legend to Fig. 6.
in the third whorl, where the siphuncle diameter = 100 mm (Fig. 6A). This number is much lower
than that observed on the siphuncle of Nautilus, which
measures 1±2 mm in diameter (N = 240±280) (Fig.
2D). Individual canaliculi of the siphuncular epithelium of Akmilleria, presuming no postmortem shrinkage, are 10 mm wide in the second whorl (Fig. 6C, D)
and 15 to 20 mm wide in the third whorl (Fig. 6A, B).
Their dimensions are, therefore, comparable with
those of the canaliculi of Nautilus, even though the
shell of Nautilus is much larger (ca. 180 mm in
diameter).
In cross-section, the siphuncle of Akmilleria consists
of a large central vein, a pair of arteries, a reticulate
network of connective tissue, and a thin epithelium on
the outside (Fig. 6D±F), though the lower half has
shrunken toward the inside (Fig. 6D). A thick, smooth
connective tissue surrounds each artery (ct; Fig. 6E).
The boundary between the outermost epithelium and
the underlying connective tissue is not clear in the
specimens examined, owing to the destruction of the
internal epithelial structure during fossilization (Fig.
6F).
The siphuncles of the other specimens do not
preserve blood vessels and epithelium, retaining only
the highly porous structure of the connective tissue
(Fig. 7).
Discussion
Comparative anatomy. ± Our SEM observations reveal
that the siphuncle of Akmilleria electraensis is essen-
90
Kazushige Tanabe et al.
LETHAIA 33 (2000)
Fig. 8. Schematic diagram of the cross-section of the siphuncle in Akmilleria, Nautilus, and Spirula. Modi®ed from Chun (1915) for Spirula.
For abbreviations, see legends to Figs 1±3.
tially similar to those of Nautilus pompilius and Spirula
spirula (Chun 1915, pl. 73, ®g. 2) in the following
aspects: (1) the epithelial layer consists of elongate
epithelial cells and canaliculi, (2) the outer connective
tissue layer is made up of a subepithelial basement, (3)
the inner connective tissue layer contains siphuncular
arteries and hemocoelic space, and (4) the siphuncular
vein exists in or near the middle of the siphuncle (Fig.
8).
In contrast, there are three major microstructural
differences among the three genera: (1) Number of
canaliculi and epithelial cells: Akmilleria has about 30
canaliculi with epithelial cells based on the presence of
about 15 ridges that are visible on the half of the
siphuncle preserved. The number of epithelial cells in
Nautilus is much larger than in Akmilleria, reaching as
many as 500. The siphuncular epithelium of Spirula
has 60 or more longitudinal lines, which may
represent canaliculi (therefore, ? 120 epithelial cells).
(2) Number of arteries: Akmilleria probably has four
arteries equal to that of Nautilus. According to Chun's
(1915, pl. 73, ®g. 2) drawing of the siphuncle of
Spirula, there are as many as nine arteries surrounded
by a thick connective tissue in this genus. (3) Space of
inner connective tissue layer: Akmilleria and Nautilus
share reticulate hemocoelic space. In contrast, the
layer is ®lled mostly with connective tissue in Spirula.
The above similarities support the homology of the
siphuncle among Akmilleria, Nautilus and Spirula on
the basis of not only positional but also structural
criteria. Meanwhile, the similarity between Nautilus
and Akmilleria (i.e. four arteries within the sponge-like
inner connective tissue layer) may represent the
plesiomorphic state inherited from a cephalopod
ancestor. However, it remains uncertain whether or
not the differences among the three distantly related
taxa are constrained phylogenetically or functionally,
because of insuf®cient data from fossil taxa.
Prior to this work, Druschits & Doguzhaeva (1981,
pl. 22, ®g. 59b) and Druschits et al. (1982, pl. 4, ®g. 1e,
f; ®g. 1a) described a peculiar structure within part of
the siphuncular tube of a single specimen of a Jurassic
(Volgian) ammonite Virgatites virgatus from the bank
of the Moskva River, Russia. The structure consists of
four larger and two smaller tubules in cross-section,
each surrounded by a thin prismatic layer. These
authors interpreted the tubules as remains of blood
vessels. Subsequently, Barskov (1996) re-examined the
same specimen by means of SEM and discovered that
the number of tubules increases from two to six during
ontogeny. Neither a central vein nor a marginal
epithelial layer is preserved in this specimen. As
already described, the number of arteries in the
siphuncle of Nautilus is invariable (two pairs)
throughout the entire length of the siphuncle. These
anomalies plus the absence of any detailed tissue
structure seem to suggest that the `blood vessels' were
formed secondarily during the phosphatization of the
siphuncle.
Functional morphology. ± In living chambered cephalopods (Nautilus, Spirula and Sepia), the siphuncular
epithelium exhibits certain common characteristic
features (Denton & Gilpin-Brown 1961, 1966; Bassot
& Mortoja 1966; Greenwald et al. 1980; Ward et al.
1980; Fukuda et al. 1981; Bandel & Spaeth 1983).
Namely, the epithelia of the three genera all consist of
high columnar cells that change adorally to the cubic
LETHAIA 33 (2000)
cells of the rear mantle. Each cell comprises a
canaliculus which is connected with the underlying
drainage channel. Cytoplasm around the canaliculus
contains numerous mitochondria and microcanals,
the latter of which open into the canaliculus and
drainage channel. Because these histological characteristics are commonly observed in excretory organs of
various animals, Denton & Gilpin-Brown (1973)
proposed that the siphuncular epithelium serves to
concentrate salt, permitting osmotic transfer of liquid
between chambers and blood vessels within the
siphuncle. During active pumping, cameral liquid is
temporally stored within the intracellular duct (=
canaliculus) and is subsequently transported osmotically to the blood vessels via a drainage channel. Since
osmotic emptying by simple osmotic pressure cannot
be applied to Nautilus and Spirula living in waters
deeper than about 400 m, Greenwald et al. (1980)
proposed a modi®ed model (`local osmosis' model)
for cameral liquid transport in Nautilus that stresses
enhanced solute concentrations within the intracellular space.
This report is, to our knowledge, the ®rst reliable
description of ammonoid siphuncular tissue structure
which provides important information on the functional morphology of these animals. The essential
similarity of the microanatomy of the siphuncle
among Akmilleria, Nautilus and Spirula strongly
suggests that ammonoids could control their buoyancy by transferring liquid osmotically between
chambers and blood vessels of the siphuncle.
Acknowledgements. ± We are grateful to R. Hewitt, C. Kulicki, Y.
Fukuda, S. Isaji and an anonymous reviewer for critical discussions
and comments, Y. Miyaji for help in SEM work, and H. Yoshida for
operating EDX analysis. This project was supported in part by the
grant-in-aid of the Japanese Ministry of Education, Science,
Culture and Sports (No. 09304049) to K. Tanabe.
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