Soft-part anatomy of the siphuncle in Permian prolecanitid ammonoids
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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. References AppeloÈf, A. 1893: Die Schalen von Sepia, Spirula und Nautilus. Kongliga Svenska Vertenskaps-Akademiens Handlingar 25, 1± 106. 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