PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024 Number 3621, 19 pp., 11 figures, 1 table August 28, 2008 Development of the Embryonic Shell Structure of Mesozoic Ammonoids KAZUSHIGE TANABE,1 CYPRIAN KULICKI,2 AND NEIL H. LANDMAN3 ABSTRACT Exceptionally well-preserved embryonic shells (ammonitellae) of the early Aptian ammonoid Aconeceras cf. trautscholdi Sinzov, 1870, preserved as coprolite remains from Symbirsk, Russia, were examined with scanning electron microscopy (SEM) to investigate the developmental sequence of the embryonic shell structure. Our SEM observations reveal that these shells can be classifiedintothefollowingthreegroupswithdifferentwallmicrostructure:Group1,withathin (ca.5 mm),double-layeredshellwall,consistingofinnerprismaticandouterhomogeneouslayers, theformerofwhichisabsentintheadapicalportionandbecomesthickeradorally;Group2,with a three-layered shell wall that consists of inner prismatic, middle homogeneous, and outer prismatic layers, with tubercles on the outer layer; and Group 3, with a thick nacreous swelling (primaryvarix)ontheanteroventralsideneartheaperture.Themiddlehomogeneouslayerofthe embryonicshellsofGroup2isthesameastheouterhomogeneouslayerinshellsofGroup1and may be composed of amorphous calcium carbonate (ACC). In embryonic shells of Group 3, the middle homogeneous layer is absent and there are voids instead. It may have been transformed intothe inner prismaticlayer orelse dissolvedduring diagenesis. In modern Nautilus and gastropods, embryonic or larval shell development is initiated by the secretion of a cap-shaped, fully organic shell prior to the deposition of calcium carbonate. This stageisnotpreservedinthematerialexamined,butprobablyexistedintheAmmonoidea.Based on our observations and data from extant Nautilus and gastropods, we propose a model for the developmentoftheembryonicshellstructureofMesozoicammonoids,startingfromsecretionof an organic primary shell, followed by deposition of ACC and its transformation into the inner prismatic layer,and terminating in the deposition of a primary varix on the inside of the ventral andventrolateral positionof the shelljust adapicalof the aperture. 1Department of Earth and Planetary Science, University of Tokyo, Hongo 7-3-1, Tokyo 113-0033, Japan ([email protected]). 2Instytut Paleobiologii, Polska Akademia Nauk, ul. Twarda 51/55, PL-00-818, Warszawa, Poland (kulicki@twarda. pan.pl). 3DivisionofPaleontology(Invertebrates),AmericanMuseumofNaturalHistory([email protected]). CopyrightEAmericanMuseumofNaturalHistory2008 ISSN0003-0082 2 AMERICAN MUSEUMNOVITATES NO. 3621 INTRODUCTION capsule as the embryonic shell, and the ammonoid hatched almost simultaneously Reconstruction of the early ontogeny of after the formation of the primary constric- extinct organisms is an important subject in tion. This theory of direct development is paleobiological research. However, this is supported by a number of morphological usually difficult in invertebrates, because features including synchronous changes of remains of embryos and larval soft tissues ornament, shell microstructure, and whorl are very rarely preserved in the fossil record, growth at the primary constriction, as well as except for special circumstances (e.g., phos- discoveries of ammonitellae (e.g., Bandel, phatized soft tissue remains of embryos of 1982, 1986; Landman, 1982, 1985; Kulicki bilateralian animals from the Neoproterozoic and Wierzbowski, 1983; Kulicki and Doushantuo Formation in southern China; Doguzhaeva,1994;Tanabeetal.,1993,1995). Xiaoetal.,1998;butseeBaileyetal.,2007,for Opinions, however, are still unsettled con- an alternative explanation). More commonly, cerning the sequence of embryonic shell only the mineralized hard parts of animals development, as indicated by three different secreted at the embryonic stage are preserved models:(1)accretionarygrowthmodelsimilar as fossils. Ammonoids, which comprise an totheembryonicshelldevelopmentofmodern extinct group of cephalopod mollusks that Nautilus (see Druschits et al., 1977; Druschits floweredintheworld’soceansduringtheearly andDoguzhaeva,1981;Kulicki,1979;Tanabe Devonian to the end of the Cretaceous, are et al., 1980, 1993); (2) ‘‘archaeogastropod’’- examplesofsuchanimals.Asinothermollusk type development model emphasizing that shells, the aragonitic outer shell wall of the embryonic shell was originally organic ammonoids was formed by accretionary (5 nonmineralized) (Bandel, 1982, 1986; growth, so that the embryonic shell prior to Kulicki and Doguzhaeva, 1994); and (3) hatching (synonymous with the ammonitel- endocochliate embryo model arguing that la—defined as the initial chamber and part of Mesozoicammonoidsweretemporarilyenvel- the next whorl with a distinct constriction at oped by the outer reflected mantle late in theaperture—byDruschitsandKhiami,1970) embryonic development (Tanabe, 1989; see is occasionally preserved in the apical shell Landmanetal.,1996:fig.18).Inaddition,the portion, even in medium to large size shells. process of biomineralization of the tubercles Based on microscopic observations of well- on the embryonic shells of Mesozoic ammo- preserved fossil material, ammonoids were noids has not yet been clearly addressed. To previously believed to have undergone a solve these problems, development of the post-hatching larval stage before metamor- embryonicshellstructurewasexaminedbased phosis as do modern gastropods and bivalves on exceptionally well-preserved ammonitellae (e.g., Erben, 1964; Erben et al., 1968, 1969). With increasing knowledge of the early of Early Cretaceous ammonoids that retain ontogeny of modern cephalopods, especially their original aragonitic shell mineralogy and of modern Nautilus (e.g., Uchiyama and microstructure. Tanabe, 1999), recent authors believe that, like modern cephalopods, ammonoids devel- MATERIAL oped directly without a larval stage (e.g., Druschits and Khiami, 1970; Druschits et al., Exceptionally well-preserved ammonoid 1977; Druschits and Doguzhaeva, 1981; embryonic shells from the lower Aptian of Birkelund and Hansen, 1974; Kulicki, 1974, Symbirsk, Volga River Basin, Russia, were 1979, 1996; Tanabe et al., 1980; Tanabe and examinedinthisstudy.Theywerepreservedas Ohtsuka, 1985; Tanabe, 1989; Landman, coprolite remains, together with small bi- 1982, 1985, 1987; Bandel, 1982; Bandel et al., valves, gastropods, and fish scales in a clayey 1982; Westermann, 1996; Klug, 2001; Sprey, calcareous concretion (fig. 1). Immature and 2002).Accordingtothistheory,theearlyshell mature specimens of Aconeceras trautscholdi portion consisting of an initial chamber and a Sinzov, 1870, and fewer specimens of subsequent whorl with a nacreous swelling Deshayesites deshayesi (Orbigny, 1840) are near the aperture was formed within the egg also present in the same concretion. Overall 2008 TANABE ET AL.:EMBRYONIC SHELLSTRUCTURE OFMESOZOIC AMMONOIDS 3 Fig. 1. Embryonic shells of Aconeceras cf. trautscholdi, lower Aptian, Symbirsk, Volga River Basin, Russia. A. Optical micrograph of part of a calcareous concretion, showing the mode of occurrence of embryonicshellspreservedascoproliteremains.UMUTMM29439-1.B.SEMofembryonicshellsonthe brokensurface ofthe concretion. UMUT MM29440-1. 4 AMERICAN MUSEUMNOVITATES NO. 3621 shape and tuberculate micro-ornamentation OBSERVATIONS of the ammonoid embryonic shells are similar to those of embryonic shells described by Based on the microstructure of the shell wall, the absolute thickness of each layer at Kulicki and Doguzhaeva (1994) as A. cf. different shell sites, the total rotation angle of trautscholdi from the same locality. The shells the preserved shell in medially broken speci- were assigned to this species on the basis of mens, and the presence or absence of tuber- their similarity in overall morphology and culate micro-ornamentation, the embryonic internal structure to juvenile and adult shells shells of the present species can be roughly of this species. Accordingly, we refer our classified into the following three groups. ammonoid embryonic shells from Symbirsk to A. cf. trautscholdi. Allspecimensexaminedarepreservedinthe Group 1 University Museum, University of Tokyo This group is represented by poorly miner- (UMUT). alized embryonic shells, all of which possess the following features: (1) absence of a calcified initial chamber wall and tuberculate METHODS micro-ornamentation, (2) shell wall consisting of a homogeneous layer in the adapical In most previous studies, the embryonic portion, and an outer homogeneous layer shell microstructure ofammonoidswas exam- and an inner prismatic layer in the adoral ined in median and cross section after portion, and (3) a short spiral length of the polishing and etching with weak acidic solu- shell without a proseptum, primary varix, or tion (e.g., Erben et al., 1968, 1969; Kulicki, dorsal shell layer. We observed the shell 1979; Kulicki and Doguzhaeva, 1994; Tanabe microstructure and mineralogy of two repre- etal.,1980, 1993; Druschitsand Doguzhaeva, sentative specimens in detail. 1981; Landman, 1982). This method is useful UMUT MM 29441-1 (fig. 2A) is a more or in tracing the change in shell wall microstruc- less medially broken shell with a spiral length ture from the initial chamber to subsequent of approximately 240 degrees. Its maximum whorls, but the details of shell wall micro- diameter is 653 mm, which is comparable to structure are difficult to observe even in that of more well-developed embryonic shells. excellently preserved specimens. For this A calcified initial chamber wall and a dorsal reason, surface ornamentation and wall mi- shell wall are both absent. In addition, this crostructure in our study were mostly ob- specimen lacks a constricted aperture and an servedbyscanningelectronmicroscopy(SEM) associated nacreous deposit (primary varix). (Hitachi S2400 and Philips XL-20) using only The ventral shell wall in the adapical (poste- naturally fractured embryonic shells without rior) portion is extremely thin (1–2 mm) and any chemical or physical treatment. SEM consists only of homogeneous material (h, images were imported to a desktop computer, fig. 2B). This homogeneous layer gradually where measurements of embryonic shell size, thickens adorally (ca. 4 mm thick, point C, rotation angle (5 the angle between line fig. 2A), and, simultaneously, a prismatic segmentsfromthecenterofanimaginarycircle layer develops underneath it (ip, fig. 2C). inscribed inside the embryonic shell and The inner prismatic layer also gradually extending to the adapical and adoral edges increases in thickness adorally (fig. 2D). The of the shell wall), shell wall thickness, and shell wall in the adoral portion is approxi- tubercle size were made using image analyz- mately 5 mm thick (fig. 2D). ing software (Quartz PCI Ver. 4). UMUT MM 29439-2 (fig. 3) is an approxi- To determine the mineralogy of the embry- mately medially broken shell with the outer onic shell layers, we also made quantitative surface partly exposed (fig. 3B). The preserved elemental analyses of shell microstructure by maximum diameter is 640 mm and the spiral means of an energy dispersion X-ray micro- lengthoftheshellisapproximately300 degrees, analyzer (EDAX) attached to the Philips XL- which is slightly longer than that of UMUT 20 SEM. MM 29441-1(fig. 2A). The shell wall at the 2008 TANABE ET AL.:EMBRYONIC SHELLSTRUCTURE OFMESOZOIC AMMONOIDS 5 Fig.2. SEMs of anembryonic shell ofAconeceras cf.trautscholdi belonging to Group1. UMUT MM 29441-1, lower Aptian, Symbirsk, Russia. A. Lateral view of medially broken embryonic shell. B–D. Shell walloftheembryonicshellatadapical(B),middle(C),andadoral(D)portions.Notethattheshellwallat the adapical portion consists of a very thin homogeneous layer, whereas that at the middle and adoral portionsismadeupofhomogeneousandinnerprismaticlayers.Abbreviations:h,homogeneous,possibly amorphouscalcium carbonate layer;ip, innerprismatic layer. apical portion (fig. 3B) is approximately 3 mm Group 2 thickandconsistsofasinglethinhomogeneous layer in the same position as in UMUT MM Embryonic shells of this group are incom- 29441-1(fig. 2B).Athin(ca.2 mmthick)inner pletely mineralized and have approximately prismaticlayerappearsadorallyunderneaththe 1.0–1.5 whorls. A calcified initial chamber homogeneous layer (ip, fig. 3C), which can be wall is not present in specimens representing traced to the preserved apertural end, and earlier growth stages, but a very thin, calcar- maintains a constant thickness (fig. 3D). The eousinitialchamberwallandaproseptumare outer shell surface is slightly rough but lacks both present in specimens representing later anytraceoftubercles(fig. 3C). growth stages. The shell wall is thicker than The elemental composition of the inner that ofthe specimens ofGroup 1 and consists prismatic and outer homogeneous layers in ofthree layers:outer prismatic, middlehomo- UMUT MM 29444-1 is presented in table 1. geneous, and inner prismatic layers, in asso- 6 AMERICAN MUSEUMNOVITATES NO. 3621 Fig. 3. SEMs ofanembryonic shell of Aconeceras cf.trautscholdi belongingto Group 1.UMUT MM 29439-2, lower Aptian, Symbirsk, Russia. A. Lateral view of medially broken embryonic shell. B–D. Shell wall of the embryonic shell at adapical (B, C) and adoral (D) portions. Note that the shell wall at the adapicalend(B)consistsofaverythinhomogeneous,possiblyamorphouscalciumcarbonatelayer,whereas thatattheotherportionsismadeupofouterhomogeneousandinnerprismaticlayers.Theoutersurfaceof the shell wall isbumpy butlacks tubercles. Forabbreviations, seethe explanationof figure 2. TABLE1 Elemental composition ofembryonic shells ofAconeceras cf. trautscholdi. Results ofEDAX analysis(all amounts given asa percentage oftotalweight, wt) SpecimenofGroup1(UMUTMM29444-1) SpecimenofGroup2(UMUTMM29444-2) Innerlayer Outerlayer Middlelayer Outerlayer Tubercle Clayey Element (prismatic) (homogeneous) (homogeneous) (prismatic) (spherulitic) matrix C 9.81 10.27 10.79 10.40 9.72 8.80 O 59.01 59.70 59.11 59.49 51.33 50.36 Na 0.25 0.33 0.40 0.31 0.49 0.26 Mg 0.45 1.94 1.50 0.58 1.56 1.83 Al 0.13 — 0.19 — 0.27 0.54 Si 0.13 0.28 0.28 0.26 0.33 0.78 S 0.14 0.10 0.08 0.08 — 0.24 Ca 28.81 27.17 27.46 28.66 36.20 36.89 Fe 1.27 0.21 0.19 0.21 0.10 0.30 Total(wt%) 100.00 100.00 100.00 99.99 100.00 100.00 2008 TANABE ET AL.:EMBRYONIC SHELLSTRUCTURE OFMESOZOIC AMMONOIDS 7 Fig.4. SEMs of anembryonic shell ofAconeceras cf.trautscholdi belonging to Group2. UMUT MM 29441-3,lowerAptian,Symbirsk,Russia.A.Lateralviewoftheembryonicshell.B–E.Close-upviewsofthe embryonicshellwallatfourdifferentportions.Thewallconsistsofinnerprismatic,middlehomogeneous, andouterprismaticlayers.Abbreviations:op,outerprismaticlayer;t,tubercles.Forotherabbreviations,see theexplanation of figure 2. ciation with tubercles on the outer layer. The appears adorally underneath the homoge- embryonic shells belonging to this group are neouslayer;accordingly,theventralshellwall the most abundant ones in the concretion at this stage is built up of three layers, i.e., slabsexamined.Fourrepresentativespecimens outer prismatic, middle homogeneous, and showing slightly different stages of shell inner prismatic layers (fig. 4C–E). The shell development are described below. wall thickness gradually increases adorally to UMUT MM 29441-3 (fig. 4) is a medially 7–8 mm near the apertural portion (fig. 4E). broken shell, whose spiral length is approxi- The outer surface of the embryonic shell is mately 320 degrees, which is slightly longer ornamented with tubercles. The tubercles, than that of the embryonic shells of Group 1. each about 2 mm in basal diameter and Its maximum diameter is approximately 0.7 mm in height, rest upon underlying prisms 645 mm. As in specimens of Group 1, neither showingpseudohexagonaltrilling, andconsist a calcified initial chamber wall nor a dorsal of irregularly oriented, minute spherulites shell of the first whorl is present. In addition, (fig. 4B, D). this specimen lacks a constricted aperture and UMUT MM 29439-3 (fig. 5) and UMUT a nacreous deposit (primary varix). The shell MM 29439-4 (fig. 6) are almost complete wall near the adapical (posterior) margin is specimens with a primary constriction at the relatively thin (ca. 4.5 mm) and consists of a aperture(arrows,figs. 5A,6).InUMUTMM thin,outerprismaticandthicker,innerhomo- 29439-3, the lateral side of the shell near the geneous layer, 1.0 mm and 3.5 mm thick, aperture was partly removed, allowing us to respectively(fig. 4B).Aninnerprismaticlayer document that the shell wall at this point 8 AMERICAN MUSEUMNOVITATES NO. 3621 Fig. 5. SEMs of an embryonic shell of Aconeceras cf. trautscholdi belonging to Group 2 with a constricted aperture. UMUT MM 29439-3, lower Aptian, Symbirsk, Russia. A. Lateral view of the embryonicshellpartlyexposedonthefracturedsurfaceofacarbonateconcretion.Thearrowpointstothe constrictedaperture.B.Close-upofthelateralsideoftheinitialchamberportionwithouttubercles.C.Shell wall microstructure consisting of inner prismatic, middle homogeneous, and outer prismatic layers on the ventralsideofthefirstwhorl.D.Shellwallmicrostructureconsistingofathinouterprismaticlayernearthe primary constriction. Forabbreviations, seethe explanationsof figures 2and 4. consists only of a thin outer prismatic layer on the venter near the aperture in UMUT (op, fig. 5D), and lacks a nacreous primary MM 29439-4 (fig. 6). varix.AsinUMUTMM29441-3(fig. 4C–E), UMUTMM29442-1(fig. 7)attains760 mm the ventral shell wall of this specimen is triple in median diameter and consists of an initial layered, consisting of outer prismatic, middle chamber and a subsequent whorl of approx- homogeneous, and inner prismatic layers imately 230 degrees spiral length (fig. 7A). (fig. 5C). Tubercles occur irregularly on the The initial chamber wall is extremely thin exposed surface of the shell, but they are (ca. 0.6–0.8 mm thick) and consists of a single absent on the lateral surface of the initial prismatic layer (ip, fig. 7B–D). This prismatic chamberinUMUTMM29439-3(fig. 5B)and layer extends adorally and is the inner 2008 TANABE ET AL.:EMBRYONIC SHELLSTRUCTURE OFMESOZOIC AMMONOIDS 9 Fig.6. SEMofanembryonicshellofAconecerascf.trautscholdibelongingtoGroup2withaconstricted aperture (ventrolateral view). UMUT MM 29439-4, lower Aptian, Symbirsk, Russia. Note that minute tubercles are absentonthe ventrolateral side of the firstwhorl. Abbreviation: pc,primary constriction. prismatic layer of the succeeding shell wall UMUT MM 29443 (fig. 8D–F) lacks a (fig. 7F,G).Atthebaseoftheinitialchamber, complete aperture and may also belong to a distinct proseptum is visible (ps, fig. 7F). this group. In this specimen, a single tubercle The shell wall abruptly thickens on the does not always cover an individual prism, adapical side of the proseptum (fig. 7E) and, and two contiguous tiny tubercles are occa- thereafter, maintains a constant thickness (ca. sionallydeveloped onasingleprismatictablet 5 mm) in the succeeding first whorl (fig. 7F– showing pseudohexagonal trilling (fig. 8F). H).Thisspecimenappearstorepresentalater The elemental composition of UMUT MM growth stage than UMUT MM 29441-3 29444-2ispresentedintable 1.Theresultsare (fig. 4), in having a longer spiral length and similar to those for the embryonic shell in the presence of a proseptum. In this belonging toGroup1(UMUTMM29444-1). specimen, only inner and outer prismatic layers in association with tubercles on the Group 3 outer layer are visible, and a middle homoge- neous layer cannot be distinguished (fig. Embryonicshellsofthisgroupconsistofan 7E–H). initialchamberandasubsequentwhorlwitha 10 AMERICAN MUSEUMNOVITATES NO. 3621 Fig. 7. SEMs of an embryonic shell of Aconeceras cf. trautscholdi belonging to Group 2 in medial section. UMUT MM 29442-1, lower Aptian, Symbirsk, Russia. A. Overall view of the medially sectioned embryonicshell.B–H.Close-upviewsoftheembryonicshellwallatsevendifferentportions.Theshellwall ofthefirstwhorlisfullymineralizedandconsistsofinnerandouterprismaticlayers,whilethatoftheinitial chamber is poorly mineralized, consisting only of a very thin inner prismatic layer. The proseptum (ps) is developedat thisstage (see F);for otherabbreviations,seethe explanations of figures2 and 4. constricted aperture in association with a 4 mm) at the connecting portion (5 umbilical nacreous varix. They are relatively rare in shoulder) with the subsequent whorl (fig. 9B). the concretion slabs examined. Micro- A dorsal prismatic layer and a nacreous structural features of one representative spec- deposit (primary varix) near the aperture are imen are described below. both observable (dp and n, respectively, UMUT MM 29442-2 (fig. 9) appears in fig. 9B). The ventral shell wall of the first oblique cross section on the polished concre- whorl, approximately 6 mm thick, is double tionslab.Theinitialchamberwallisextremely layered, consisting of outer and inner pris- thin (ca. 1 mm thick) in the adapical portion matic layers, without any trace of a middle butrapidlyincreasesinthicknessadorally(ca. homogeneous layer. UMUT MM 29440-2