Development of the Embryonic Shell Structure of Mesozoic Ammonoids

2008·19.7 MB·English

by  Kazushige Tanabe

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