Volume 274, Number 3, March 2013
J
O
U
R
N
A
L
O
F
ISSN 0362-2525
Editor: J. Matthias Starck
JOURNAL OF MORPHOLOGY 274:243–257 (2013)
Skeletal Ontogeny in Basal Scleractinian
Micrabaciid Corals
Katarzyna Janiszewska,1 Jakub Jaroszewicz,2 and Jarosław Stolarski1*
1
2
Institute of Paleobiology, Polish Academy of Sciences, PL-00-818 Warsaw, Poland
Faculty of Materials Science and Engineering, Warsaw University of Technology, PL-02-507 Warsaw, Poland
ABSTRACT The skeletal ontogeny of the Micrabaciidae, one of two modern basal scleractinian lineages, is
herein reconstructed based on serial micro-computed tomography sections and scanning electron micrographs.
Similar to other scleractinians, skeletal growth of micrabaciids starts from the simultaneous formation of six
primary septa. New septa of consecutive cycles arise
between septa of the preceding cycles from unique
wedge-shaped invaginations of the wall. The invagination of wall and formation of septa are accompanied by
development of costae alternating in position with septa.
During corallite growth, deepening invagination of the
wall results in elevation of septa above the level of a
horizontal base. The corallite wall is regularly perforated thus invaginated regions consist of pillars inclined
downwardly and outwardly from the lower septal margins. Shortly after formation of septa (S2 and higher
cycles) their upper margins bend and fuse with the
neighboring members of a previous cycle, resulting in a
unique septal pattern, formerly misinterpreted as ‘‘septal
bifurcation.’’ Septa as in other Scleractinia are hexamerally arranged in cycles. However, starting from the quaternaries, septa within single cycles do not appear simultaneously but are inserted in pairs and successively flank
the members of a preceding cycle, invariably starting
from those in the outermost parts of the septal system. In
each pair, the septum adjacent to older septa arises first
(e.g., the quinaries between S2 and S4 before quinaries
between S3 and S4). Unique features of micrabaciid skeletal ontogeny are congruent with their basal position in
scleractinian phylogeny, which was previously supported
by microstructural and molecular data. J. Morphol.
274:243–257, 2013. Ó 2012 Wiley Periodicals, Inc.
KEY WORDS: basal
Scleractinia;
skeletal ontogeny; microtomography
Micrabaciidae;
INTRODUCTION
Recent molecular studies revealed that solitary
and exclusively azooxanthellate Micrabaciidae and
Gardineriidae form the most deeply diverging
clade of scleractinian corals (Kitahara et al., 2010;
Stolarski et al., 2011). According to relaxed molecular clock analyses calibrated by scleractinian fossils, the basal clade splits deeply in the Palaeozoic,
around 425 Ma. One can expect that skeletal features of corals with such a long and separate evolutionary history may differ from those of other
recent Scleractinia. Indeed, Stolarski (1996) proved
Ó 2012 WILEY PERIODICALS, INC.
that the skeletal architecture of gardineriids (i.e.,
by the presence of thick, exclusively epithecal
wall) is distinctly different from that of other
modern corals. In turn, Janiszewska et al. (2011)
showed that micrabaciid thickening deposits
(structures forming one of the main microstructural regions in scleractinian skeletons; see Stolarski, 2003) are composed of an irregular meshwork
of short and thin fibers organized into small, chiplike bundles, what distinguishes them from other
Scleractinia.
Micrabaciids form cupolate skeletons (up to 5 cm
in diameter) with a peculiar lace-like pattern of
septa, costae, and porous corallum wall (Moseley,
1876; Squires, 1967; Cairns, 1989). Calices are
everted, often with distinct calicular rim (marginal
shelf; see Cairns, 1989), and with septa growing
upwards and outwards from the corallum centre.
Septa are arranged in a distinct flower-like pattern
of oval chambers around the columella (Moseley,
1881). Repeatedly branching costae correspond
with the number of septa and alternate in position
with them (Wells, 1933). The arrangement of septa
as observed in adult coralla suggests formation by
symmetrical division of septa of the preceding
cycle. This lead Cairns (1982, 1989, 1995, 2001;
Cairns and Zibrowius, 1997) to propose that the
micrabaciid septal system consists of members of
the first two cycles and multiple bifurcations of
Additional Supporting Information may be found in the online
version of this article.
Contract grant sponsor: European Regional Development Fund
(Innovative Economy Operational Programme); Contract grant number:
POIG.02.02.00-00-025/09; Contract grant sponsor: National Science
Centre (Poland); Contract grant number: DEC-2011/03/N/ST10/06471
(K.J.); Contract grant sponsor: European Union SYNTHESYS; Contract
grant number: NL-TAF-947 (J.S.).
*Correspondence to: Jarosław Stolarski; Institute of Paleobiology,
Polish Academy of Sciences, PL-00-818 Warsaw, Poland.
E-mail: stolacy@twarda.pan.pl
Received 11 August 2012; Revised 28 August 2012;
Accepted 2 September 2012
Published online 15 October 2012 in
Wiley Online Library (wileyonlinelibrary.com)
DOI: 10.1002/jmor.20085
244
K. JANISZEWSKA ET AL.
the Laboratory of Microtomography, Institute of Paleobiology,
Polish Academy of Science, Warsaw. Voltage, current, and number of projections were varied depending on the type of sample
(density, skeletal size etc.). Radial projections were reconstructed with Skyscan NRecon and XMReconstructor (for XRadia data) software. The 3D images of corallites and serial
micro-CT sections were obtained with Skyscan Data Viewer and
Avizo software, respectively.
Skeletal micromorphology was visualized using a scanning
electron microscope (SEM). The specimens were first sputter
coated with platinum and then photographed with a Philips XL
20 SEM in the Institute of Paleobiology PAS, Warsaw.
Terminology
Fig. 1. Diagrammatic representation of one system of septa
(solid lines) and costae (dotted lines) in Leptopenus discus.
According to Cairns, higher order septa arise by branching of the
third cycle septa. Successive bifurcations of tertiaries were desigIII
nated as SI3 , SII
3 , and S3 . Figure adapted from Cairns 1982.
tertiary septa (Fig. 1). This model was consistently
applied for 30 years despite it being based mostly
on adult specimens with fully developed septal
cycles. Thus, the goal of this article is to clarify
the nature of the micrabaciid skeletal ontogeny
based on a series of specimens in various stages of
growth and their serial sections.
MATERIAL AND METHODS
Material
We have examined all the micrabaciid genera: recent representatives of Leptopenus Moseley (1881), Letepsammia Yabe and
Eguchi (1932), and Rhombopsammia Owens (1986b), both recent
and fossil representatives of Stephanophyllia Michelin (1841),
and known only from the Cretaceous Micrabacia Milne-Edwards
and Haime (1849). Despite the differences between micrabaciid
taxa (the robust skeleton of Micrabacia vs. fragile Leptopenus,
different number of septa in adult specimens, porosity of septa,
etc.), they share the same arrangement of septa and costae.
Thus, to propose a general model of micrabaciid ontogeny, we
selected specimens that most accurately show the successive
phases of corallite growth, regardless of their generic affiliation.
The taxonomic details are given in figure captions, whereas locality data are provided in Supporting Information, Table S1.
Museum abbreviations: NMNH—National Museum of
Natural History, Smithsonian Institution, Washington, D.C.;
RMNH—Netherlands Centre for Biodiversity Naturalis, formerly Rijksmuseum van Natuurlijke Historie, Leiden; ZPAL—
Institute of Paleobiology, Polish Academy of Sciences.
Methods
The micrabaciid coralla were scanned with a micro-computed
tomography (micro-CT) system. Radial projections were then
used to reconstruct virtual slices and three-dimensional (3D)
models of corallites. Thus, thin sections (traditionally used in
studies of coral ontogeny) were replaced by serial micro-CT sections (microtomograms). To interpret the septal insertion pattern, horizontal (perpendicular to the corallite axis) sections
were used.
Micro-CT data were collected with Skyscan 1172 at the Faculty of Materials Science and Engineering, Warsaw University
of Technology system and with XRadia MicroXCT-200 system in
Journal of Morphology
To date, the terminology used for descriptions of mostly adult coralla of micrabaciids has been largely adopted from those describing
skeletal structures of other scleractinians. Our ontogenetic observations of micrabaciid coralla show, however, that the formation
and structure of some of the skeletal elements are very different
from traditional interpretations. The following glossary provides
an overview of the terminology used previously and herein
(including new terms) for micrabaciid skeleton descriptions.
Costa (plural: costae). Radial structure outside the corallite
wall. Usually, costae appear as prolongations of septa (Budd
and Stolarski, 2011). However, in a few genera (e.g., micrabaciids, turbinoliids: Idiotrochus and Dunocyathus) costae alternate in position with septa (Cairns, 1989); costae-like structures protruding outside the calice outline, but formed as convexity of the wall are called crests and occur in some
flabellids (Stolarski, 1995).
Septum (plural: septa). Radially arranged longitudinal partition
of corallite, in Scleractinia hexamerally arranged in cycles.
New septa are inserted between members of the preceding
cycle. Septa of successive cycles are designated as primaries,
secondaries, tertiaries, quaternaries etc. (abbreviated S1, S2,
S3, S4, respectively). Septum S1 and all septa between it and
adjacent septum S1 (comprising one-sixth of a corallite) form
a system of septa. According to Cairns (1982, 1989), new septa
in Micrabaciidae arise from the division of the preexisting
septa of the third cycle. Thus, he introduced a new notation, in
which the septal system in Micrabaciidae consists of septa of
the first (S1) and second (S2) cycles and multiple bifurcations of
the third cycle designated as S3’, S3’’, S3III, S3IV, S3V, and S3VI
(Fig. 1). The data presented in this article show that micrabaciid
septa are not formed by bifurcation, but are inserted separately
from the neighboring septa (Fig. 2B); therefore the ‘‘traditional’’
notation of septa is used. Septa within a single cycle do not appear
simultaneously, thus roman numerals are used to show the minor
differences between the time of septal formation, for example, for
quinaries: S5I, S5II, S5III, S5IV, whereby S5I appear as first.
Synapticula (plural: synapticulae). Rod or bar-like structure connecting opposing faces of adjacent septa and perforating mesenteries between them; synapticulae are formed by joining of two
granules growing toward each other from adjacent septa (Budd
and Stolarski, 2011; Jell, 1974; Nothdurft and Webb, 2007)
Synapticulotheca. Corallite wall formed by one or more rings of
synapticulae (Wells, 1956)
Pillar (new term). Bar-like structure, which is a part of invaginated micrabaciid wall; converse to synapticulae, pillars
growth simultaneously with the formation of septa and appear
in pairs (thus plural form—pillars—is herein most frequently
used (see also Discussion).
Wall (or theca). Skeletal deposit enclosing the column of the polyp
and uniting the outer edges of septa (Wells, 1956).
RESULTS
Formation of Septa
New septa are formed on the wedge-shaped
invaginations of the wall between septa of the
SKELETAL ONTOGENY OF MICRABACIIDS
245
Fig. 2. Early stage of septal growth in recent Leptopenus (ZPAL H.25/7-576): (A) enlarged in (B) lateral and (C) distal view of a
corallite fragment. New septum is formed on invagination of wall between septa of preceding cycles; invaginated parts of the wall
composed of two sets of pillars inclined downwardly and outwardly from the lower septal margin. Upper margin of septum curves
toward neighboring member of a lower cycle; (B) desmocyte attachment scars (arrows) cover an inner part of the wall. (D) proximal
view of a corallite (fragment of the same specimen): costae composed of two rows of granules outlining the invaginations of wall
and alternating in position with septa. (SEM micrographs).
preceding cycle (Fig. 2). In its invaginated parts,
the wall is composed of two sets of pillars inclined
downwardly and outwardly from the lower septal
margins (Fig. 4C). In the course of corallite growth
(from the centre of the base) and deepening invagination of the wall, the lower margins of septa are
gradually lifted above the level of the horizontal
base. In the early stages of growth, septa are not
connected to neighboring septa (Figs. 2B,C, and
5C). However, their upper margins strongly bend
toward the adjacent septa (Fig. 2B) and, in the
next stage of growth, join the nearest members of
a former cycle. This connection occurs shortly after
the formation of septa, thus, usually independent
septal blades are not observed in adult skeletons,
unless last-cycle septa are still in the process of
completion. The pseudobifurcate septal pattern
observed in most specimens is the outcome of the
ontogenetic development of septa, which in the
earliest growth phases occur as separated blades.
Because the neighboring septa are fused in the
juvenile stages of growth, the septa of consecutive
cycles in adult coralla are morphologically indistinguishable from each other (Fig. 3E).
In addition to pillars which are herein recognized as parts of the invaginated wall, the bar-like
elements connect faces of opposite septa in the
upper parts of a corallite (Figs. 4A and 5C,F).
Those structures, representing typical synapticu-
lae, arise after the formation of septa and grow
perpendicular to the septal planes (Fig. 5F).
Although various micrabaciid taxa may differ in
porosity of septa (highly porous septa of Letepsammia vs. imperforate in Rhombopsammia; Cairns,
1989), their common features are a series of oval
foramina between the lower edge of each septum
and regularly arranged pillars and costae (e.g.,
Fig. 2A). The inner part of the wall between septa
is covered with rows of oval depressions. These
shallow pits, few tens of micrometers in diameter,
are arranged parallel to the septal planes (Figs.
2B and 5H).
Costae
The outer part of the micrabaciid wall is covered
with granules or ridges forming radially arranged
costae. Granules occur along the edges of wall
invaginations which, as described above, are the
regions where the new septa are formed (Figs. 2D
and 5E,I). Because the new septa appear at the
top of each invagination, costae alternate in position with septa. Formation of septa and simultaneous invagination of the wall occurs in the interseptal spaces (Fig. 5H); thus costae associated with
previous cycles of septa divide symmetrically and
two rows of granules outline the new invaginations. In this way, the bifurcate pattern of costae
Journal of Morphology
246
K. JANISZEWSKA ET AL.
Fig. 3. Cretaceous Micrabacia in different stage of skeletal development. (A–C) specimen (ZPAL H.II/9-36) with 36 fused septa
in (A) distal and (B) proximal view and (C1–C5) horizontal micro-CT sections. (D–F) Adult specimen (ZPAL H.II/10-38) having 96
septa: (D1–D5) micro-CT sections of a corallite, (E) distal and (F) proximal view. (G–I) specimen (ZPAL H.II/11-449; enlarged in Fig.
4) with 24 septa: (G1–G5) micro-CT sections, (H) distal and (I) proximal view. Solid central part of the base in all specimens (B,F,I)
is disrupted by 12 invaginations of wall reflecting arrangement of first two cycles of septa on the other side of the base. In horizontal micro-CT sections (C1,D1,G1) first cycle septa, formed on wedge-shaped invaginations of wall, are visible as six V-shaped structures. (A,B,E,F,H,I. SEM micrographs).
Journal of Morphology
SKELETAL ONTOGENY OF MICRABACIIDS
247
Fig. 4. Early juvenile Cretaceous Micrabacia sp. (specimen ZPAL H.II/11-449): (A) distal view of a corallite; septa of three cycles
arranged in typical micrabaciid fashion—septa of higher cycle fused with adjacent members of a lower cycle by their inner margins.
Synapticulae connect first and third cycle septa (arrows), columella unites inner ends of primaries (S1). (B) proximal view; 12 porous invaginations of wall reflect arrangement of first two septal cycles. (C) lateral view; septa ‘‘supported’’ on oblique pillars of
wall, costae alternating with septa. (SEM micrographs).
emerges (Figs. 5E,I and 6E, Supporting Information, Fig. S1B). The number of costae is always
equal to the number of septa. Division of costae
(Fig. 5E) coincides precisely with the formation of
incipient septa (Fig. 5C) on the other side of the
base.
Double ridges forming the marginal parts of
costae in juvenile Stephanophyllia (Fig. 5I) correspond to two sets of pillars, each associated with a
different invagination and formation of another
septal cycle. Costal ridges that appear on the sides
of younger (higher cycle) septa are a little less
developed than their counterparts on the sides of
older (lower cycle) septa, which results in asymmetrical ornamentation of costae (Fig. 5G). At the
calicular rim of specimens with incomplete septal
cycles that are often bifurcated or have split ends
of costae can be discerned (Figs. 6F and 7D). These
structures represent incipient skeletal modifications, which during further growth would be followed by invagination of the wall and formation of
septa (Fig. 6D).
Micrabaciid taxa differ in thickness and ornamentation of costae. In taxa with thick costae (e.g.,
Leptopenus: Fig. 2D, Stephanophyllia: Fig. 7C,D),
two separate rows of granules (each corresponding
to one set of neighboring pillars) outline the wide
portions of nonporous horizontal wall. In the genera with a more porous base (Letepsammia: Fig.
6B,E; Supporting Information, Fig. S1B; Rhombopsammia: Supporting Information, Fig. S4B), the
wall between invaginations is reduced to linear
elements, covered with one row of granules located
directly at the junction of two neighboring sets of
pillars (Fig. 6F, Supporting Information, Fig. S1C).
In juvenile Micrabacia (Figs. 3B,F, and 4B),
there are no well-defined ridges of costae, but the
horizontal parts of the wall between invaginations
have slightly elevated margins. A nonporous wall
with a cornflower outline forms the central part of
the base. In the next stages of growth, outward
from the corallite axis, the base becomes more porous and only fragile linear structures of costae
are discerned (Fig. 3B,F).
Micrabaciid costae, together with concentric
rows of pillars form the characteristic porous base
of a corallite (e.g., Figs. 5D, 6B, 7CD, and 8C). In
all examined specimens, the small (1–2 mm in diameter) central part of the base has a nonporous
surface with no trace of attachment (Figs. 6C and
7C, Supporting Information, Fig. S1B). With
increasing corallum diameter, the solid, compact
structure of the base is disrupted by wall invaginations associated with pores. The consecutive invaginations of wall, accompanied with bifurcation of
costae, reflect the order of formation of septa and
allow recognition of septa of successive cycles even
if they do not differ in size or ornamentation (Fig.
4B, Supporting Information, Figs. 2, 3, and 4). The
youngest of two neighboring septa is the one in
the youngest (farthest from the centre) fork of costae (Figs. 6B and 7D, Supporting Information, Fig.
S1).
Septal Insertion Pattern
The septal insertion pattern in Micrabaciidae is
herein interpreted based on a series of specimens
(SEM observations) and virtual sections (microCT). As described above, the septal formation
occurs on the invaginations of wall between septa
of preceding cycles, and not by bifurcations of third
cycle septa. Thus, the traditional notation of sclerJournal of Morphology
248
K. JANISZEWSKA ET AL.
Fig. 5. Arrangement of septa in juvenile Miocene Stephanophyllia. (A–E) specimen ZPAL H.27/1-3 (S. elegans) with four cycles
of septa: (A1–A4) horizontal micro-CT sections; note solid central part of a base (A1). (B,C) distal and (D,E) proximal view of a corallite. Arrows indicate incipient septa of fifth cycle (C) corresponding to bifurcation of costae on the other side of the base (E). (F–I)
specimen ZPAL H.27/2-14 (Stephanophylllia sp.): (F, enlarged in H) desmocyte attachment scars (arrows) cover inner part of the
wall between adjacent septa. Note the onset of wall invaginations in the peripheral part of a corallite (arrowheads). In the upper
part of a corallite, synapticulae connect faces of neighboring septa (e.g., F-asterisk). (G) lateral and (I) proximal view; different
time of invagination (formation of pillars) result in asymmetrical ornamentation of corresponding costae (arrowheads); (B-I. SEM
micrographs).
actinian septa is used to designate septa of successive cycles in micrabaciids.
Scanning electron microscope. The youngest
of the specimens studied herein has three cycles of
septa (Figs. 3G–I and 4, Supporting Information,
Fig. S1). The secondary septa are inserted between
Journal of Morphology
septa of the first cycle and septa of the third
cycle—between first and second cycle septa. Secondaries join adjacent primaries with their upper
margins. Two S2 join one S1, the opposite S1
remains free, and each one of the remaining S2’s
joins one of the four S1’s (Fig. 4A). The bilateral
SKELETAL ONTOGENY OF MICRABACIIDS
249
Fig. 6. Arrangement of septa in recent specimen of Letepsammia formosissima (ZPAL H.25/21-621) with 60 septa: (A) distal and
(B) proximal view of a corallum; bifurcations of costae reflects septal insertion pattern (dotted lines). (C) close-up to the solid central part of the base. (D–F) new septa (first two quinaries in each system) appear between bifurcate ends of a costae (arrows) (C–F.
SEM micrographs).
symmetry of the corallite, now gently accentuated,
is emphasized in the next stages of growth by the
elongated columella, developing at the junction of
the primaries (Figs. 3A,E, 5B, and 8B). The third
cycle is comprised of 12 septa. Pairs of tertiaries
join each S2. In the subsequent step (36 septa),
the first 12 quaternary septa appear in the spaces
next to primaries and join S3’s at their upper/inner
margins (Fig. 3A–C). In micrabaciids with a complete fourth cycle of septa (48 septa), the S4’s adjacent to primaries join the S3’s closer to the corallite axis than the S4’s growing in spaces between
S3 and S2 (Figs. 5A and 6B).
In the next stage of skeletal growth (60 septa,
see Fig. 6), the first quinaries arise in the spaces
between S1 and S4. The next 12 quinaries appear
on either side of these S4’s (based on Cairns’ 1982
drawing of Leptopenus but modified using traditional notation; Fig. 1). Again, younger septa
(those between S3 and S4) join quaternaries further from the axis than septa of the same cycle
formed beside S1. In the case of the specimens
with 84 septa, quinaries develop also between S2
and S4 (Fig. 7). In accordance with the previous
pattern, these 12 quinary septa join quaternaries
farthest from the corallite axis. In a juvenile specimen with an incomplete fifth cycle of septa (lack of
septa between S3 and S4 adjacent to S2), quinaries
differ in height and thickness (septa adjacent to
primaries are higher and thicker than septa
between S4 and S3 and between S2 and S4). Also
neighboring septa differ in thickness and development of ornamentation (Fig. 7F).
Despite the incompleteness of the fifth cycle of
septa in juvenile Letepsammia (the lack of septa
between S3 and S4), 12 septa in the spaces
assigned to S6 are discerned (septa appear in the
interseptal spaces closest to the primaries; Supporting Information, Fig. S2). If four S6’s are present in the septal system (specimens with 120
septa—Supporting Information, Fig. S3), S6 septa
adjacent to primaries join S5’s closer to the center
of a corallite than S6’s inserted between S5 and
S4. In Micrabaciidae with 144 septa (Supporting
Information, Fig. S4), pairs of S6’s flank S5 septa
lying in the next (in the direction from primaries)
spaces. Septa between S3 and S5 join quinaries
closer to the corallite center than S6’s inserted
between S5 and S4.
Depending on the species, coralla of adult micrabaciids consist of 96 to 144 septa (with equal numbers of costae), arranged in up to 6 cycles (the last
incomplete). Cairns and Zibrowius (1997) mentioned one specimen of Letepsammia with 228
septa (that suggests the occurrence of a seventh,
incomplete cycle of septa).
Journal of Morphology
250
K. JANISZEWSKA ET AL.
Fig. 7. Arrangement of septa in recent specimen of Stephanophyllia complicata (RMNH Coel. 23396) comprising of 84 septa
(fifth cycle incomplete).: (A1–A5) horizontal micro-CT sections; note 12 notches in the spaces lacking last septa of fifth cycle (A5arrowheads). (B) distal and (C) proximal view, enlarged in (D)—bifurcation pattern of costae reflects arrangement of septa on the
other side of the base (dotted lines). Arrowheads indicate places that lack quinaries between S3 and S4– note splitted ends of costae; (E, enlarged in F—SEM micrograph) lateral view; neighboring septa are different in thickness and size of ornamentation.
Note also differences in size of quinaries.
Virtual micro-CT sections. The sections of a
lower part of corallites show six radially arranged
V-shaped elements (Fig. 3C1,D1, and G1). In the
upper sections, these elements are replaced by
Journal of Morphology
simple linear structures. According to our SEM
observations, these elements are invaginations of
wall which, in the upper part of a corallite, continue as unbranched septal blades. In a series of
SKELETAL ONTOGENY OF MICRABACIIDS
251
Fig. 8. Arrangement of septa in recent specimen of Stephanophyllia complicata (ZPAL H.25/22-635) with 96 septa (five complete
cycles): (A1–A6) horizontal micro-CT sections of corallite (one system of septa was bold), (B) distal and (C) proximal view of a skeleton; (D) diagrammatic representation of one system of septa based on A4 section.
sections, septa of the first cycle appear simultaneously and merge in the centre of a corallite. In the
upper sections, septa of the second cycle are visible
between primaries. At first free and strongly
curved toward adjacent septa of a former cycle, the
secondaries finally join the primaries revealing the
bilateral symmetry of the corallite (one pair of S2
join one of primaries, an opposite S1 remains free,
the other four S2 join each remaining S1; Figs.
3C4, 7A3, and 8A2,3). The pattern of septal appear-
ance in the subsequent sections of juvenile corallites corresponds with those from the lowest
(oldest) parts of the skeletons in the later stages of
growth.
Twelve third cycle septa appear between septa of
the first and second cycle (Figs. 3C3, D3, and 8A2).
The S3 septa are at first straight and free, but
strongly curve toward the nearest S2 in the upper
part of a corallite (Fig. 3C4, D4). In the next sections, pairs of tertiaries join secondaries. AfterJournal of Morphology
252
K. JANISZEWSKA ET AL.
wards, 12 quaternaries appear between S1 and S3
and, in the upper sections, another 12 S4 between
S2 and S3. Twenty-four septa of the fourth cycle
join neighboring tertiaries (S4 appearing in the
lower part of a skeleton join S3 closer to the corallite axis).
The fifth cycle comprises of 48 septa. Initially, 12
S5 septa appear adjacent to primaries and join S4
septa closest to the corallite axis. Then, the quinaries between S4 and S3 arise followed by quinaries
adjacent to secondaries. The septa located between
S3 and S4 (closer to secondaries) are located furthest from the axis, and last in the subsequent sections (Figs. 3D and 8A4,D). In juvenile specimen
with incomplete fifth cycle of septa, the 12 spaces
that ‘‘lack’’ of the last quinaries (septa between S3
and S4) are clearly visible (Fig. 7A5).
The micro-CT sections (Figs. 3C5,D5, 7A5, and
8A5,A6) also exhibit regularly spaced connections
between adjacent septa, arranged perpendicular to
the septal planes. On the basis of these sections, it
is not possible to interpret their origin (whether
they were formed by granules growing toward one
other from faces of opposite septa), but, based on
SEM observations, they are interpreted as true
synapticulae.
Micrabaciid costae are arranged almost horizontally, thus the data provided by micro-CT scanning
are similar to SEM micrographs of the basal part of
the corallite described above. Costae are radially
arranged in the interseptal spaces. The bifurcation
pattern of costae corresponds to insertions of septa in
slightly upper sections of a corallite (Fig. 8A2–A3).
DISCUSSION
Formation of Septa, Costae and the Nature of
the Corallite Wall
The most important outcome for scleractinian
taxonomy is the observation that micrabaciid septa
do not form by repeated peripheral branching of
septa. Instead, they are formed in the peripheral
zone of a corallite, on the invaginations of the wall
between septa of preceding cycles (Fig. 9A). During
the course of corallite growth, series of oval foramina appear between the lower margins of septa,
regularly arranged pillars and costae, giving the
wall a porous character (Fig. 2B and 9C,E,F).
According to Moseley (1881, p 203), ridges of soft
tissue located in the intercostal grooves connect
with the bases of mesenteries lying above the costae through these foramina (interpreted as ‘‘perforations’’ in the base). Indeed, the inner part of the
wall in the interseptal spaces (of both fossil and
recent micrabaciids) bear shallow pits arranged in
zones parallel to the septal planes (Figs. 2B and
5H). Similar structures, called desmocyte attachment scars, occur in many other scleractinians and
correspond with the position of mesenteries in living polyps (Wise, 1970; Muscatine et al., 1997).
Journal of Morphology
The above observations challenge previous interpretations of the micrabaciid wall. The corallite
wall (often called the base, e.g., Stephenson, 1916)
was described as regularly perforated and composed of numerous concentric and radial trabeculae (Moseley, 1881; Duncan, 1884; Fowler, 1888).
Concentric trabeculae were next interpreted as
synapticular rings, and the wall, consequently, as
synapticulothecal (Owens, 1986b; Cairns, 1989;
Baron-Szabo, 2008). Our observations show that
skeletal ‘‘rings’’ are parts (pillars) of invaginated
wall that grow simultaneously with septa, in contrast to synapticulae which develop as a result of
fusion of granulation of two opposite septa (Wells,
1956). Therefore, growing in structural continuity
with septa, the micrabaciid wall is not synapticulothecate as formerly suggested (Duncan, 1884;
Stephenson, 1916; Squires, 1967; Cairns, 1989) but
bears resemblance to a marginotheca in flabellids
and traditional caryophylliids (Mori and Minoura,
1980; Stolarski, 1995). Moreover, formation of
septa in flabellids is preceded by ‘‘inward warping’’
of the wall (Mori and Minoura, 1980: 323), similar
to that in Micrabaciidae (‘‘invagination of wall’’).
Concentric rows of pillars, representing the successive stages of base growth (Figs. 3B,F, 5B,
7A3,C, and 8C) may be analogous to thecal rings
known from corals attached to substrata (Durham,
1949). However, even the oldest, central part of a
base in juvenile specimens has a nonporous
smooth surface with no trace of attachment (Figs.
6C, Supporting Information, Fig. S1B). The micrabaciid basal plate has not been observed so far and
further studies (and findings) are required to decipher the initial phase of corallum growth. The
main difficulty is that micrabaciid polyps completely enwrap the corallum (Cairns, 1989), and
the initial stages are entirely overgrown by the
skeleton secreted during subsequent growth steps.
The specimens examined so far do not show any
type of different substrate (sand grain or the shell
fragment) than is observed in some other corals as
initial substrate (Cairns, 1989).
The micrabaciid costae are formed along the
edges of wall invaginations. As the septa develop
at the top of invaginations, micrabaciid costae
alternate in position with septa (Figs. 2D, 6C, and
9A,C,E,F), instead of being their prolongations as
in the majority of Scleractinia. Wells (1933) considered costae as formed by the fusion of two sets of
synapticulae (skeletal elements herein recognized
as pillars of invaginated wall). Indeed, when costae are narrow, single rows of granules seem to be
formed directly at the junction between two adjacent sets of pillars (Fig. 6C, Supporting Information, Figs. 2B and 3B). However, in species with
broader costae, invaginations are clearly separated
by wide fragments of nonporous horizontal wall
(Figs. 2D, 4B,C, and 7D), thus there is no fusion
between neighboring sets of pillars.
SKELETAL ONTOGENY OF MICRABACIIDS
253
Fig. 9. Model of septal growth and insertion pattern in Micrabaciidae. (A) Incipient septum arises at the top of invagination of
wall; granules arranged along the edges of invagination form costae. The invaginated part of the wall is composed of two sets of pillars that raise the septum above the level of a base. In the next stages of growth, septum bends toward adjacent septum of a former cycle (C, F—oblique view) and joins it by its upper margin (E). (B,D) Diagrammatic representation of one system of micrabaciid septa: according to Cairns (1982) higher cycle septa arise by branching of the third cycle septa; septa of the first cycle remain
free (B—adapted from Cairns, 1989; modified). In contrast, according to the model proposed herein (A,C–F), septa of successive
cycles are inserted as independent blades; pseudo-bifurcate pattern is an effect of fusion of neighboring septa. Roman numerals
indicate the order of formation of septa within single cycle.
Journal of Morphology
254
K. JANISZEWSKA ET AL.
Septal Arrangement
A flower-like pattern of micrabaciid septa, which
results from multiple connections of septa of various cycles, was noticed already by 19th century
researchers and was used as a criterion for the
higher rank classification of the group. For example, Milne-Edwards and Haime (1850) described
Stephanophyllia and Leptopenus as eupsamiids
(synonym of dendrophylliids) based on septal development. Micrabaciids were later considered a
distinct family but their septal arrangement was
still described as of ‘‘dendrophylliid type’’
(Vaughan and Wells, 1943). Seeming similarity of
septal arrangement in micrabaciid and dendrophyllid corals led Chevalier (1987) to classify both
families within suborder Dendrophylliina, a view
that was not supported by further morphological
(Cairns, 1989) and molecular (Kitahara et al., 2010)
studies. Moseley (1881) was the first to point out the
unique bifurcation pattern of micrabaciid septa.
This regular arrangement of septa was so striking
that Moseley (1881, p 207) was ‘‘at a loss to designate the quinary, quaternary and tertiary septa in
each system’’ in some specimens, and suggested
that these ‘‘terms would seem hardly to apply.’’
Nonetheless, the traditional notation of septal
cycles was still in use (Alcock, 1902; Keller, 1977).
When Cairns (1982) resurrected Moseley’s idea of
bifurcating septa, he proposed a new interpretation,
in which the septal system in Micrabaciidae consists of septa of the first two cycles and multiple
bifurcations of third cycle septa. This model was
later extended to all fossil and extant species (e.g.,
Owens, 1986b,1994; Cairns, 1989). The bifurcate
pattern of septa being very different from dendrophylliid fusion of septa (Pourtalès plan) was suggested as a micrabaciid synapomorphy. Contrary to
Cairns’ model, our data show that micrabaciid septa
do not arise by symmetrical division of older septa
but are formed as independent septal blades
between members of preceding cycles as in other
Scleractinia (Fig. 9A). Shortly after the formation of
septa, their upper margins bend and fuse with adjacent septa of a former cycle (Fig. 9E), yielding a
pseudobifurcate pattern observed in adult specimens. Noteworthy, despite some similarity in fusion
of septa, the micrabaciid arrangement of septa still
differs from that of dendrophylliids. The dendrophylliid Pourtalès plan is a form of septal substitution (Cairns, 2001), which does not take place in the
ontogeny of micrabaciids. ‘‘Fusion of septa’’ in the
Pourtalès plan refers to members of the same cycle,
which grow simultaneously and join by its inner
ends (Wells, 1956), whereas newly formed micrabaciid septa join the septa of the preceding cycle.
Finally, the lower cycle septa of dendrophylliids are
shorter than the members of a higher cycle (Wells,
1956: Fig. 239) contrary to the micrabaciid septal
insertion pattern (discussed below).
Journal of Morphology
The septal ontogeny of micrabaciids bear some
resemblance to that of fungiids. In both groups,
septa of a higher cycle may join those of a lower
cycle. However, in fungiids, first cycle septa
remain free, whereas in micrabaciids primaries
are united with the second cycle septa. Moreover,
pairs of higher cycle septa, which in fungiids consistently merge with septa of lower cycles (starting
from fourth cycle up), flank symmetrically the
older septa and join them at the same distance
from the corallite axis (Boschma, 1923). In contrast, in micrabaciids in each pair, one septum
appears earlier and joins older septum closer to
the corallite axis than the other. In both groups,
septa of a higher cycle may be formed before preceding cycle is completed: first members of a new
cycle are inserted in the vicinity of S1’s (Boschma,
1923: Fig. 1 for fungiids, and Supporting Information, Fig. S2 for micrabaciids). However, the order
of formation of the other septa within single cycle
is different in both groups. In fungiids, septal
insertion pattern is taxon-specific: often each sector of the same corallite has different number and/
or arrangement of septa. For example, in fungiid
taxa with elongated calices (e.g., Ctenactis echinata, Herpolitha limax, Polyphyllia talpina), consecutive higher cycles septa are formed along axial
S1’s, whereas there is a lack of septa of those
cycles in the vicinity of other S1’s (Boschma, 1923;
Hoeksema, 1989 Fig. 41). In contrast, in all micrabaciids, septa successively appear in all spaces
along the septa of preceding cycle, invariably following the same order for each sector of the calice
(see ‘‘Septal insertion pattern’’).
Septal Insertion Model
The serial micro-CT sections (septa appearing in
the lower part of a corallite and closer to its axis
were considered as older) combined with SEM
micrographs of consecutive ontogenetic stages
allow reconstruction of the septal insertion model.
As in most Scleractinia, skeletal growth begins
with simultaneous (judging from their equal size)
formation of six primary septa. The members of
successive cycles are inserted between previously
formed septa in the peripheral part of a corallite.
The septa of each cycle join with those of the preceding cycle by their upper margins. Fusion of primaries and secondaries gives a bilateral symmetry
to the corallite (four S2’s join four S1’s and two of
S2’s join one S1, leaving an opposite S1 free). Only
the septa within the first three cycles appear
simultaneously. The succession for the fourth cycle
is twofold. The septa next to the primaries appear
first, then those inserted between S2 and S3. The
next cycle begins with pairs of quinaries flanking
S4’s nearest to the primaries. The insertion of S5
adjacent to primaries is followed by development
of a septum between S4 and S3 septa. Thereafter
SKELETAL ONTOGENY OF MICRABACIIDS
the remaining quinaries arise: septa in the spaces
between S2 and S4 septa and those between S3
and S4 septa afterwards. Species having 120 septa
have additional pairs of S6 septa inserted along S5
septa lying in the outermost part of the septal system (S6 between S1 and S5 appear first). In micrabaciids with 144 septa, new S6 septa are inserted on
each side of the next S5 septum (in the direction
from the primaries). Following the previous pattern:
S6 septa appear between S3 and S5 septa before
they appear between S4 and S5 septa (Fig. 9D).
To sum up: the micrabaciid septa are inserted as
follows: 6S1, 6S2, 12S3, 12S4I, 12S4II, 12S5I,
12S5II, 12S5III, 12S5IV, 12S6I, 12S6II. In every
cycle, the insertion starts in the outermost part of
the septal system where pairs of newly formed
septa flank members of a former cycle adjacent to
primaries. Then, septa along the next (in the direction from primaries) septa of a previous cycle
arise. In each pair of septa, those inserted between
older septa are formed first (e.g., quinaries
between S4 and S2 before quinaries between S4
and S3). Thus, the final composition of a half-system of micrabaciid septa is: S1, S6I, S5I, S6II, S4I,
S6IV, S5II, S6III,S3, S5IV, S4II,S5III, S2 (for specimen with 144 septa; Fig. 9D).
In juvenile specimens, neighboring septa differ
in height, thickness, and development of ornamentation (Fig. 7F). As the skeleton grows, the differences between adjacent septa become blurred, and
fused septa of two cycles may appear as if they
formed by branching of the older septum (Figs.
3D–F, 8B, and 9D). However, the above-mentioned
dissimilarities between septa in the early stages of
development preclude formation of septa by symmetrical division of a lower cycle septa as suggested by Owens (1986b).
Phylogenetic and Taxonomic Implications
Since the beginning of studies on Scleractinia,
skeletal features have been used as the main criteria for taxonomic and phylogenetic interpretations
of the group. However, traits originally considered
taxonomically significant often diminish in importance and are replaced by new ‘‘unique’’ features.
A good example of such an intricate quest for useful diagnostic characters are studies on micrabaciids.
Despite the striking similarity in skeletal architecture (e.g., Duncan, 1884; Fowler, 1888), the species that are now grouped in the Micrabaciidae
were originally assigned to different coral taxa.
Micrabacia was considered as a member of the
Fungiidae (a family only consisting of reef corals;
see Hoeksema, 1989; Gittenberger et al. 2011),
whereas Stephanophyllia and Leptopenus were
described as Eupsammiidae (Milne-Edwards and
Haime, 1850). When Vaughan (1905) established
the new family Micrabaciidae, only Micrabacia,
255
Diafungia, Microsmilia, Podoseris, and Antilloseris
were included. In 1933, Wells revised the diagnosis
of a family which included Stephanophyllia, Micrabacia, and Leptopenus (Letepsammia and Rhombopsammia were added by Owens in 1986a,b) and
pointed out that the feature that distinguishes
micrabaciids from other scleractinians is the alternate position of costae and septa. However, this
feature is not unique for micrabaciids—costae
alternating in position with septa have been
described also in some turbinoliids (Dunocyathus
and Idiotrochus; Cairns, 1989). From all morphological features that were considered as supporting
monophyletic status of Micrabaciidae, only the
‘‘bifurcation pattern of septa and costae’’ (Cairns,
1989) has not yet been challenged. However, as it
is shown herein, the dichotomous pattern is not
created by true division of septa, but is the result
of fusion of newly inserted septa with adjacent
members of a former cycle at an early stage of development. Nonetheless, such fusion is unknown
in other corals, as well as the micrabaciid-specific
insertion pattern of septa within single cycles.
Thus, paradoxically, although the in-depth analysis of ontogeny does not support features traditionally considered as unique for micrabaciids, it indicates other traits associated with the same skeletal
elements, which seem to be true autapomorphies
of the group. This taxonomic aspect of the paper is
summarized in the emended diagnosis of Micrabaciidae appended at the end.
The presence of so many features that distinguish micrabaciids dovetails with their unique basal position in scleractinian phylogeny, which is
suggested by molecular analysis of recent species
(Kitahara et al., 2010; Stolarski et al., 2011). It
also shows that morphology, when properly recognized, remains a reliable tool for interpreting the
phylogeny and taxonomy of corals.
The above described details of skeletal ontogeny,
particularly the fusion of newly inserted septa at a
very early stage of development, show the necessity to scrutinize the skeletal traits of those groups
of corals (Palaeozoic kilbuchophyllids) that were
considered similar to micrabaciids precisely
because of the bifurcation of septa (see discussion
in Stolarski et al., 2004, 2011). The results also encourage deeper analysis of the still poorly known
anatomy and physiology of deep-water corals that
are involved in the formation of such unique macro
and microstructural skeletal features.
Taxonomic Note: Emended Diagnosis of
Micrabaciidae
Corallum solitary, cupolate, free, completely
enwrapped by the polyp tissue. Septa haxamerally
arranged, formed on wedge-shaped invaginations
of wall; invaginated parts of the wall porous, composed of pillars inclined downwardly and outJournal of Morphology
256
K. JANISZEWSKA ET AL.
wardly from the lower septal margins. Each septum (S2 and higher cycles) joins the nearest member of a former cycle at the upper margin resulting
in a pseudobifurcation pattern; starting from the
fourth cycle, septa within a single cycle do not
appear simultaneously but are inserted in pairs
which successively flank the members of the preceding cycle, invariably starting from the outermost part of septal system. In each pair, the septum adjacent to older septa arises first (e.g., the
quinaries between S2 and S4 before quinaries
between S3 and S4) and joins the neighboring septum closer to the corallite axis. Costae alternate in
position with septa by successive bifurcation, and
match the number of septa. Microstructure of
thickening deposits, unique in Scleractinia:
aragonite fibres organized into small, chip-like
bundles forming an irregular meshwork within
the skeleton.
ACKNOWLEDGMENTS
The authors wish to thank Tina Molodcova for
help in access to coral collection of Institute of
Oceanology, Russian Academy of Sciences, Moscow.
Ann Budd (The University of Iowa) provided useful comments on the manuscript. The authors also
thank two anonymous reviewers who made very
helpful comments on the manuscript.
LITERATURE CITED
Alcock AW. 1902. Report on the deep-sea Madreporaria of the
Siboga-Expedition. Leiden. p 52.
Baron-Szabo RC. 2008. Corals of the K/T-boundary: Scleractinian corals of the suborders Dendrophylliina, Caryophylliina,
Fungiina, Microsolenina, and Stylinina. Zootaxa 1952:1–244.
Boschma H. 1923. The Madreporaria of the Siboga Expedition.
Part 4. Fungia patella. Siboga-Expeditie 16d:1–20.
Boschma H. 1934. On the septal arrangement in Fungid corals.
In: Proceedings of 5th Pacific Science Congress, Victoria, Vancouver, pp 4199–4206.
Budd AF, Stolarski J. 2011. Corallite wall and septal microstructure in scleractinian reef corals: Comparison of molecular clades within the family Faviidae. J Morphol 272:66–88.
Cairns SD. 1982. Antarctic and Subantarctic Scleractinia. Antar
Res S 34:1–74.
Cairns SD. 1989. A revision of the ahermatypic Scleractinia of
the Philippine Islands and adjacent waters, Part 1: Fungiacyathidae, Micrabaciidae, Turbinoliinae, Guyniidae, and Flabellidae. Smithson Contrib Zool 486:1–136.
Cairns SD. 1995. The marine fauna of New Zealand: Scleractinia (Cnidaria: Anthozoa). N Z Oceanogr Inst Mem 103:1–210.
Cairns SD. 2001. A Generic revision and phylogenetic analysis
of the Dendrophylliidae (Cnidaria: Scleractinia). Smithson
Contrib Zool 615:1–75.
Cairns SD, Zibrowius H. 1997. Cnidaria Anthozoa: Azooxanthellate Scleractinia from the Philippine and Indonesian regions.
Mém Mus Natl Hist Nat 172:27–243.
Chevalier J.-P, Beauvais L. 1987. Ordre des Scléractiniaires. In:
Grasse P.P. (ed.) Traité de Zoologie, Cnidaires, Anthozoaires.
Masson: Paris. pp 403–764.
Duncan M. 1884. On the internal structures and classificatory
position of Micrabacia coronula. Q J Geol Soc 40:561–566.
Journal of Morphology
Durham JW. 1949. Ontogenetic Stages of Some Simple Corals.
Bulletin of the Department of Geological Sciences, California
University Publications Berkeley CA, Vol. 28, pp 137–172.
Fowler GH. 1888. The anatomy of the Madreporaria: IV. Q J
Microsc Sci 28:415–430.
Gittenberger A, Reijnen BT, Hoeksema BW. 2011. A molecularly
based phylogeny reconstruction of mushroom corals (Scleractinia: Fungiidae) with taxonomic consequences and evolutionary implications for life history traits. Contrib Zool 80:107–
132.
Hoeksema BW. 1989. Taxonomy, phylogeny and biogeography of
mushroom corals (Scleractinia: Fungiidae). Zool Verh 254:1–
295.
Janiszewska K, Stolarski J, Benzerara K, Meibom A, Mazur M,
Kitahara MV, Cairns SD. 2011. A unique skeletal microstructure of the deep-sea micrabaciid scleractinian corals. J Morphol 272:191–203.
Jell JS. 1974. The microstructure of some scleractinian corals.
In: Proceeding of 2nd International Coral Reef Symposium,
Brisbane, Australia. Vol. 2. pp 301–320.
Keller NB. 1977. New species of the genus Leptopenus and
some peculiarities of deep-sea ahermatypic corals. Trudy Inst
Okeanol 108:37–43.
Kitahara MV, Cairns SD, Stolarski J, Blair D, Miller DJ. 2010.
A comprehensive phylogenetic analysis of the Scleractinia
(Cnidaria, Anthozoa) based on mitochondrial CO1 sequence
data. Plos One 5(7):e11490.
Michelin JLH. 1840–1847. Iconographie zoophytologique,
description par localités et terrains des Polypiers fossiles de
la France et pays environnants. 2 vol. P. Bertrand: Paris. pp
1–348.
Milne Edwards H, Haime J. 1849. Observations sur les
polypiers de la famille des astréides. C R Acad Sci 29:465–470.
Milne-Edwards H, Haime J. 1850. Introduction; corals from the
Tertiary and Cretaceous Formations. A monograph of the
British fossil corals, First Part. London: Palaeontographical
Society. p 171.
Mori K, Minoura K. 1980. Ontogeny of ‘epithecal’ and septal
structures in scleractinian corals. Lethaia 13:321–326.
Moseley HN. 1876. Preliminary report to Professor Wyville
Thomson, F.R.S., director of the civilian staff, on the true corals ddredged by H.M.S. Challenger in Deep Water between
the dates Dec. 30th, 1870, and August 31st, 1875. Proc R Soc
Lond 24:544–569.
Moseley HN. 1881. Report on certain hydroid, alcyonarian, and
madreporarian corals procured during the voyage of H.M.S.
Challenger, in the years 1873–1876. Part 3. On the deep-sea
Madreporaria. In: Thomson CW, editor. Report of the Scientific Results of the Voyage of HMS Challenger during the
Years 1873–76 under the command of Captain George S Nares and Captain Frank Tourle Thomson. London. p 248.
Muscatine L, Tambutte E, Allemand D. 1997. Morphology of
coral desmocytes, cells that anchor the calicoblastic epithelium to the skeleton. Coral Reefs 16:205–213.
Nothdurft LD, Webb GE. 2007. Microstructure of common reefbuilding coral genera Acropora, Pocillopora, Goniastrea and
Porites: constraints on spatial resolution in geochemical sampling. Facies 53:1–26.
Owens MJ. 1986a. On the elevation of the Stephanophyllia subgenus Letepsammia to generic rank (Coelenterata: Scleractinia: Micrabaciidae). P Biol Soc Wash 99:486–488.
Owens MJ. 1986b. Rhombopsammia, a new genus of the family
Micrabaciidae (Coelenterata, Scleractinia). P Biol Soc Wash
99:248–256.
Owens MJ. 1994. Letepsammia franki, a new species of deepsea coral (Coelenterata: Scleractinia: Micrabaciidae). P Biol
Soc Wash 107:586–590.
Squires DF. 1967. The evolution of the deep-sea coral family
Micrabaciidae. Stud Trop Oceanogr 5:502–510.
Stephenson LW. 1916. North American Upper Cretaceous corals
of the genus Micrabacia. Prof Pap US Geol Surv 98–J:115–
131.
SKELETAL ONTOGENY OF MICRABACIIDS
Stolarski J. 1995. Ontogenetic development of the thecal structures in caryophylliine scleractinian corals. Acta Palaeontol
Pol 40:19–44.
Stolarski J. 1996. Gardineria—A scleractinian living fossil.
Acta Palaeontol Pol 41:339–367.
Stolarski J. 2003. Three-dimensional micro- and nanostructural
characteristics of the scleractinian coral skeleton: A biocalcification proxy. Acta Palaeontol Pol 48:497–530.
Stolarski J, Roniewicz E, Grycuk T. 2004. A model for furcate
septal increase in a Triassic scleractiniamorph. Acta Palaeontol Pol 49:529–542.
Stolarski J, Kitahara MV, Miller DJ, Mazur M, Meibom A, Cairns
SD. 2011. The ancient evolutionary origins of Scleractinia
revealed by azooxanthellate corals. BMC Evol Biol 11:316.
Vaughan TW. 1905. A critical review of the literature on the
simple genera of the Madreporaria Fungida, with a tentative
classification. Proc US Natl Mus 28:371–424.
257
Vaughan TW, Wells JW. 1943. Revision of the suborders, families, and genera of the Scleractinia. Geol Soc Spec Paper
44:1–363.
Wells JW. 1933. Corals of the Cretaceous of the Atlantic and
Gulf coastal plains and western interior of the United States.
Bull Am Paleo 18:85–288.
Wells JW. 1956. Scleractinia. In: Moore RC, editor. Treatise on
Invertebrate Paleontology, Part F: Coelenterata. New York:
Geological Society of America and University of Kansas
Press. p F328–F444.
Wise SW, Jr. 1970. Scleractinian coral exoskeletons: Surface
microarchitecture and attachment scar patterns. Science
16:978–980.
Yabe H, Eguchi M. 1932. Some Recent and fossil corals of the
genus Stephanophyllia H. Michelin from Japan. Sci Rep
Tohoku Univ, Ser 2 (Geology) 15:55–63.
Journal of Morphology