Corallite wall and septal microstructure in scleractinian reef corals: Comparison of molecular clades within the family Faviidae

Abstract

Recent molecular phylogenies conflict with traditional scleractinian classification at ranks ranging from suborder to genus, challenging morphologists to discover new characters that better agree with molecular data. Such characters are essential for including fossils in analyses and tracing evolutionary patterns through geologic time. We examine the skeletal morphology of 36 species belonging to the traditional families Faviidae, Merulinidae, Pectiniidae, and Trachyphylliidae (3 Atlantic, 14 Indo-Pacific, 2 cosmopolitan genera) at the macromorphological, micromorphological, and microstructural levels. Molecular analyses indicate that the families are not monophyletic groups, but consist of six family-level clades, four of which are examined [clade XV = Diploastrea heliopora; clade XVI = Montastraea cavernosa; clade XVII (“Pacific faviids”) = Pacific faviids (part) + merulinids (part) + pectiniids (part) + M. annularis complex; clade XXI (“Atlantic faviids”) = Atlantic faviids (part) + Atlantic mussids].

Comparisons among molecular clades indicate that micromorphological and microstructural characters (singly and in combination) are clade diagnostic, but with two exceptions, macromorphologic characters are not. The septal teeth of “Atlantic faviids” are paddle-shaped (strong secondary calcification axes) or blocky, whereas the septal teeth of “Pacific faviids” are spine-shaped or multidirectional. Corallite walls in “Atlantic faviids” are usually septothecal, with occasional trabeculothecal elements; whereas corallite walls in “Pacific faviids” are usually trabeculothecal or parathecal or they contain abortive septa. Exceptions include subclades of “Pacific faviids” consisting of a) Caulastraea and Oulophyllia (strong secondary axes) and b) Cyphastrea (septothecal walls). Diploastrea has a diagnostic synapticulothecal wall and thick triangular teeth; Montastraea cavernosa is also distinct, possessing both “Pacific faviid” (abortive septa) and “Atlantic faviid” (paddle-shaped teeth) attributes. The development of secondary axes is similar in traditional Atlantic faviids and mussids, supporting molecular results placing them in the same clade. Subclades of “Pacific faviids” reveal differences in wall structure and the arrangement and distinctiveness of centers of rapid accretion. J. Morphol. 272:66–88, 2011. © 2010 Wiley-Liss, Inc.

INTRODUCTION

This article is the second in a series defining and illustrating new and rarely used morphological characters, which better match the results of molecular analyses that are transforming our understanding of the systematics and evolution of scleractinian corals. Phylogenetic analyses of mitochondrial (cytB and COI) and nuclear (ß-tubulin) genes have shown that as many as 11 traditional families and three genera are polyphyletic (Fukami et al.,2004,2008). They have revealed for the first time the existence of a new family-level clade (clade XXI) that consists exclusively of Atlantic members of the traditional families Mussidae and Faviidae, both of which have long been thought to be cosmopolitan. In the first paper in the series (Budd and Stolarski,2009), we focused on the family Mussidae Ortmann1890 and compared representatives of Atlantic and Pacific genera. Our results showed that several micromorphological characters associated with septal teeth and granules are effective at distinguishing the two groups, and that these characters support molecular trees indicating that Atlantic and Pacific mussids belong to separate families. In this article, we turn our attention to the family Faviidae Gregory1900 and compare not only Atlantic and Pacific faviids but also subclades (roughly subfamily- or genus-level) within a large family-level large clade consisting primarily of Pacific faviids. Our objective is to discover morphologic characters that effectively distinguish these groups and can be used to trace their evolutionary history in the fossil record.

The family Faviidae was originally described by Gregory (1900) and, like the family Mussidae, it has contained a mixture of Atlantic and Pacific taxa since its inception. In a recent monograph on scleractinian reef corals (Veron,2000), the coral family Faviiidae was divided into 24 modern genera: four are currently restricted to the western Atlantic, 17 are restricted to the Indo-Pacific, and three are cosmopolitan (Table 1). Cairns et al. (1999) include one additional modern genus in the family, Astraeosmilia (restricted to the Indian Ocean), which Veron (2000) synonymized with Caulastraea. Contrary to this traditional grouping, molecular analyses of these genera (Fukami et al.,2004,2008) show that Atlantic and Indo-Pacific members of the family are evolutionarily distinct, and many Atlantic members of the family Faviidae (Favia, Diploria, Manicina, Colpophyllia) are more closely related to Atlantic members of the family Mussidae (Isophyllia, Mussa, Mycetophyllia) than they are to Pacific members of the family Faviidae. These Atlantic members of the families Faviidae and Mussidae form clade XXI (Fig. 1). On the other hand, Atlantic Montastraea are polyphyletic, with members of the M. annularis complex embedded within clade XVII (composed mostly of Pacific faviids) and M. cavernosa forming a separate clade (clade XVI), which is basal to most faviids and mussids. Moreover, some members of the family Pectiniidae (Pectinia, Mycedium), and all members of the families Merulinidae (Merulina, Hydnophora, Scapophyllia) and Trachyphylliidae (Trachyphyllia) are embedded within clade XVII. With the possible exception of the Montastraea annularis complex, there are no modern Atlantic corals in clade XVII; however, numerous genera within clade XVII (e.g., Favites, Goniastrea, Leptoria, Trachyphyllia, Hydnophora) have been interpreted as occurring in the Caribbean Cenozoic fossil record and having become regionally extinct in the Caribbean during the Miocene or Pliocene (Vaughan,1919; Budd et al.,1992). Since Fukami et al. (2008), Huang et al. (2009) have used COI and IGR sequence data to confirm that Pacific members of the genera Montastraea and Favia are polyphyletic and show that Fukami et al. (2008) clade XVII consists of subclades.

Figure 1. Molecular tree after Fukami et al. (2008) showing the 36 species (underlined) under consideration and the subclades/clades to which they have been assigned for the purposes of comparisons. We were unable to obtain specimens for three species in the tree, Goniastrea deformis, Leptoria irregularis, and Echinopora pacificus, which were first described from Japan in Veron (1990). Veron (2000) described G. deformis as being morphologically similar to G. aspera; L. irregularis as similar to Scapophyllia cylindrica and Merulina ampliata (in addition to L. phyrgia); and E. pacificus as similar to E. lamellosa. We also did not include three species that were not analyzed in Fukami et al. (2004): Scapophyllia cylindrica, Barabattoia amicorum, Favia speciosa. Goniastrea aspera was analyzed in Fukami et al. (2004) but not in Fukami et al. (2008), and is included herein.

Table 1. List of genera currently assigned to the family Faviidae and the molecular clades to which they belong. Nineteen genera are examined in this study

Genera within the family Faviidae (Veron2000)	Modern distribution	Fukami et al., (2008) clade	Treated in this study
Colpophyllia Milne Edwards and Haime,1848	Atlantic	XXI	x
Diploria Milne Edwards and Haime,1848	Atlantic	XXI	x
Manicina Ehrenberg,1834	Atlantic	XXI	x
Solenastrea Milne Edwards and Haime,1848	Atlantic	XIII
Cladocora Ehrenberg,1834	Cosmopolitan	XIII
Favia Oken,1815 (= Ehrenberg,1834)	Cosmopolitan	XVII, XXI	x
Montastraea Blainville, 1930	Cosmopolitan	XVI, XVII	x
Australogyra Veron and Pichon,1982	Indo-Pacific	?XVII
Barabattoia Yabe and Sugiyama,1941 [= Bikiniastrea Wells,1954]	Indo-Pacific	XVII
Caulastraea Dana,1846	Indo-Pacific	XVII	x
Cyphastrea Milne Edwards and Haime,1848	Indo-Pacific	XVII	x
Diploastrea Matthai,1914	Indo-Pacific	XV	x
Echinopora Lamarck,1816	Indo-Pacific	XVII	x
Erythrastrea Scheer and Pillai,1983	Indo-Pacific	?XVII
Favites Link,1807	Indo-Pacific	XVII	x
Goniastrea Milne Edwards and Haime,1848	Indo-Pacific	XVII	x
Leptastrea Milne Edwards and Haime,1848	Indo-Pacific	XI
Leptoria Milne Edwards and Haime,1848	Indo-Pacific	XVII	x
Moseleya Quelch,1884	Indo-Pacific	?XVII
Oulastrea Milne Edwards and Haime,1848	Indo-Pacific	XI
Oulophyllia Milne Edwards and Haime,1848	Indo-Pacific	XVII	x
Parasimplastrea Sheppard,1985	Indo-Pacific	?
Platygyra Ehrenberg,1834	Indo-Pacific	XVII	x
Plesiastrea Milne Edwards & Haime,1848	Indo-Pacific	XIV
Additional genera within clade XVII of Fukami et al. (2008)	Modern distribution	Traditional family to which it is assigned	Treated in this study
Hydnophora Fischer,1807	Indo-Pacific	Merulinidae	x
Merulina Ehrenberg,1834	Indo-Pacific	Merulinidae	x
Mycedium Oken,1815 (= Milne Edwards and Haime,1850)	Indo-Pacific	Pectiniidae	x
Pectinia Oken,1815 (= Faustino,1927)	Indo-Pacific	Pectiniidae	x
Scapophyllia Milne Edwards and Haime,1848	Indo-Pacific	Merulinidae
Trachyphyllia Milne Edwards and Haime,1848	Indo-Pacific	Trachyphylliidae	x

Although minor modifications (e.g., Cairns et al.,1999; Veron,2000) have subsequently been made, the traditional classification system that is most widely used by coral workers today was originally proposed by Vaughan and Wells (1943) and Wells (1956) and is based on skeletal morphology (see discussion in Stolarski and Roniewicz,2001). Three different aspects of skeletal morphology are considered: 1) macromorphology (budding; colony form and integration; size and shape of corallites; numbers of septal cycles), 2) micromorphology (shape and orientation of septal teeth; shape and distribution of granules), and 3) microstructure (arrangement of centers of rapid accretion and fibers; development of thickening deposits). In the classification system of Wells (1956), the families Faviidae and Mussidae are based on a combination of micromorphologic (i.e., septal teeth) and microstructural (i.e., trabeculae) features. The family Faviidae is distinguished by having “Septa (…) formed by 1 or 2 fan systems of simple (compound in later forms) trabeculae, more or less regularly dentate marginally” (Wells,1956, p. F400); whereas the family Mussidae is distinguished by having “Septa… formed by several fan systems of large, simple trabeculae, each fan system producing a lobulate dentation” (Wells,1956, p. F416).

However, these two diagnoses are based on the traditional concept of “trabeculae” (Ogilvie,1897), which does not capture the full range of observed variation at the micromorphologic and microstructural levels, including the complex relationships between the mineral and organic-enriched phases of the skeleton. The relationships between the mineral and organic-enriched skeletal regions are explained by new models of scleractinian skeletal growth that reinterpret differences between two main skeletal regions traditionally referred to as “centers of calcification” (COC) and “fibers” (Bourne,1887; Ogilvie,1897; Vaughan and Wells,1943; Cuif et al.,1998; Cuif and Dauphin,2005). New observations show that “centers of calcification” and “fibers” are formed simultaneously (not in successive steps) and that their structural differences result from their growth dynamics (Stolarski,2003; Nothdurft and Webb,2007; Brahmi et al.,2010). Following the new microstructural models, faviid wall structure should be redescribed, distinguishing “rapid accretion deposits” that are arranged in different ways and surrounded to varying degrees by “thickening deposits.”

Previous attempts at using fine-scale morphological characters in combined skeletal-molecular studies have shown their potential to provide support for molecular-based clades (Cuif et al.,2003; Benzoni et al.,2007). Here, we conduct a comprehensive and more exhaustive survey (36 species in the family Faviidae and other closely related families) of skeletal variation in costoseptal microstructure (fibers, rapid accretion deposits; including the structure of the corallite wall) using scanning electron microscopy (SEM) and standard (30 μ thick) transverse petrographic thin sections. In these 36 species, we also describe characters originally defined in Budd and Stolarski (2009), namely costoseptal micromorphology (teeth, granules), using SEM of calicular surfaces. We assess homology by comparing states of the newly constructed characters among the molecular clades and subclades of Fukami et al. (2008) and between Atlantic and Pacific faviids. We use the results to propose several new morphologic characters, which can be applied in future phylogenetic analyses and classification of these and other related scleractinian groups.

MATERIAL AND METHODS

Material Examined

We examined eight Atlantic species and 28 Pacific species (Table 2; Supporting Information Appendix I), which were treated in the molecular analyses of Fukami et al. (2004,2008). These species belong to three Atlantic genera (Colpophyllia, Diploria, and Manicina), 14 Indo-Pacific genera (Caulastraea, Cyphastrea, Diploastrea, Echinopora, Favites, Goniastrea, Leptoria, Oulophyllia, Platygyra; Hydnophora, Merulina, Mycedium, Pectinia, and Trachyphyllia), and two cosmopolitan genera (Favia and Montastraea). All have been recently placed (Cairns et al.,1999; Veron,2000) within the traditional families Faviidae, Pectiniidae, Merulinidae, and Trachyphylliidae (Vaughan and Wells,1943; Wells,1956).

Table 2. List of species and the subclades to which they have been assigned in this study

Clade	Branch support (mitochondrial cox1 and cob; Fig. 1 of Fukami et al.,2008)	Branch support (tubulin; Fig. 2 of Fukami et al.,2008)	Traditional family	Consistent molecular placement	Inconsistent molecular placement
a Type species of the genus. b M. annularis s.l. is grouped with XVII-C on the basis of the tubulin tree. c F. stelligera is grouped with XVII-A on the basis on the mitochondrial tree. d M. curta is grouped with XVII-A on the basis of the mitochondrial tree in Fukami et al. (2004). e G. aspera is grouped with XVII-F on the basis of the mitochondrial tree in Fukami et al. (2004).
XVII-A	100/98	99/77	Faviidae and Merulinidae	aMerulina ampliata, M. scabricula; Goniastrea pectinata	dMontastraea curta;cFavia stelligera
XVII-B	for B + C: 100/82	100/88	Faviidae and Trachyphylliidae	Favia pallida, F. favus;aTrachyphyllia geoffroyi	—
XVII-C	for B + C: 100/82	100/93	Faviidae	Cyphastrea serailia, C. chalcidicum	bMontastraea annularis s.l.
XVII-D	for D + E: 100/92	<70%/<50%	Faviidae	aCaulastraea furcata;aOulophyllia crispa, O. bennettae	—
XVII-E	for D + E: 100/92	100/82	Pectiniidae	Pectinia alcicornis, P. paeonia;aMycedium elephantotus	—
XVII-F	100/95	<70%/<50%	Faviidae	eGoniastrea aspera; Favites halicora; F. chinensis; Montastraea valenciennesi, M. magnistellata	—
XVII-G	<70%/<50%	92/75	Faviidae	aLeptoria phrygia; Platygyra daedalea,aP. lamellina	—
XVII-H	<70%/<50%	97/66	Merulinidae	aHydnophora exesa, H. grandis	—
XVII-I	<70%/<50%	90/−	Faviidae	Echinopora gemmacea	—
XVI	79/	100/98	Faviidae	Montastraea cavernosa	—
XV	100/55	na	Faviidae	aDiploastrea heliopora	—
XXI	100/83	100/100	Faviidae	aFavia fragum; Diploria strigosa, D. clivosa,aD. labyrinthiformis; Manicina areolata;aColpophyllia natans	—

For the purposes of morphological comparisons, we subdivided the 36 species into family-level clades as defined by Fukami et al. (2008, Fig. 1), and the large clade XVII into genus-level “subclades,” which conform more or less to the molecular trees of Fukami et al. (2008) (Table 2; Fig. 1). These subclades vary in amount of branch support (and integrity). For example, subclade D has weak support on both the mitochondrial and tubulin trees; subclade F has strong support on the mitochrondrial tree but weak support on the tubulin tree; subclades G and H have weak support on the mitochrondrial tree but strong support on the tubulin tree; subclade A has strong support on both trees. In this study, we use the term “Atlantic faviids” to refer to clade XXI, and “Pacific faviids” to refer to clade XVII.

The specimens that we studied are listed in Supporting Information Appendix II, and consist of: 1) material that was studied molecularly by Fukami et al. (2004) and deposited in the University of Iowa Paleontology Repository (SUI) or in the Florida Museum of Natural History (UF); 2) nontype material deposited at the National Museum of Natural History (Smithsonian Institution), Washington, DC (USNM) and the Florida Museum of Natural History (UF); and 3) type material (12 of the 36 species) deposited at the Natural History Museum, London (BM(NH)); Muséum national d'Histoire naturelle, Paris (MNHN); the National Museum of Natural History (Smithsonian Institution), Washington, DC (USNM); and the Yale Peabody Museum, New Haven, CT (YPM).

Characters

Our survey consists of three groups of skeletal characters, which involve different scales of analysis and preparation methods (Cuif and Perrin,1999; Budd and Stolarski,2009).

Macromorphological characters (3D-observations using a regular light microscope)

Macromorphology involves the study of many traditional diagnostic features related to colony form (corallite budding and integration, the length and shape of calicular series); the size and shape of the calice; and development of the septa (number, spacing, relative thickness and length), the columella (and associated lobes), the endo- and exotheca, and the coenosteum. For example, modern genera within family Faviidae are traditionally subdivided into two subfamilies (Faviinae Gregory1900 and Montastreinae Vaughan and Wells1943) based on whether budding is primarily intracalicular (Faviinae: including Caulastraea, Favia, Diploria, Favites, Oulophyllia, Goniastrea, Platygyra, Leptoria, Hydnophora, Manicina, Colpophyllia of this study) or extracalicular (Montastreinae: including Montastraea, Diploastrea, Cyphastrea, Echinopora of this study) (Wells,1956). A third smaller subfamily (Trachyphylliinae: including Trachyphyllia of this study) possesses intracalicular budding and highly well-developed septal lobes. Genera within the Faviinae are distinguished by colony form (cerioid versus plocoid versus meandroid versus phaceloid, etc.) and by the structure of the columella (trabecular versus lamellar, continuous versus discontinuous). Genera within the Montastreinae are also distinguished by colony form and the structure of the columella, as well as by the structure of the coenosteum (costate versus vesicular versus spinose, etc.).

Micromorphological characters (3D-observations using SEM of calicular surfaces, at magnifications <200×)

Micromorphology involves the study of the shapes of teeth along the upper margins of the wall, septa, and columella, and of the granulation on septal faces (Fig. 2). Samples of selected calices (limited breakage of septal teeth) were mounted on stubs with double-sided adhesive tape and sputter-coated with conductive platinum film for 3D-observations using SEM. These characters were the focus of a previous publication (Budd and Stolarski,2009) comparing septal teeth and granules between Atlantic and Pacific members of the family Mussidae.

Figure 2. Comparisons between Atlantic and Pacific faviids, which have meandroid colony forms. In Diploria: D. labyrinthiformis (A) and D. strigosa (B) have regular, blocky teeth that are tricorne in shape, have well-developed granules formed by secondary calcification axes, and are separated by a smooth interarea between teeth along the septal margin. In Platygyra: P. lamellina (C) and P. daedalea (D) have thin teeth that are less regular and separated by a palisade interarea. The granules formed by secondary axes are more closely spaced in Platygyra than in Diploria. Dotted white arrows outline the shape of septal teeth; black circles indicate granules. A: D. labyrinthiformis (SUI122810 (FA1061), Bocas del Toro, Panama (Atlantic)). B: D. strigosa (SUI122813 (FA1062), Bocas del Toro, Panama (Atlantic)). C: P. lamellina (USNM91127, Irian Java, Indonesia (Indo-Pacific)). D: P. daedalea (SUI122833 (FA1112), Lizard Island, Queensland, Australia (Indo-Pacific)).

Microstructural characters (2D-observations using transverse thin sections at magnifications <100×)

Microstructure involves the study of the internal structure (i.e., the arrangement of centers of rapid accretion and fibers) within the wall, septa, and columella. Samples of selected calices were cut transversely, impregnated with epoxy, and thin-sectioned to ca. 30 μ thickness. As shown in Figure 3, microstructural observations include the structure of the corallite wall, which may be parathecal (formed by dissepiments), septothecal (formed by septal thickening, sometimes including abortive septa), trabeculothecal (formed by remnants of the initial marginothecal corallite wall between costosepta), or synapticulothecal (formed by synapticulae) in the family Faviidae. Figures 4–13 illustrate the microstructural observations made in this study.

Figure 3. Corallite wall structures as observed in transverse thin section (for each drawing/photograph pair: left, interpretative drawing; right, photograph). White arrows indicate key wall features. A: Drawing of corresponding septal margin. B, C: Trabeculothecal wall (wall formed by inserting septal features that are perpendicular to the septa) in Leptoria phrygia (SUI122821 (FA1106), Lizard Island, Queensland, Australia). D, E: Parathecal wall (wall formed by dissepiments) in Favia pallida SUI122819 (FA1105), Lizard Island, Queensland, Australia). F, G: Septothecal wall (wall formed by septal thickening) in Favia fragum (SUI122816 (FA1065), Bocas del Toro, Panama). H, I: Septothecal wall constructed by “abortive septa” (wall formed by inserting septal features that are parallel to the septa) in Favia stelligera (USNM1013045 (FA1040), French Polynesia). J, K: Synapticulothecal wall (wall formed by synapticulae) in Diploastrea heliopora (USNM48046, Malaysia).

Figure 4. The Atlantic “faviids” in Clade XXI are characterized by primarily septothecal wall structure and carinae. The exception is Colpophyllia (F), which has parathecal walls. Additional intercorallite elements (trabeculotheca) are also found in the corallite walls of Manicina (E) and some Diploria (e.g., Diplora clivosa, C). Poorly defined, irregular septa are occasionally inserted between costosepta (e.g., Favia fragum, Diploria strigosa, B). Rapid Accretion Deposits associated with costae in this group range from aligned (Colpophyllia, Manicina) to clustered (Favia). Rapid Accretion Deposits associated with septa and the columella are diffuse (“weakly aligned” or “weakly clustered”). Black arrows, septotheca; grey arrows, trabeculotheca; white arrows, wall dissepiments (paratheca). A: Favia fragum (1-3, SUI122816 (FA1065), Bocas del Toro, Panama (Atlantic)). B: Diploria strigosa (1, USNM 1123429 (NF505), Andros Island, Bahamas (Atlantic); 2-3, SUI122813 (FA1062), Bocas del Toro, Panama (Atlantic)). C: Diploria clivosa (1, USNM1123428 (NF506), Andros Island, Bahamas (Atlantic); 2-3, SUI122807 (FA1060), Bocas del Toro, Panama (Atlantic)). D: Diploria labyrinthiformis (1-3, SUI122810 (FA1061), Bocas del Toro, Panama (Atlantic)). E: Manicina areolata (1, USNM96241 (NF497), Dry Tortugas (Atlantic). 2-3, SUI122822 (FA1067)). F: Colpophyllia natans (1-3, SUI122804 (J115), Discovery Bay, Jamaica (Atlantic)). Subscript 1: SEM micrograph, Subscripts 2-3: thin sections.

Figure 5. Clade XVII, Subclade A, is characterized by septothecal walls made of “abortive septa” (Favia, Goniastrea, Montastraea), with trabeculothecal elements in Merulina. Rapid Accretion Deposits are usually weakly aligned within costae and septa. Rapid Accretion Deposits within the columella are faintly clustered, and paliform lobes are well-developed. Black arrows, septotheca; grey arrows, trabeculotheca. A: Favia stelligera (1, SUI122820 (FA1119), Lizard Island, Queensland, Australia (Indo-Pacific); 2-3 USNM1013045 (FA1040), French Polynesia (Indo-Pacific)). B: Goniastrea pectinata (1-3, USNM89567, Enewetok Atoll, Marshall Islands (Indo-Pacific)). C: Montastraea curta (1-3, USNM00014 (syntype), Fiji (Indo-Pacific)). D: Merulina ampliata (1,3, USNM100519 (FA1033), Madagascar (Indo-Pacific); 2, UF2051 (FA1056), Palau (Pacific)). E: Merulina scabricula (1, USNM00165 (syntype), Fiji (Indo-Pacific). 2-3, USNM95776, Papua New Guinea (Pacific)). Subscript 1: SEM micrograph, Subscripts 2-3: thin sections.

Figure 6. Clade XVII, Subclade B, is generally characterized by parathecal wall structure and weak carinae; however, septothecal elements are sometimes present. Rapid Accretion Deposits are usually aligned within costae, with lines broken by clusters of centers, and faintly clustered within septa and the columella. Black arrows, septotheca; white arrows, wall dissepiments (paratheca). A: Favia pallida (1, USNM44952, Bikini Island, Marshall Islands (Indo-Pacific); 2-3, SUI122819 (FA1105), Lizard Island, Queensland, Australia (Indo-Pacific)). B: Favia favus (1-3, USNM93662, Papua New Guinea (Indo-Pacific)). C: Trachyphyllia geoffroyi (1, USNM91340, Malaysia (Indo-Pacific). 2-3. UF1383 (FA1073), Palau (Indo-Pacific)). Subscript 1: SEM micrograph, Subscripts 2-3: thin sections.

Figure 7. Clade XVII, Subclade C, is characterized by septothecal wall structure, with occasional parathecal elements. Poorly defined irregular septa are sometimes inserted between costosepta. Rapid Accretion Deposits (wall, septum, columella) are neither aligned nor distinctively clustered; instead they are diffuse (“faintly clustered”). Large black arrows, septotheca; small black arrows, wall dissepiments (paratheca). A: Cyphastrea chalcidium. (1-3, SUI122805 (FA1055), Taiwan (Indo-Pacific)). B: Cyphastrea serailia (1-2, SUI122806 (FA1118), Lizard Island, Queensland, Australia (Indo-Pacific); 3, USNM93729 (FA1034), Papua New Guinea (Indo-Pacific)). C: Montastraea annularis s.l. (1, SUI122826 (MANN), San Blas Islands, Panama (Atlantic). 2-3. SUI122827 (B003), Bahamas (Atlantic)). Subscript 1: SEM micrograph, Subscripts 2-3: thin sections.

Figure 8. Clade XVII, Subclade D, is characterized by parathecal (Caulastraea) or trabeculothecal (Oulophyllia) wall structure, and by carinae. Rapid Accretion Deposits are usually aligned within costae and faintly clustered within septa. Black arrows, wall dissepiments (paratheca); grey arrows, trabeculotheca. A: Caulastraea furcata (1,3, USNM 92348, Palau (Indo-Pacific); 2, USNM92394 (FA1035), Palau (Indo-Pacific)). B: Oulophyllia crispa (1, SUI122832 (FA1111), Lizard Island, Queensland, Australia (Indo-Pacific). 2-3, USNM83131, Banda Islands, Indonesia (Indo-Pacific)). C. Oulophyllia bennettae (1-2, UF2057 (FA1064), Palau (Indo-Pacific); 3, USNM83187, Geographe Bay, Western Australia (Indo-Pacific)). Subscript 1: SEM micrograph, Subscripts 2-3: thin sections.

Figure 9. Clade XVII, Subclade E, is characterized by parathecal walls, thickened by stereome. Rapid Accretion Deposits are strongly aligned within costae and septa. White arrows, wall dissepiments (paratheca). A: Pectinia alcicornis (1, UF2121 (FA1086), Palau (Indo-Pacific). 2-3, UF2048 (FA1085), Palau (Indo-Pacific)). B: Pectinia paeonia (1-2, UF2105 (FA1087), Palau (Indo-Pacific). 3, USNM000132 (syntype), Fiji (Indo-Pacific)). C: Mycedium elephantotus (1, UF2062 (FA1082), Palau (Indo-Pacific); 2, USNM00169 (syntype of Phyllastraea tubifex, a junior synonym), Fiji (Indo-Pacific). 3, UF2072 (FA1083), Palau (Indo-Pacific)). Subscript 1: SEM micrograph, Subscripts 2-3: thin sections.

Figure 10. Clade XVII, Subclade F, is characterized by parathecal (Favites, Montastraea) or trabeculothecal (Goniastrea) wall structure. Additional septothecal elements are present in Favites. Rapid Accretion Deposits are usually aligned within costae and septa, with lines broken by clusters of centers. Endothecal dissepiments are usually well-developed. Black arrows, septotheca; grey arrows, trabeculotheca; white arrows, wall dissepiments (paratheca). A: Favites halicora (1, USNM90627(FA1036), Philippines (Indo-Pacific); 2-3, USNM1019616, Egypt (Indian Ocean)). B: Favites chinensis (1-3, USNM90755, Philippines (Indo-Pacific). C: Montastraea valenciennesi (1-3, USNM45391, Philippines (Indo-Pacific). D: Montastraea magnistellata (1-3, USNM48178, Malaysia (Indo-Pacific). E: Goniastrea aspera (1, USNM00402 (syntype), Lo Choo (Indo-Pacific); 2-3, USNM00079 (holotype of Prionastrea spectabilis, a junior synonym), Fiji (Indo-Pacific)). Subscript 1: SEM micrograph, Subscripts 2-3: thin sections.

Figure 11. Clade XVII, Subclade G, is characterized by trabeculothecal wall structure, with septothecal elements present in Leptoria and parathecal elements in Platygyra. Rapid Accretion Deposits are aligned to varying degrees within costae and septa. Black arrows, septotheca; grey arrows, trabeculotheca; white arrows, wall dissepiments (paratheca). A: Leptoria phrygia (1, USNM 38508, Murray Island, Australia (Indo-Pacific). 2, SUI122821 (FA1106), Lizard Island, Queensland, Australia (Indo-Pacific). 3, USNM00018 (syntype of Meandrina gracilis, a junior synonym)). B: Platygyra daedalea (1, USNM91091, Manipa Island, Indonesia (Indo-Pacific). 2-3, SUI122833 (FA1112), Lizard Island, Queensland, Australia (Indo-Pacific)). C: Platygyra lamellina (1-3. USNM91127, Irian Java, Indonesia (Indo-Pacific)). Subscript 1: SEM micrograph, Subscripts 2-3: thin sections.

Figure 12. Clade XVII, Subclade H, is characterized by trabeculothecal walls with septothecal elements, and a distinctive hydnophoroid growth form. Rapid Accretion Deposits are aligned within costae and septa. A: Hydnophora exesa (1-3. USNM83232 (FA1041), Marshall Islands (Indo-Pacific). B: Hydnophora grandis (1, UF2063 (FA1084), Palau (Indo-Pacific). 2-3, USNM83226, Banc Gail, New Caledonia (Indo-Pacific). Subscript 1: SEM micrograph, Subscripts 2-3: thin sections.

Figure 13. Clade XVII (Subclade I) and clade XVI are characterized by septothecal walls (occasionally with “abortive septa”); whereas clade XV is characterized by synapticulothecal walls. All three groups have distinctively clustered costae and septa. White arrows in A and B indicate abortive septa; white arrows in C indicate synapticulothecal bars. A: Clade XVII, Subclade I, Echinopora gemmacea (1-3, USNM1113168, Red Sea (Indo-Pacific). B: Clade XVI, Montastraea cavernosa (1-3, SUI122828 (FA1093), Bocas del Toro, Panama (Atlantic)). C: Clade XV, Diploastrea heliopora (1, USNM93732, Papua New Guinea (Indo-Pacific). 2-3, USNM48046, Malaysia (Indo-Pacific) l. Subscript 1: SEM micrograph, Subscripts 2-3: thin sections.

Glossary of key skeletal terms

(Plural and/or adjective forms in brackets), see also glossary in Budd and Stolarski (2009).

Abortive septum (-a): Slender, septum-like structure formed between normally developed septa (Fig. 3); abortive septa do not protrude into calicular space but are discernible within the corallite wall (septotheca) as narrow structures parallel to septa with their own centers of rapid accretion (see Alloiteau,1952, p. 595).

Ambulacral groove: A depression on the calical surface, corresponding with the coenosteum.

Budding (-): Addition of new corallites to a corallum. Budding is either intracalicular (within the wall of the parent corallite) or extracalicular (outside of the wall of the parent corallite).

Calice (-s; adj. calicular): Cup-like structure at the distal end of solitary and outermost surface of solitary and, respectively, colonial coralla. Corresponding to the part of the skeleton occupied by a polyp.

Calcification center (-s): See Rapid Accretion Deposits.

Carina (-e): A ridge on the lateral septal face, which is formed by a secondary calcification axis that crosses the main septum axis.

Coenosteum (-a; adj. coenosteal) or peritheca (-e; adj. perithecal): Skeleton between corallites. In “robust” corals (as defined in Fukami et al.,2008), the structure of the coenosteum can be costate (composed of costae), vesicular (composed of dissepiments), spinose (composed of spines), or solid.

Colline (-s): A surficial ridge (corresponding with corallite wall) on the calicular surface of a colony.

Colony (-ies): A corallum consisting of two or more corallites whose polyps are integrated to different degree (Coates and Oliver,1973). Colonies in the family Faviidae may have plocoid (corallites separated by coenosteum), cerioid (corallites juxtaposed), meandroid (corallites arranged in series), or phaceloid (corallites forming branches separated by void space) growth forms, as well as various combinations of these forms.

Columella (-e): Vertical axial structure within a corallite. In the family Faviidae, the columella consists of interwoven threads. The threads may extend from the inner septal margins, or they may form separately. The threads may be loosely to tightly (= spongy) interwoven. Centers of adjacent corallites may be linked by interwoven threads (“trabecular linkage”) or by septal plates (“lamellar linkage”).

Corallite (-s): Skeleton of an individual within a colony.

Corallum (-a): Entire skeleton of a coral.

Costa (-e): Radial structure outside the corallite wall. They may be formed by costal parts of costosepta, as is the case in the Family Faviidae; or they may develop independently from them. Costae may be located along or alternating in position with intracalicular radial elements.

Costoseptum (-a): Fan-shaped radial element with outer (costal) and inner (septal) parts.

Dissepiment (-s): Small, horizontal domed plate inside (“endothecal”) or outside (“exothecal”) of a corallite. Dissepiments are often formed at regular intervals and stacked more or less regularly on top of each other to form a continuous structure. They may be thickened by stereome.

Epitheca (adj. epithecal): Usually thin, external thecal sheath surrounding an individual corallite or corallum (in the case of colonial coralla, it is called “holotheca”). In the Family Faviidae, epitheca, if present, surrounds the corallum. The calcareous fibers of the outer epithecal part are oriented distally; whereas those of the inner part (epithecal stereome) show centripetal orientation (Barnes,1972).

Fiber (-s): A slender and elongated object, in particular a scleractinian coral biocrystal. In contrast to abiotically precipitated calcium carbonate crystals, scleractinian biocrystals have nanocomposite structure with mineral nanograins (ca. 30–100 nm in diameter) embedded in a thin layer of organic material. (Cuif et al.,1998; Stolarski and Mazur,2005).

Foliaceous: Colony shape consisting of thin laminae that are curved, undulating, vase-shaped, or in whorls.

Granule (-s): A small elevation on a septal face or a septal tooth. Granules may be pointed, rounded, or bifurcated; they may be scattered over the skeletal surface or aligned. They are formed by secondary calcification axes.

Hydnophoroid: Colony form in which series form interconnected rings surrounding monticules (short ridges or projections); formed by circummural budding.

Paratheca (adj. parathecal): Wall consisting of intercostal or epicostal dissepiments (Fig. 3).

Radial elements: Skeletal structures that radiate toward the axis of a calice (mainly septa, costae, costosepta, paliform lobes, septal spines).

Rapid Accretion Depostits (RAD): Skeletal deposits (“layers of fibers”) formed within well-differentiated regions of skeletal rapid accretion, enriched in organic components (Stolarski,2003; Brahmi et al.,2010). They can form more or less continuous zone (c.f. rapid accretion front) or can be separated from each other (c.f. centers of rapid accretion); Stolarski2003. Traditionally, RAD were recognized in transverse sections of various skeletal elements as “dark spot […] from which fascicles of fibrous crystals radiate toward those of neighboring centers” (Vaughan and Wells,1943, p. 32) and described as centers of calcification.

Septal lobe (-s): A lobe on the distal margin of a septum, which is formed by an additional fan system of centers of rapid accretion.

Septotheca (adj. septothecal): Wall formed by fusion of outer parts of septa, which are typically thickened during ontogeny (Fig. 3). Septotheca may be formed by abortive septa.

Septum (-a): Radially arranged vertical partition within a calice. In a fully developed costoseptum, the inner part (i.e., septal part of costoseptum). Septa are arranged in cycles.

Series (-): Corallites or corallite centers arranged in straight or meandering rows (“valleys”).

Stereome (or stereoplasm): See thickening deposit.

Solitary: A corallum consisting of a single center (monocentric).

Synapticulotheca (adj. synapticulothecal): Wall formed by “synapticulae“, which are defined as rod- or bar-like structures extending between septal faces (Fig. 3).

Thickening deposit (-s): Skeletal deposits formed outside the areas of rapid accretion and typically consisting of layers of fibers continuous with those of RAD but poorer in organic components (Stolarski,2003; Brahmi et al.,2010). There are several formal or informal terms that are alternatively used to describe fibrous deposits e.g., “stereoplasm,” “secondary thickening” (see Ogilvie,1897), “stereome” (see Vaughan and Wells,1943; Sorauf,1972), or “tectura” (Stolarski,1995).

Tooth (pl. teeth): Projections along the septal margins, and/or upper ends of columellar threads. Septal teeth extend from the septa and are not formed by septal substitution. Columellar teeth may or may not differ in shape from septal teeth. Teeth may be spine-like, lobate, paddle-shaped, lacerate, beaded, or acute in shape. They may have circular or elliptical outlines.

Trabecula (-e): Pillars or rods of calcareous fibers radiating from centers of calcification that are aligned in axes (but see Stolarski,2003). Trabeculae have been previously termed “simple” (single axis) and “compound” (multiple axes) and arranged in single or multiple “fan systems” (see Wells,1956); however, these terms are obsolete based on up-to-date models of septal growth (Stolarski,2003).

Trabeculotheca (adj. trabeculothecal): Wall formed by vertical plates developed between costae; vertical plates (trabeculothecal segments) are perpendicular in orientation to the septa and have distinct centers of rapid accretion (Fig. 3). In ontogeny, trabeculotheca is preceded by marginotheca (see Stolarski,1995).

Wall (-s) or theca (-e): Skeletal structure uniting the outer edges of septa in a corallite.

Museum abbreviations

BM(NH): Natural History Museum, London, UK.

MNHN: Muséum national d'Histoire naturelle, Paris, France.

SUI: University of Iowa Paleontology Repository, Iowa City, IA, USA.

UI: University of Iowa, Iowa City, IA, USA.

UF: Florida Museum of Natural History, Gainesville, FL, USA.

USNM: National Museum of Natural History, Smithsonian Institution, Washington, DC, USA.

YPM: Yale Peabody Museum, New Haven, CT, USA.

RESULTS

Macromorphological Characters

Coralla and calices

The 19 studied genera consist exclusively of colonial forms; budding is either intracalicular or extracalicular or both (Supporting Information Table 3). In two Pacific genera [Pectinia (XVII-E), Mycedium (XVII-E)], there is a central polymorphic corallite, and intracalicular budding is circumoral around this central corallite. In the other 17 genera, there is no evidence of polymorphism. Colony shapes in the 19 genera are usually massive, but sometimes they are foliaceous [the Pacific genera Merulina (XVII-A), Pectinia (XVII-E), Mycedium (XVII-E)] or branching [the Pacific genera Caulastraea (XVII-D) and Hydnophora (XVII-H)].

Colony forms are highly variable (Supporting Information Table 3) and range from subcerioid or cerioid [corallite walls juxtaposed; e.g., the Pacific genera Favites (XVII-F) and Goniastrea (XVII-A, F)]; to plocoid [corallite walls separated by a well-developed coenosteum; e.g., the Pacific genera Cyphastrea (XVII-C) and Echinopora (XVII-I), and the cosmopolitan genera Favia (XVII-A, B; XXI) and Montastraea (XVII-C,G,F; XVI)]; to meandroid [corallites form series; e.g., the Atlantic genera Colpophyllia (XXI), Diploria (XXI), and Manicina (XXI), and the Pacific genera Leptoria (XVII-G), Platygyra (XVII-G), and Oulophyllia (XVII-D)]; to phaceloid [e.g., corallites separated by void space; e.g., the Pacific genus Caulastraea (XVII-D)]; and even to flabello-meandroid [corallite series are separated by void space; e.g., the Pacific genus Trachyphyllia (XVII-B)], hydnophoroid [very high collines or “monticules” produced by circummural budding; e.g., the Pacific genus Hydnophora (XVII-H)], and having no definite corallite walls on thecalical surface [“corallites organically united”using the terminology of Vaughan and Wells (1943), e.g., Pectinia (XVII-E), Mycedium (XVII-E)].

By the same token, numbers of corallites per series (Supporting Information Table 3) range from one in genera with extracalicular budding [e.g., Montastraea (XVII-C,G,F; XVI), Cyphastrea (XVII-C), Echinopora (XVII-I), Diploastrea (XV)] to more than 10 in some genera with intracalicular budding [e.g., Merulina (XVII-A), Hydnophora (XVII-H)]. Corallites range in size from small (<4 mm) to medium (4–10 mm) in “Atlantic faviids” (clade XXI) and from small to very large (15–30 mm) in “Pacific faviids” (clade XVII). Calice relief ranges from low (<2 mm) to high (4–10 mm) in “Atlantic faviids” and from low (<2 mm) to very high (>10 mm) in “Pacific faviids” (Supporting Information Table 3). Epitheca is well-developed in both “Atlantic faviids” and “Pacific faviids” but does not occur in some Pacific genera [e.g., Merulina (XVII-A), Oulophyllia (XVII-D), Pectinia (XVII-E), Mycedium (XVII-E)].

Clearly, no consistent differences exist in corallum or corallite-level characters between Atlantic and Pacific faviids as traditionally defined (Supporting Information Table 3). As in Atlantic and Pacific mussids, the similarities in colony form between Atlantic and Pacific taxa are so striking that Diploria (= Maeandra) has sometimes been referred to as the Atlantic counterpart of Platygyra (=Coeloria) and vice versa (see discussion in Verrill,1901). However, corallum or corallite-level characters appear to be diagnostic of two subclades: 1) subclade XVII-E (Pectinia, Mycedium) is distinguished by circumoral budding and the lack of corallites walls (corallites organically united) and 2) subclade XVII-H (Hydnophora) is distinguished by a hydnophorid colony form.

Radial elements

No consistent differences could be detected between Atlantic and Pacific genera, or between subclades, in number of septal cycles, relative thicknesses of costae or septa in different cycles, septal spacing, or development of minor septa (Supporting Information Table 3); these characters have traditionally been used in scleractinians to distinguish species (Vaughan1902,1907). Confluent septa are not present in “Atlantic faviids” but occur in subclades XVII-A (Merulina), XVII-G (Leptoria, Platygyra), XVII-D (Oulophyllia), and XVII-E (Pectinia, Mycedium) in “Pacific faviids.” Only two genera have well-developed septal lobes: Manicina (XXI) in the Atlantic and Trachyphyllia (XVII-B) in the Pacific. Several genera have paliform lobes: Diploria (XXI) in the Atlantic; and Cyphastrea (XVII-C), Favia (XVII-A,B), Merulina (XVII-A), Goniastrea (XVII-A), Favites (XVII-F), Montastraea (XVII-F) in the Pacific.

Columella and endotheca

Columellae are formed by intermingling threads (Supporting Information Table 3), which extend from the inner septal margins (= trabecular), in all genera except Leptoria (XVII-G) and Hydnophora (XVII-H). They are generally larger in size (i.e., their diameter is greater than one quarter of the calice width) in “Atlantic faviids” than in “Pacific faviids,” with the exception of Colpophyllia (XXI) in the Atlantic. Leptoria and Hydnophora have lamellar columellae. Endothecal dissepiments range from sparse to abundant, with sparse, moderate, and abundant dissepiments occurring in both “Atlantic faviids” than “Pacific faviids.”

Summary

No single macromorphological character or combination of macromorphological characters distinguishes “Atlantic faviids” from “Pacific faviids.” In the traditional classification system of Vaughan and Wells (1943) and Wells (1956), faviid genera are distinguished primarily by colony form, but many of the same colony forms exist in both Atlantic and Pacific genera. As noted above, colony form is diagnostic of only two subclades: XVII-E (Pectinia, Mycedium) and XVII-H (Hydnophora). Examination of radial elements, columellae, and dissepiments reveals no diagnostic differences between “Atlantic faviids” and “Pacific faviids,” or among subclades within clade XVII.

Micromorphological Characters

Septal teeth and granulation, and columella structure

SEM reveals distinct differences in the shape of septal teeth between “Atlantic faviids” and “Pacific faviids” (Supporting Information Table 4). In Atlantic genera, septal teeth are usually regular and paddle-like or tricorne in shape, with the paddle axis oriented perpendicular to the axis of the septum (see also Cuif and Perrin,1999; Cuif et al.,2003), whereas in Pacific genera, septal teeth are irregular and spine-like or ”lacerate” (equidimensional, distinctively multidirectional) in shape (Fig. 2). Teeth in subclade XVII-D (Caulastraea, Oulophyllia) consist of low spines; teeth in subclades XVII-F (Favites, Goniastrea,Montastraea) and XVII-G (Leptoria, Platygyra) consist of longer spines. Diploastrea has large triangular teeth, which have different shapes in different septal cycles. All of the other Pacific genera that were studied have teeth that have multidirectional calcification axes and are highly irregular.

Septal granules are strongly aligned in “Atlantic faviids,” and weakly aligned or scattered in “Pacific faviids” (Supporting Information Table 4). The granules range from low to high spikes, with distinctively high spikes occurring in XVII-C (Cyphastrea). The area between teeth ranges from smooth in clade XV (Diploastrea) and subclades XVII-A (Goniastrea, Merulina, Montastraea), XVII-C (Cyphastrea), XVII-F (Favites, Goniastrea,Montastraea), XVII-G (Leptoria), and XVII-I (Echinopora); to horizontal bands in subclade XVII-E (Pectinia, Mycedium); to a possible palisade-like structure (a line of small vertical rods) in subclades XVII-A (Favia stelligera), XVII-B (Favia, Trachyphyllia), XVII-D (Caulastraea, Oulophyllia), XVII-G (Platygyra), and XVII-H (Hydnophora). Columella structure ranges from compact to spongy in both Atlantic and Pacific genera, and contrary to its common usage in traditional classification, it does not appear to be diagnostic.

Summary

Like Atlantic and Pacific mussids (Budd and Stolarski,2009), “Atlantic faviids” and “Pacific faviids” differ in tooth shape, tooth and septal granulation, and the structure of the interarea between teeth. Teeth are regular and paddle-shaped or blocky in “Atlantic faviids” (clade XXI), and irregular and spine-shaped or multidirectional in “Pacific faviids” (clade XVII). Granules are strongly aligned in “Atlantic faviids,” and scattered or weakly aligned in “Pacific faviids.” Highly spiked granules are diagnostic of subclade XVII-C (Cyphastrea), and horizontal bands between teeth are diagnostic of subclade XVII-E (Pectinia, Mycedium).

Microstructural Characters

Wall structure and coenosteum

The structure of the corallite wall and coenosteum are best observed in transverse thin section and are, therefore, treated herein as microstructural, although relatively coarse in scale. In both Atlantic and Pacific genera, corallite walls range from septothecal (with and without abortive septa) to trabeculothecal to parathecal. With the exception of Colpophyllia (parathecal; Fig. 4F), corallite walls are primarily septothecal in the observed “Atlantic faviids” in clade XXI (Fig. 4A–E) and in the Montastraea annularis complex (Fig. 7C; Supporting Information Table 5). Montastraea cavernosa is unusual among “Atlantic faviids” in having abortive septa (Fig. 13B). Within “Pacific faviids” (clade XVII), Cyphastrea (subclade C) is unique in having a septothecal wall (Fig. 7A,B); and Diploastrea (clade XV, Fig. 13C) is unique in having a synapticulothecal wall. Subclades XVII-A (G. pectinata, F. stelligera, M. curta, Merulina; Fig. 5) and XVII-I (Echinopora; Fig. 13A) are septothecal with abortive septa. Subclades XVII-G (Leptoria, Platygyra; Fig. 11) and XVII-H (Hydnophora; Fig. 12) are distinguished by having trabeculothecal walls. The remaining subclades have para-septothecal walls (B; Fig. 6), or parathecal walls with stereome (E; Fig. 9), or they contain species with either parathecal or trabeculothecal walls (D, F; Figs. 8 and 10).

The coenosteum is generally costate in “Atlantic faviids,” with the exception of Diplora clivosa in which the walls are fused and coenosteum is absent (cerioid). It is limited in Colpophyllia natans, which possesses a distinctive double-wall, and well-developed in Diploria labyrinthiformis, which possesses a distinctive ambulacral groove. By contrast, the coenosteum is highly variable in “Pacific faviids,” with only three subclades having distinctive characteristics: subclade XVII-C (Cyphastrea but not the M. annularis complex), which has a spinose coenosteum; subclade XVII-E (Pectinia, Mycedium), which has a vesicular or solid coenosteum; subclade XVII-I (Echinopora), which has an extensive costate coenosteum.

Centers of rapid accretion and thickening deposits

Centers of rapid accretion in “Atlantic faviids” (clade XXI) range from clustered to aligned (forming a medial line) within costae, septa, and columellae (Supporting Information Table 5). They differ from other clades in the presence of carinae, which are formed by secondary lines of centers of rapid accretion that cross the medial axis line of the septum. The carinae correspond with paddle-shaped septal teeth and ridges (aligned granules) on the septal face, which are observed by study of micromorphology. Atlantic Montastraea lack carinae. The M. annularis complex has faint centers of rapid accretion (Fig. 7C), whereas M. cavernosa (clade XVI; Fig. 13B) has well-defined, discrete centers.

Centers of rapid accretion in “Pacific faviids” (clade XVII) also range from clustered to aligned (forming a medial line) but may also consist of a combination of both patterns, in which aligned centers are broken at regular intervals by clusters of centers. Subclades C (Cyphastrea, Fig. 7A,B) and I (Echinopora; Fig. 13A) have clustered centers. By contrast, centers of rapid accretion are strongly aligned in subclades D (Caulastrea, Oulophyllia, Fig. 8), E (Pectinia, Mycedium, Fig. 9), and H (Hydnophora, Fig. 12), with distinctive carinae occurring in subclade D. Centers of rapid accretion in subclades F (Favites, Pacific Montastraea, G. aspera, Fig. 10) and B (Favia favus, F. pallida, Trachyphyllia; Fig. 6) are also aligned, with medial axis lines on septa broken by clusters of centers. Subclades A (Merulina, G. pectinata, F. stelligera, M. curta; Fig. 5) and G (Platygyra, Leptoria; Fig. 11) have thick fibrous tissue associated with their costosepta. Diploastrea (clade XV; Fig. 13C) has discrete centers of rapid accretion surrounded by well-developed thickening deposits containing concentric rings, similar to those found in the family Mussidae.

Summary

With the exception of Diploastrea (clade XV) which has a uniquely synapticulothecal wall, no single microstructural character distinguishes “Atlantic faviids” (clade XXI) from “Pacific faviids” (clade XVII), or Montastraea cavernosa (clade XVI). However, clades XVI and XXI can each be distinguished using various unique combinations of microstructural characters, as can subclades within clade XVII. These results contrast with those of micromorphological characters, which do show diagnostic differences among major clades.

Summary of Diagnostic Characters

Clade XXI (Atlantic Favia, Diploria, Manicina, Colpophyllia; Fig. 4); septothecal wall, with occasional trabeculothecal elements (except Colpophyllia, which is exclusively parathecal); regular paddle-shaped septal teeth, which are relatively stout and blocky in appearance; carinae that correspond with widely spaced aligned granules on septal faces.

Clade XVII: irregular, spine-shaped or multidirectional septal teeth, aligned parallel to the septal plane.

Subclade XVII-A (Merulina, G. pectinata, F. stelligera, M. curta; Fig. 5): septothecal wall with abortive septa, sometimes with trabeculothecal elements (Merulina); weakly to strongly aligned centers of rapid accretion, with thick fibrous tissue; multidirectional septal teeth; F. stelligera differs by sometimes having discrete centers of rapid accretion, especially within costae, and a palisade interarea between teeth.

Subclade XVII-B (Favia favus, F. pallida, Trachyphyllia; Fig. 6): parathecal wall, aligned centers of rapid accretion, with lines broken by clusters of centers; multidirectional septal teeth with a palisade interarea.

Subclade XVII-C (Cyphastrea, Montastraea annularis complex; Fig. 7): septothecal wall; faint centers of rapid accretion, in clusters; multidirectional septal teeth, with widely scattered granules.

Subclade XVII-D (Oulophyllia, Caulastraea; Fig. 8): parathecal or trabeculothecal wall; strongly aligned centers of rapid accretion with carinae; low spine-shaped teeth with a palisade interarea.

Subclade XVII-E (Pectinia, Mycedium; Fig. 9): parathecal wall; thickening deposits composed of stereome (very fine fibers); strongly aligned centers of rapid accretion; multidirectional septal teeth with a horizontally banded interarea.

Subclade XVII-F (Favites, Pacific Montastraea, G. aspera; Fig. 10): parathecal wall (except Goniastrea); aligned centers of rapid accretion, with lines broken by clusters of centers; spine-shaped septal teeth.

Subclade XVII-G (Platygyra, Leptoria; Fig. 11): trabeculothecal wall; aligned centers of rapid accretion, with thick fibrous tissue; spine-shaped septal teeth.

Subclade XVII-H (Hydnophora; Fig. 12): hydnophoroid growth form, trabeculothecal wall; strongly aligned centers of rapid accretion; multidirectional septal teeth with a palisade interarea.

Subclade XVII-I (Echinopora; Fig. 13A): septothecal wall with abortive septa, extensive costate coenosteum; centers of rapid accretion in clusters; multidirectional septal teeth.

Clade XVI (Montastraea cavernosa; Fig. 13B): septothecal wall with abortive septa; discrete centers of rapid accretion; blocky paddle-shaped septal teeth.

Clade XV (Diploastrea; Fig. 13C): synapticulothecal wall; discrete centers of rapid accretion surrounded by well-developed thickening deposits containing concentric rings.

DISCUSSION

New Diagnostic Characters

Differences between Atlantic and Pacific faviids

This study represents a continuation of our ongoing survey delineating morphologic characters that can potentially be used in phylogenetic analyses and systematic revisions of the families Faviidae and Mussidae and related taxa. We show that wall microstructure and the arrangement and distinctiveness of centers of rapid accretion within costosepta differ among molecular clades and subclades associated with the traditional family Faviidae. These microstructural features were first described in many faviid taxa by Chevalier (1971,1975), whose exquisite drawings inspired the present study. However, Chevalier did not attempt to use these features in classification, or to define morphological characters and their states, and systematically illustrate and compare these characters among taxa, as in this study. In addition, we build upon our previous work on micromorphology (Budd and Stolarski,2009), including the shapes of septal teeth, the development of granulation on septal teeth and faces, the shape of the interarea between teeth, and the development of thickening deposits; and compare these previously described micromorphological characters for the first time among molecular clades and subclades associated with the family Faviidae. Last, we show that most macromorphologic characters that have traditionally been used to distinguish scleractinian families, genera, and species associated with the family Faviidae exhibit extensive homoplasy, and are only of limited use in scleractinian phylogeny reconstruction and classification.

Specifically, our results show that the most definitive diagnostic differences between “Atlantic faviids” and “Pacific faviids” are: a) micromorphology: the regular, paddle-shaped or blocky teeth of “Atlantic faviids” versus the irregular, spine- or multidirectional teeth of “Pacific faviids”, and b) microstructure: the septothecal wall (with occasional trabeculothecal elements) in most “Atlantic faviids” versus the abortive-septa, trabeculothecal, or parathecal wall structure in most “Pacific faviids”. Exceptions include 1) Pacific subclades XVII-D and E, which form carinae (ridges formed by granules that are transverse to the septal plane) similar in orientation to paddle-shaped teeth, and 2) Cyphastrea, which has a septothecal wall similar to the M. annularis complex. One of the first studies to show that tooth shape is indeed diagnostic of family-level molecular clades was that of Cuif et al. (2003), who mapped the shapes of septal teeth onto a 28rRNA phylogeny. Cuif et al. (2003) showed that “paddle-shaped” septal teeth were diagnostic of a clade composed of faviid+mussid “robust” corals.

In general, we find that morphologic differences between Atlantic and Pacific mussids (Budd and Stolarski,2009) are more pronounced than between “Atlantic faviids” and “Pacific faviids.” Secondary calcification axes are better developed in the teeth of Atlantic mussids; whereas thickening deposits are more extensive in Pacific mussids. As a result, granules are more pronounced and pointed in Atlantic mussids, because they are not engulfed by thickening deposits. Enhanced thickening deposits in Pacific mussids may be responsible for their thicker, more triangular-shaped septal teeth.

Similarly, in Atlantic faviids (as traditionally defined, except Montastraea), secondary calcification axes (transversal axes) are also well-developed, but they are longer and more pronounced than in Atlantic mussids. As a result, in Atlantic faviids, the secondary axes form carinae (ridges formed by granules that are transverse to the septal plane), which are expressed on the calical surface as blocky, paddle-shaped teeth. These results support the grouping of traditionally defined Atlantic faviids and mussids into a single clade (clade XXI), initially discovered by molecular phylogenetics (Fukami et al.,2004,2008), with well-developed secondary calcification axes being the synapomorphy.

Fewer characters (macromorphological, micromorphological, or microstructural) appear to be diagnostic of “Pacific faviids” (clade XVII), whose teeth are more irregular and have both spine-shaped and multidirectional shapes. However, one potential synapomorphy may involve their thinner, more delicate, spine or multidirectional teeth.

The taxonomic importance of the relative development of calcification axes and thickening deposits has been highlighted by researchers working on microstructures of Cenozoic corals (Alloiteau,1957; Chevalier,1971,1975; for review see Stolarski and Roniewicz,2001). For example, Alloiteau (1957) distinguished between “fibreux,” “granuleux,” and “lamellaire” costoseptal histological structure based on the size and arrangement of calcification centers and fibers observed in transverse thin section (Alloiteau,1957, p. 21). In fact, he removed the family Meandrinidae from the suborder Faviina, which also contains the families Faviidae and Mussidae, and raised it to subordinal rank on the basis of its lack of “ornamentation” (e.g., teeth, granulation).

Differences between subclades of “Pacific faviids”

Our results show that wall microstructure agrees with the separation of genus-level subclades of “Pacific faviids” (clade XVII) based on molecular trees (Fukami et al.,2004,2008). Different combinations of characters support each subclade. Septothecal walls are characteristic of subclade XVII-C; trabeculothecal walls are characteristic of subclades XVII-G and H; para-septothecal walls are characteristic of subclades XVII-B; parathecal walls with stereome are characteristic of subclade E. Abortive septa are characteristic of subclades A and I. Members of subclades D and F have variable wall structures (either parathecal or trabeculothecal). Of the two subclades with variable wall structures, subclade F has high spined teeth, whereas subclade D has distinctively low spined teeth. Subclades B and D are further distinguished by weak carinae. Of the two subclades with trabeculothecal walls, subclade G generally has weakly aligned centers of rapid accretion and extensive thickening deposits, whereas subclade H has strongly aligned centers and a hydnophoroid growth form.

Comparisons between these morphological data and support for branches in the molecular tree (Table 2) indicates that in some cases the morphological data may be more informative than the molecular data. For example, based on wall structure, two species with inconsistent molecular placement, Montastraea curta and Favia stelligera, clearly belong to subclade A, and the Montastraeaannularis complex belongs to subclade C.

Taxonomic Implications

Polyphyly in Montastraea

As in Budd and Stolarksi (2009), the taxonomic implications of this are many. First, the genus Montastraea is traditionally defined as having plocoid colonies, with costate coenosteum and a trabecular columella, formed by extracalicular budding (Wells,1956). Wells (1956) states that the genus is also characterized septothecal wall structure; however, our observations indicate that species currently assigned to the genus (Veron,2000) have septothecal (with and without abortive septa) and/or parathecal wall structure. Our results agree with the molecular trees of Fukami et al (2004,2008), which show the genus Montastraea consists of at least four separate genera, which are not cosmopolitan: 1) Atlantic M. annularis complex (Fig. 7C), 2) Atlantic M. cavernosa (Fig. 13B), 3) Pacific Montastraea with abortive septa (Fig. 5C), and 4) Pacific Montastraea with parathecal walls (Fig. 10C,D). The two Atlantic Montastraea are unrelated to other “Atlantic faviids,” but the two Pacific Montastraea belong to separate subclades within clade XVII.

Regarding Atlantic Montastraea, our results support the molecular results of Fukami et al. (2004,2008), which show that M. cavernosa belongs to its own separate clade (clade XVI). M. cavernosa differs from other “Atlantic faviids” by having abortive septa. In the molecular trees of Fukami et al (2004,2008), the placement of the M. annularis complex varies such that it may either belong to, or be closely related to, clade XVII, which is comprised of “Pacific faviids.” Of the different Pacific faviid subclades, the M. annularis complex is morphologically most similar to Cyphastrea (subclade C) because of its septothecal walls and multidirectional, distinctively spiky teeth (Fig. 7). However, it also differs from Cyphastrea in the reduced size of its granules and its costate (not spinose) coenosteum.

The basal placement of M. cavernosa in the molecular trees of Fukami et al. (2004,2008) indicates that this lineage may be ancestral to both Atlantic and Pacific faviids, a hypothesis that is supported by the long fossil record of “cavernosa”-like corals dating back to the Eocene or even to the Mesozoic (Budd et al.,1992,1994). Indeed, M. cavernosa possesses the paddle-shaped teeth that are diagnostic of Atlantic faviids, but it has a wall structure similar to subclades A and B of Pacific faviids.

The placement of the M. annularis complex within the clade of “Pacific faviids” (clade XVII) in the molecular trees of Fukami et al. (2004,2008) appears odd, because it is the only Atlantic coral in a clade composed of exclusively Pacific corals. However, as noted above, the M. annularis complex has unique morphological attributes. Previous interpretations of the fossil record indicate that other Atlantic corals (e.g., Favites, Goniastrea, Leptoria, Trachyphyllia, Hydnophora) may have also belonged to clade XVII in the geological past and subsequently become extinct in the region (Budd et al.,1992,1994). Careful study of the micromorphology and microstructure of these fossils is needed to determine whether they indeed belong to clade XVII.

Regarding Pacific Montastraea, our results also agree with the molecular results of Fukami et al (2004,2008) and show that M. curta has abortive septa, whereas M. valenciennesi and M. magnistellata have parathecal walls. Our findings that members of each subclade are generally characterized by the same wall structure and that wall structures often differ among subclades, indicate that these two groups of Pacific Montastraea belong to different genera.

Polyphyly in Favia and Goniastrea

The genus Favia is traditionally defined as having plocoid colonies, with a costate coenosteum and a trabecular columella, formed by intracalicular budding (Wells,1956). Our results agree with the molecular trees of Fukami et al (2004,2008), which indicate the genus Favia consists of at least three separate genera and is not cosmopolitan: 1) Atlantic Favia fragum (Fig. 4A; note: Favialeptophylla belongs to Mussismilia, see Nunes et al.,2008; Budd and Stolarski,2009), 2) Pacific Favia with abortive septa (Fig. 5A), and 3) Pacific Favia with para-septothecal walls (Fig. 6A,B). Atlantic Favia have the paddle-shaped septal teeth, which are diagnostic of clade XXI, whereas Pacific Favia have equidimensional, spine or multidirectional septal teeth. As in Montastraea, the facts that members of each subclade are generally characterized by the same wall structure and that wall structures often differ among some subclades, suggest that Pacific Favia with abortive septa (F. stelligera) and Pacific Favia with para-septothecal walls (F. favus, F. pallida) are separate genera. The same is true in Goniastrea with abortive septa (G. pectinata; Fig. 5B) versus trabeculothecal (G. aspera; Fig. 10E) wall structure.

Distinctiveness of Diploastrea

Diploastrea differs traditionally in definition from all other members of the family Faviidae, because it is characterized by synapticulothecal wall structure and large septal teeth (Wells,1956). Our observations confirm these differences and reveal the presence of extensive thickening deposits forming concentric rings that are more similar to the family Mussidae than the family Faviidae. These morphological results agree with the molecular trees of Fukami et al. (2004,2008), which show that Diploastrea is basal to all other traditional faviids and mussids. The presence of synapticulae is shared with siderastreids, agariciids, and other “complex” corals (as defined in Fukami et al.,2008), and may be a plesiomorphic trait.

The families Merulinidae, Pectiniidae, and Trachyphylliidae

The families Merulinidae Verrill1866 and Pectiniidae Vaughan and Wells1943 are both traditionally defined as having irregularly dentate septa, formed by one fan system of “compound” trabeculae, i.e., lacerate teeth (Wells,1956, p. F416, F419). They differ from the traditional family Faviidae by having irregular septal teeth; faviids being defined as having “regular” septal teeth. The families Merulinidae and Pectiniidae differ from the traditional family Mussidae in number of trabecular fan systems per septum and size of septal teeth; mussids being defined as having >2 fans systems and large teeth. The families Merulinidae and Pectiniidae differ from one another in that merulinids have “trabecular linkage” among centers, whereas pectiniids have “lamellar linkage” among centers and “organically united” corallites (Vaughan and Wells,1943, p. 153-154). By contrast, the family Trachyphylliidae Wells1956 was originally defined as having two fan systems of simple trabeculae such that the inner fan system forms a prominent septal lobe (Wells,1956, p. F407).

In the molecular tree (Fig. 1), merulinids and trachyphylliids occur in clade XVII, and pectiniids are split between clades XVII and XIX. Of the subclades of clade XVII in this study, merulinids occur in subclades A and H [note: subclade H consists exclusively of the genus Hydnophora, which wasassigned to the family Faviidae by Vaughan and Wells (1943) and Wells (1956)], trachyphylliids occur in subclade B, and pectiniids occur in subclade E. Our observations confirm that traditional merulinids (Merulina) and pectiniids (Pectinia, Mycedium) have irregular “lacerate” (=multidirectional) teeth, but Trachyphyllia also has multidrectional teeth (Fig. 6C) and so do other subclades of “Pacific faviids,” for example, subclade C (Cyphastrea) and the species Favia stelligera and Goniastrea pectinata in subclade B (Supporting Information Table 4). Thus, tooth shape does not separate traditional merulinids, pectiniids, and trachyphylliids from other “Pacific faviids”, supporting the interpretation of clade XVII as representing a single family-level clade containing members of four traditional families, Faviidae, Merulinidae, Pectiniidae, Trachyphylliidae.

Future work

This study provides the groundwork for future morphologic work on the systematics of the family Faviidae: 1) performing morphology-based phylogenetic analyses and quantitatively comparing morphologic and molecular data, 2) formally revising the taxonomy of this polyphyletic group, and 3) incorporating fossils into phylogenetic analyses and examining the divergence of Atlantic and Pacific “faviids” and “mussids” within a geologic context. Although taxon sampling in Budd and Stolarski (2009) and this study is adequate for distinguishing and recognizing diagnostic characters in the major family-level clades (i.e., clades XV, XVI, XVII, XIX, XXI), it is less adequate for distinguishing genus-level subclades within Pacific faviids (clade XVII). More species of traditional Pacific faviids need to be genetically and morphologically characterized to obtain the necessary resolution. Nevertheless, the results presented herein indicate that the study of wall structure and arrangements of centers of rapid accretion and fibers are more effective than traditional macromorphologic characters at distinguishing genera and tracing their evolutionary histories through geologic time.

One question that still remains unresolved is the effect of environment on the new diagnostic characters. Foster (1979) found that the thickness of the costosepta and associated corallite wall in Montastraea annularis changed in response to transplantation between Jamaican forereef and lagoon environments. Cursory examination of thin-sections of the transplanted colonies has shown that arrangements of centers of rapid accretion do not change in response to transplantation, but that thickening deposits are better developed in forereef environments. However, the amount of variation observed in transplanted colonies is far less than that reported herein. Moreover, the colonies in this study were collected in a range of reef environments at varied geographic locations (Supporting Information Appendix II) and represent a broad spectrum of the variation that exists within Atlantic and Pacific faviids. This sampling and the observed agreement between morphologic and genetic data indicates that the reported morphologic differences are genetic in origin and not caused solely by phenotypic plasticity in response to environmental factors. Support for environmental stability of some microstructural features is also provided by experiments showing that even drastic differences in seawater geochemistry (carbonate-ion concentrations), which cause the suppression of calcification rate, do not affect the gross micro-architectural and microstructural features of corals. For example, Marubini et al. (2002) showed that scale-like fibrous units typical of skeleton surface of Acropora develop in corals cultured in sea-water with normal and low carbonate-ion concentrations. The hypothesis that the formation of the scleractinian skeleton is biologically controlled down to the microstructural level is also supported by the finding that a phylogenetically well-defined clade of extant micrabaciids (Kitahara et al.,2010), which are recovered from all oceans and from widely different depths, shows a unique and consistent microstructural pattern of thickening deposits in all representatives of the family (Janiszewska et al.,2010).

One final component that will need to be comprehensively discussed in further studies is the link between micromorphological and microstructural characters viewed from an ontogenetic perspective. The biomineralization activity of the polyp is expressed as small-scale microstructural differences that during successive growth steps (skeletal ontogeny) result in development of micromorphological features on the surface of the skeleton. Additional models of skeletal growth, based on growth experiments and more precise preparation methods, are needed to make the connection, and further refine the characters defined herein.

CONCLUSIONS

The results of this morphological study agree with the molecular analyses of Fukami et al. (2004,2008), which show that Atlantic and Pacific “faviid” corals are evolutionarily distinct and belong to different taxonomic groups. Contrary to traditional scleractinian classification, which is based primarily on macromorphology, our observations show that newly recognized micromorphological and microstructural characters are effective at distinguishing not only these two taxonomic groups but also more generally, family-level clades and genus-level subclades within scleractinians belonging to the traditional suborder Faviina. The new characters are based on models of growth of the costosepta and corallite wall, and thus are more likely to be homologous. They involve the shapes and distribution of teeth along the costoseptal margin (micromorphology), and the internal structure of the corallite wall and arrangement of centers of rapid accretion within costosepta (microstructure). Our findings underscore the need for rethinking the morphologic characters on which traditional scleractinian classification is based, and for using refined micromorphological and microstructural characters when tracing the long-term evolutionary history of scleractinian corals and reconstructing their phylogeny.

Acknowledgements

The authors thank Nancy Knowlton and Ewa Roniewicz for discussion; Nancy Knowlton and Hiro Fukami for skeletons with molecular data; the UI Department of Geoscience Petrographic Facilities (Matt Wortel and Kaye Saville) for thin sections; the UI Central Microscopy Research Facility, and the National Museum of Natural History Scanning Electron Microscopy Lab (Scott Whittaker and Linda Cole), for SEM photography; Tiffany Adrain (SUI), Steve Cairns (USNM), Gustav Paulay (UF), Eric Lazo-Wasem (YPM), Aude Andouche (MNHN), and Ken Johnson (BM(NH)) for assistance with museum specimens.