FAVIINAE GREGORY, 1900: 29

Budd, Ann F., Fukami, Hironobu, Smith, Nathan D. & Knowlton, Nancy, 2012, Taxonomic classification of the reef coral family Mussidae (Cnidaria: Anthozoa: Scleractinia), Zoological Journal of the Linnean Society 166 (3), pp. 465-529 : 515-518

SUBFAMILY FAVIINAE GREGORY, 1900: 29 .

Type genus: Favia Milne Edwards, 1857

Original description: ‘Compound Aporosa in which the corallum is massive or dendroid; the septa are numerous, imperforate, radial and usually hexameral. The endotheca is dissepimental. Growth is in the main by fission.’ ( Gregory, 1900: 29).

Diagnosis: Macromorphology: colonial only; corallites discrete or arranged in uniaxial series (includes plocoid, meandroid, and phaceloid forms); coenosteum usually present, although limited; costosepta not confluent; epitheca reduced or well developed; septal lobes (except Mussismilia ) ( Fig. 2 ).

Micromorphology: regular, narrowly spaced (<1 mm), tricorne or fan-shaped septal teeth (never spine-shaped or triangular), with elliptical bases orientated transverse to the septal plane; interarea of teeth smooth or consisting of horizontal bands; septal granules strong and aligned ( Figs 3 , 4 ).

Microstructure: septothecal or parathecal corallite walls, containing occasional trabeculothecal elements; clusters of centres of calcification within the costosepta and columella weakly developed (except Mussismilia ), narrowly separated (<0.6 mm), and connected by medial lines; carinae usually well developed ( Figs 5 , 6 ).

Genera included:

Favia Milne Edwards, 1857

Colpophyllia Milne Edwards & Haime, 1848 Diploria Milne Edwards & Haime, 1848

Manicina Ehrenberg, 1834

Mussismilia Ortmann, 1890

Pseudodiploria Fukami, Budd & Knowlton gen. nov.

Remarks: In the classification system of Vaughan & Wells (1943: 153) and Wells (1956: F400), the family Faviidae is distinguished by having a septothecal or parathecal wall; simple trabeculae, in one or two fan systems; dentate septal margins; dissepiments; and relatively small corallites (<10 mm in diameter). As herein defined, the subfamily Faviinae is monophyletic ( Fig. 7 ) and restricted to taxa whose septal teeth are regular and narrowly spaced, with elliptical bases orientated transverse to the septal plane (i.e. paddleshaped), and whose septal granules are strong, spiky, and aligned.

Unlike the subfamily Mussinae , which possesses spine-shaped or triangular teeth and diffuse granulation, the septal teeth of the Faviinae are tricorne or fan-shaped (elliptical bases); and septal granulation is well developed (evenly scattered or organized in lines).

Traditional Atlantic ‘faviids’ (including Montastraea cavernosa and the Orbicella annularis complex) are also distinguished from traditional Indo-Pacific ‘faviids’ on the basis of tooth shape. Indo-Pacific taxa have irregular spine-shaped or multidirectional teeth (often lacerate); whereas Atlantic taxa (excluding the Orbicella annularis complex) have regular, blocky teeth that are often paddle-shaped (see description in Budd & Stolarski, 2011).

Distribution: Atlantic only.

GENUS FAVIA MILNE EDWARDS, 1857: 426

( FIGS 10A–D , 15A–D, 20A–F , 24A–F )

[not Oken, 1815: 67, because all taxa in Oken book rejected by ICZN opinion 417 ( ICZN Commission, 1956)]

Synonyms: None.

Type species: Madrepora fragum Esper, 1795: 79 , pl. 64, figs 1, 2 [= Madrepora ananas Pallas, 1766 ]; by subsequent designation, Verrill, 1901: 88–91. Holotype is lost ( Scheer, 1990; Cuif & Perrin, 1999). We herein designate specimen MNHN-scleFAV560 collected by Mr Ricord in Haiti ( Cuif & Perrin, 1999) as the neotype ( Fig. 10C, D ).

Original type species locality: ‘südlichen Americanischen Meeren’ ( Esper, 1795: 80) [Recent].

Original descriptions:

1. ‘Röhren (=walls) in einem kitt, öffnen sich oben gleich hoch, laufen in leinen gemeinschaftlichen Stamm zusammen.’ ( Oken, 1815: 67).

2. ‘Le polypier se compose de polypiérites unis entre eux par des côtes plus ou moins développées et une exothèque celluleuse. Les calices coservant des bords libres, soit subcirculaires, soit ovalaires. La columelle est spongieuse. Les cloisons sont débordantes; leurs dents internes sont les plus grandes et souvent même simulent des palis. L’endothèque est bien développée.’ ( Milne Edwards, 1857: 426–427).

Subsequent morphological descriptions ( Matthai, 1928 and later): Not in Matthai, 1928 (but see Matthai, 1919); Vaughan & Wells (1943: 163, 166); Wells (1956: 402); Laborel (1969: 191–198); Cuif & Perrin (1999: 137–156); Walton Smith (1971: 79–80); Zlatarski & Estalella (1982: 61–66); Veron (2000: vol. 3: 100–131).

Diagnosis: Macromorphology: plocoid; discrete (one to three centres per series); costate coenosteum; small calices (<4 mm) with three or more septal cycles; continuous, compact trabecular columella; well-developed epitheca; moderate endotheca; small septal lobes ( Figs 10A–D , 15A–D).

Micromorphology: distinctive paddle-shaped teeth, occasionally tricorne, with elliptical bases orientated transverse to the septal plane; smooth interarea of teeth; spiked granules organized in lines; teeth in major and minor septal cycles differ slightly in size ( Fig. 20A–F ).

Microstructure: septothecal wall; small (<0.6 mm), well-defined clusters of calcification centres within costosepta, forming carinae orientated transverse to the septal plane; layered fibrous thickening deposits ( Fig. 24A–F ).

Species included: Favia fragum ( Esper, 1795: 79, pl. 64, figs 1, 2). Holotype is from ‘südlichen Americanischen Meeren’, and is lost; neotype (herein designated) = MNHN-scleFAV560, Figure 10C, D , Haiti.

Favia gravida Verrill, 1868: 354 [syntypes = YPM1465A, B; Fig. 15C, D, Abrolhos Archipelago, Brazil] (= Favia conferta Verrill, 1868: 355 ) [syntypes = YPM1466A, B; YPM8268, Abrolhos Archipelago, Brazil].

Remarks: The genus Favia was originally described by Oken (1815: 67), who listed ‘ Favia ananas ’ first as belonging to the genus. However, according to ICZN opinion 417 ( ICZN Commission, 1956), the names originally proposed by Oken (1815) are rejected. Therefore authorship is based on subsequent use of the name. Ehrenberg (1834) was the second to use the name, but assigned an assortment of species to the genus, all of which have been subsequently assigned to other genera. Cuif & Perrin (1999) indicate ‘Milne-Edwards, 1857’ as the author of Favia , after Verrill (1901). This usage is followed here.

In the classification system of Vaughan & Wells (1943) and Wells (1956), the genus Favia is distinguished by having a plocoid colony form; a costate coenosteum; a parietal (= trabecular) columella; and intracalicular budding. Septal margins are strongly dentate; trabeculae are usually simple, in one or two fan systems; and corallites are relatively small (<10 mm) ( Vaughan & Wells, 1943: 153–154, 163, 166). As discussed above, it is distinguished from Indo-Pacific ‘ Favia ’, herein referred to as Dipsastraea de Blainville, 1830 , on the basis of its paddle-shaped septal teeth and septothecal corallite wall structure.

Our work shows that species traditionally assigned to the genus vary considerably in corallite wall structure (including parathecal, septothecal, and trabeculothecal walls) and in the shape of their septal teeth. We hereby restrict the definition of the genus to species with septothecal walls and multicentred paddleshaped teeth orientated transverse to the septal plane, three characters that the genus Favia shares with Manicina as defined below. Favia is distinguished from Manicina on the basis of its short corallite series (= valleys), small calice width (<4 mm) with low relief, its regular minor septa, and its compact (one to three threads) columella. In addition, the corallite walls of Favia are exclusively septothecal, whereas those of Manicina contain trabeculothecal elements.

Following Laborel (1969), Cairns, Hoeksema & Land (1999) listed two species of Favia ( Favia fragum , Favia gravida ) with septothecal walls from the Caribbean and Brazil; however, both Zlatarski & Estalella (1982) and Veron (2000) synonymized the two species. Walton Smith (1971) recognized F. fragum as distinct, and further split F. gravida into two species ( F. gravida , F. conferta ). Here we list and illustrate two species of Favia ( F. fragum , F. gravida ) following Nunes et al. (2008), who showed F. fragum and F. gravida to be genetically distinct. Favia gravida ( Fig. 15C, D) is distinguished from F. fragum ( Fig. 15A, B) on the basis of its more numerous septa (four complete septal cycles), somewhat longer series, higher calice elevation, and taller, more widely spaced septal teeth.

Following the molecular results of Fukami et al. (2004, 2008), we restrict the definition of the genus Favia to include only Atlantic taxa. The emended genus does not include the following species, which were assigned to it by Veron (2000) and are herein assigned to the genus Dipsastraea de Blainville, 1830 [type species: Madrepora favus Forskål, 1775 (SD: Wells, 1936)].

Species Assigned to Dipsastraea :

1. Favia favus ( Forskål, 1775: 132) [lectotype = ZMK28, unknown locality]; not seen but illustrated in Veron et al., 1977: 26 (fig. 28).

2. Favia albida Veron, 2000 (3): 112 [‘Holotype’ in Veron, 2002: 140 = G55788 (MTQ), Sharm al-Sheikh, Sinai Peninsula, Egypt], seen.

3. Favia danai ( Milne Edwards, 1857: 442) [holotype = USNM00032 , Tonga-Tabou], seen .

4. Favia helianthoides Wells, 1954: 458 [holotype = USNM44980 , Bikini Atoll], seen .

5. Favia lacuna Veron, Turak & DeVantier ; in Veron, 2000 (3): 111 [‘holotype’ in Veron, 2002: 139 = G55836 (MTQ), northern Red Sea coast of Saudi Arabia], seen.

6. Favia laxa ( Klunzinger, 1879: 49) [holotype = ZMB-Cni2193, Red Sea]; seen .

7. Favia lizardensis Veron & Pichon ; in Veron et al. (1977: 45 [holotype = BM (NH)1977.1.1.2, MacGillivray , eastern Australia], seen.

8. Favia maritima ( Nemenzo, 1971: 169) [syntypes = UP C-859, C-861, Puerto Princesca Bay , Palawan, Philippines]; not seen .

9. Favia marshae Veron, 2000 (3): 122 [‘holotype’ in Veron, 2002: 145 = WAM Z12910 ], Ashomore Reef, north-west Australia, not seen.

10. Favia matthaii Vaughan, 1918: 109 [holotype = USNM38381 , Indian Ocean], seen .

11. Favia maxima Veron & Pichon ; in Veron et al. (1977): 43 [holotype = BM (NH)1977.1.1.1, Hook Island , Whitsunday Islands, Great Barrier Reef], seen .

12. Favia pallida ( Dana, 1846: 224) [syntype = USNM00076 , ‘Feejee Islands’], seen .

13. Favia rosaria Veron, 2000 (3): 119 [‘holotype’ in Veron, 2002: 143 = G55822 (MTQ), Milne Bay, eastern Papua New Guinea], seen.

14. Favia rotumana ( Gardiner, 1899: 750) [Neotype = ZMA Coel. 5686, Rotumana, Fiji], not seen but illustrated in Wijsman-Best, 1972: pl. 3, fig. 2.

15. Favia rotundata (Veron & Pichon) ; in Veron et al. (1977): 64 [holotype = BM (NH)1977.1.1.6, southwest Swain Reefs , eastern Australia], not seen .

16. Favia speciosa Dana, 1846: 220 [syntype = USNM00037 , ‘ East Indies’ ], seen .

17. Favia stelligera ( Dana, 1846: 216) [syntype = USNM00055 , ‘Feejee Islands’], seen .

18. Favia truncata Veron, 2000 (3): 113 [‘holotype’ in Veron, 2002: 142 = G55836 (MTQ), Milne Bay, eastern Papua New Guinea], seen.

19. Favia veroni Moll & Borel Best, 1984: 48 [holotype = RMNH 15209 , Kudigareng Keke , Spermonde Archipelago, Indonesia], seen .

20. Favia vietnamensis Veron, 2000 (3): 127 [‘holotype’ in Veron, 2002: 146 = G55859 (MTQ), Nha Trang, Vietnam], seen.

Note: Following ICZN Commission (2011: 162–166), the species named in Veron, (2000) are valid. However, the type specimens designated in Veron (2002) are not valid.

The Atlantic species Favia leptophylla Verrill, 1868: 353 [holotype = YPM1517, Abrolhos Archipelago, Brazil] is transferred for the first time to the genus Mussismilia , as described below under Mussismilia .

Figures

Figure 2. Phylogenetic character mapping of representative macromorphological characters on a subset (clades XV to XXI) of the molecular tree of Fukami et al. (2008). Clade XV is composed of Diploastrea heliopora, and clade XVI is composed of Montastraea cavernosa; clades XVII to XXI are indicated. Ancestral states have been reconstructed using parsimony and calculated using MESQUITE v. 2.72 (Maddison & Maddison, 2009); equivocal branches are in grey. Character states are given in Table 3. A, extracalicular budding; B, corallite integration; C, corallite centre linkage; D, epitheca. Additional macromorphological character maps are in Appendix S5.

Figure 3. Phylogenetic character mapping of representative micromorphological characters on a subset (clades XV to XXI) of the molecular tree of Fukami et al. (2008). Clade XV is composed of Diploastrea heliopora, and clade XVI is composed of Montastraea cavernosa; clades XVII to XXI are indicated. Ancestral states have been reconstructed using parsimony and calculated using MESQUITE v. 2.72 (Maddison & Maddison, 2009); equivocal branches are indicated in grey. Character states are given in Table 3. A, tooth base; B, tooth tips; C, tooth height; D, granule shape and distribution. Additional micromorphological character maps are in Appendix S6.

Figure 4. Micromorphological differences amongst the three major clades (XXI, XIX, XVII). The vertically oriented plates shown in each photo are septa. The projections along their upper margins are teeth, and those across their lateral faces are granules. Clade XXI (A-C) is distinguished by regular blocky teeth with pointed tips, and aligned granules. Clade XIX (D-F) is distinguished by irregular lobate or bulbous teeth with elliptical tooth bases, and rounded granules enveloped by extensive thickening deposits. Clade XVII (G-I) is distinguished by irregular multiaxial teeth with circular bases, and irregular scattered granules. A, XXI, Pseudodiploria strigosa, FA1062, SUI122813, Bocas del Toro, Panama, Atlantic. B, XXI, Mussismilia braziliensis, YPM9104, Abrolhos Archipelago, Brazil, Atlantic. C, XXI, Isophyllia sinuosa, FA1014, SUI102757, Bocas del Toro, Panama, Atlantic. D, XIX, Lobophyllia pachysepta, USNM45515, Murray Island, Australia, Indo-Pacific. E, XIX, Parascolymia vitiensis, USNM91254, Great Palm Island, Australia, Indo-Pacific. F, XIX, Echinophyllia echinoporoides, FA1023, UF2103, Palau, Indo-Pacific. G, XVII, Merulina ampliata, FA1033, USNM100519, Madagascar, Indo-Pacific. H, XVII, Favites halicora, USNM91305, Malaysia, Redang Island, Indo-Pacific. I, XVII, Hydnophora exesa, FA1068, UF2143, Palau, Indo-Pacific.

Figure 5. Phylogenetic character mapping of representative microstructural characters on a subset (clades XV to XXI) of the molecular tree of Fukami et al. (2008). Clade XV is composed of Diploastrea heliopora, and clade XVI is composed of Montastraea cavernosa; clades XVII to XXI are indicated. Ancestral states have been reconstructed using parsimony and calculated using MESQUITE v. 2.72 (Maddison & Maddison, 2009); equivocal branches are indicated in grey. Character states are given in Table 3. A, septotheca; B, paratheca; C, thickening deposits/structure; D, costoseptum centre clusters. Additional microstructural character maps are in Appendix S7.

Figure 6. Microstructural differences amongst the three major clades (XXI, XIX, XVII). All photos are of transverse thin sections at the same scale. The radiating linear plates are costosepta, which are connected in different ways to form corallite walls. Clade XXI (A-C) has costoseptal medial lines that are crossed by transverse structures (tc) such as carinae or clusters of calcification centres; corallite walls are predominantly either septothecal (Favia + Diploria + Pseudodiploria + Manicina subgroup) or parathecal. Clade XIX (D-F) is distinguished by well-developed thickening deposits (tk) and parathecal corallite walls, and widely spaced clusters of calcification centres. Clade XVII (G-H) is distinguished by small, closely spaced clusters of calcification centres (cl); wall structures range the gamut, and appear to be diagnostic of genus-level subclades. A, XXI, Favia fragum, FA1065, SUI122816, Bocas del Toro, Panama, Atlantic. B, XXI, Mussismilia hartti, YPM4516, Maria Farinha, Brazil, Atlantic. C, XXI, Isophyllia rigida, FA1009, SUI102752, Bocas del Toro, Panama, Atlantic. D, XIX, Lobophyllia pachysepta, USNM45515, Murray Island, Australia, Indo-Pacific. E, XIX, Homophyllia australis, USNM85709, Blyth Island, Australia, Indo-Pacific. F, XIX, Oxypora lacera, USNM93809, Madang, Papua New Guinea, Indo-Pacific. G, XVII, Merulina ampliata, UF2051, Palau, Indo-Pacific. H, XVII, Favites halicora, USNM90627, Philippines, Indo-Pacific. I, XVII, Hydnophora exesa, USNM83232, Marshall Islands, Indo-Pacific.

Figure 7. Strict and Adams consensus trees for the morphological phylogenetic analysis (maximum parsimony) focusing on clades XIX and XXI (analysis 1). Numbers above and below nodes are bootstrap values (> 50) and Bremer support values (> 1), respectively. C.I., consistency index; MPTs, most parsimonious trees; R.I., retention index.

Figure 10. Type specimens of type species of genera in the subfamily Faviinae. A–D, genus Favia Milne Edwards & Haime, 1857; Madrepora fragum Esper, 1795; neotype (C, D, designated herein) = MNHN-scle560, Haiti. E, F, genus Colpophyllia Milne Edwards & Haime, 1848; Meandrina gyrosa de Lamarck, 1816 [= Madrepora natans Houttuyn, 1772]; neotype (designated herein) = SUI130588 (Carlon #828), Crawl Cay, Bocas del Toro, Panama. G, H, genus Diploria Milne Edwards & Haime, 1848; Meandrina cerebriformis de Lamarck, 1816; holotype = MNHN-scle102, unknown locality.

Figure 20. Favia, Diploria, and Pseudodiploria micromorphology (scanning electron microscopy): left column, wall; middle column, mid-septum; right column, columella. Favia, Diploria, and Pseudodiploria have paddle-shaped to tricorne teeth with elliptical bases orientated perpendicular to the septal plane. The interarea of teeth is smooth, and granules are spiked and aligned. Teeth in different septal cycles differ slightly in Favia, but are equal in Diploria and Pseudodiploria. A–C, Favia fragum (Esper, 1795); figured specimen = SUI122816 (FA1065), Bocas del Toro, Panama. D–F, Favia gravida (Verrill, 1868); figured specimen = YPM4518, Rio Grande Do Norte State, Fernando de Noronha Archipelago, Brazil. G–I, Diploria labyrinthiformis (Linnaeus, 1758); figured specimen = SUI122810 (FA1061), Bocas del Toro, Panama. J–L, Pseudodiploria strigosa (Dana, 1846); figured specimens = SUI122813 (FA1062), Bocas del Toro, Panama (J, K); SUI122815 (FA1103), Discovery Bay, Jamaica (L). M–O, Pseudodiploria clivosa (Ellis & Solander, 1786); figured specimen = SUI122807 (FA1060), Bocas del Toro, Panama.

Figure 24. Favia, Diploria, and Pseudodiploria microstructure (transverse thin section): left column, whole corallite; middle column, wall; right column, columella. Favia, Diploria, and Pseudodiploria all have septothecal walls (w). In Pseudodiploria, there are also trabeculothecal components, and Pseudodiploria strigosa has abortive septa. Clusters of calcification centres (c) are well defined in Favia, moderately well defined in Diploria, and weak in Pseudodiploria; however, Pseudodiploria has better defined medial lines. Carinae are well developed in Favia, but not in the other two genera; thickening deposits are moderately developed in all three genera. A–C, Favia fragum (Esper, 1795); figured specimen = SUI122816 (FA1065), Bocas del Toro, Panama. D–F, Favia gravida (Verrill, 1868); figured specimen = YPM9085, Rio Formoso, Pernambuco, Brazil. G–I, Diploria labyrinthiformis (Linnaeus, 1758); figured specimen = SUI122810 (FA1061), Bocas del Toro, Panama. J–L, Pseudodiploria strigosa (Dana, 1846); figured specimen = SUI122813 (FA1062), Bocas del Toro, Panama. M–O, Pseudodiploria clivosa (Ellis & Solander, 1786); figured specimen = SUI122807 (FA1060), Bocas del Toro, Panama.