MUSSINAE ORTMANN, 1890: 315

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 : 496-499

SUBFAMILY MUSSINAE ORTMANN, 1890: 315

Type genus: Mussa Oken, 1815

Original description: ‘Von der Basis der Koralle erhebt sich keine Ringfalte, die eine echte Mauer abscheidet... Die Septen verbinden sich durch seitliche Verschmelzung zu einer falschen Mauer... Koloniebildung durch Theilung. Vorwiegend acrogenes Wachstum mit reichlicher Traversenbildung.’ ( Ortmann, 1890: 314–315).

Diagnosis: Macromorphology: solitary or colonial; corallites discrete, or arranged in uniserial or multiserial valleys formed by circumoral budding (includes meandroid and phaceloid forms); coenosteum usually absent (except Isophyllia ); medium to large calices with high relief (> 6 mm); widely spaced septa (<six per 5 mm); relatively small trabecular columella, with either lamellar or trabecular centre linkage; reduced epitheca; well-developed endotheca ( Fig. 2 ).

Micromorphology: regular, tall (> 0.6 mm), widely spaced (1–2 mm), spine-shaped septal teeth, with circular bases; interarea of teeth consisting of horizontal bands; weak, aligned septal granules consisting of diffuse spikes ( Figs 3 , 4 ).

Microstructure: mostly parathecal corallite walls, containing trabeculothecal elements; clusters of centres of calcification within the costosepta and columella well developed, widely separated (> 0.6 mm), and connected by medial lines ( Figs 5 , 6 ).

Genera included:

Mussa Oken, 1815

Isophyllia Milne Edwards & Haime, 1851a Mycetophyllia Milne Edwards & Haime, 1848 Scolymia Haime, 1852

Remarks: As explained by Vaughan & Wells (1943: 191), ‘the most marked feature of the group is the large, multi-trabecular septal dentations marking the most complex type of faviid septum’. Both traditional Atlantic and Indo-Pacific ‘mussids’ have spine-shaped or triangular teeth. However, the teeth of traditional Indo-Pacific ‘mussids’ are orientated parallel to the septal plane, whereas the teeth of traditional Atlantic ‘mussids’ are transverse, sometimes forming carinae. Moreover, the septal granulation of traditional Indo-Pacific ‘mussids’ consists of rounded knobs, whereas the granules of traditional Atlantic ‘mussids’ consist of spikes. The walls of traditional Indo-Pacific ‘mussids’ are thickened extensively by stereome (see description in Budd & Stolarski, 2009).

The subfamily Mussinae is monophyletic ( Fig. 7 ) and distinguished from the subfamily Faviinae on the basis of: greater distances (> 0.6 mm) between costoseptal clusters of calcification centres in the Mussinae , teeth with circular bases and weak granules in the Mussinae , and circumoral budding with wide septal spacing (<six septa per cm) in the Mussinae .

Distribution: Atlantic only.

GENUS MUSSA OKEN, 1815: 73 ( FIGS 9A, B , 12A, B , 18A–C , 22A–C )

[all taxa in Oken, 1815 rejected by ICZN opinion 417 (September 1956; ICZN Commission, 1956); but Mussa Oken, 1815 conserved by ICZN opinion 2061 (March 2004; ICZN Commission, 2004)].

Synonyms: Lithodendron Schweigger, 1819, tab. vi [type species: Madrepora angulosa Pallas, 1766: 299– 300 , as listed by Schweigger, 1820: 415–416 (see Wells, 1936: 116).]

Type species: Madrepora angulosa Pallas, 1766: 299– 300 ; by subsequent designation, Vaughan, 1918: 122. Holotype is lost ( Matthai, 1928). We herein designate specimen YPM9035 ( Fig. 9A, B ) collected by J. C. Lang at Lime Cay off Port Royal, Jamaica as the neotype of Mussa angulosa (Pallas) .

Original type species locality: ‘Mare Americanum’ ( Pallas, 1766: 300) [Recent].

Early descriptions:

1. ‘Sterne vertieft am End, meist gedrückt, weiter als Stamm, einzel oder wenige.’ ( Oken, 1815: 73).

2. ‘Large Astraeidae , segregate, also explanatoglomerate; tentacles numerous, unequal, the inner tumid. Coralla calicularly branched or explanatoglomerate; calicles very stout, subturbinate, with orbiculate or lobed cells, sometimes very broadly compressed with the cells long meandering; exterior stoutly lamello-striate and echinato-dentate; lamellae coarsely dentate or gashed-toothed, unequally exsert.’ ( Dana, 1846: 173).

3. ‘Le polpier est composé, élevé, plus ou moins cespiteux; les polypiérites sont libres entre eux ou unis en séries toujours simples et toujours libres latéralement. Les murailles sont nues ou ne présentent qu’une épithèque rudimentaire; elles sont striées longitudinalement et garnies d’épines plus ou moins nombreuses. Les calices sont plus ou moines déformés; ils ont une fossette bien distincte et même assez profonde; la columelle est spongieuse et plus or moins développée. Les systèmes cloisonnaires sont en général inégaux et irréguliers, mais on reconnaît ordinairement dans l’appareil septal des traces manifested du type hexaméral. On trouve toujours des cloisons nombreuses, débordantes, très-peu granulées et fortement dentées; leurs dents sont longues, mais inégales, les extérieures étant beaucoup plus fortes que les autres et spiniformes. Les loges interseptales sont médiocrement profondes; le tissu endothécal est bien développé.’ ( Milne Edwards, 1857: 328–329).

Subsequent morphological descriptions ( Matthai, 1928 and later): Matthai (1928: 202–208); Wells (1936: 120–121; 1956); Vaughan & Wells (1943: 192, 195; F418); Walton Smith (1971: 92); Zlatarski & Estalella (1982: 165–177); Veron (2000: vol. 3: 64–65).

Diagnosis: Macromorphology: colonial; intracalicular budding. Phaceloid, with short series (usually one to three centres per series, but occasionally up to five); large calices (2.5–4.5 cm) with high relief (> 6 mm), four septal cycles, slightly unequal; thin, curved septa, with wide septal spacing; continuous, spongy (> three threads) columella with trabecular linkage; reduced epitheca; no septal or paliform lobes; abundant endotheca ( Figs 9A, B , 12A, B ).

Micromorphology: high (> 0.6 mm), widely spaced (1–2 mm), spine-shaped, pointed teeth, regularly arranged; layered (banded) interarea of septal teeth; teeth in major and minor septal cycles similar in size; spongy columella, with columellar teeth differing in size and shape from septal teeth; spiky, aligned granules ( Fig. 18A–C ).

Microstructure: parathecal wall with trabeculothecal elements. Widely separated (> 1.2 mm), welldeveloped clusters of calcification centres that cross medial lines; reduced thickening deposits ( Fig. 22A–C ).

Included species [monotypic genus]: Mussa angulosa ( Pallas, 1766: 299) . [Holotype is from ‘Mare Americanum’ and is lost; neotype (herein designated) = YPM9035 , Fig. 9A, B , Port Royal , Jamaica.]

Remarks: Concepts of the genus have progressively narrowed through time. In Vaughan & Wells (1943) and Wells (1956), the genus was broadly defined to include solitary forms [e.g. Scolymia (= Lithophyllia )] in addition to the phaceloid colonial form Mussa angulosa . Later Wells (1964), followed by Walton Smith (1971), separated solitary Scolymia from colonial Mussa .

In the classification system of Vaughan & Wells (1943) and Wells (1956), the genus Mussa is distinguished by having a phaceloid colony form, regular septal dentation, and corallite centres with trabecular linkage ( Vaughan & Wells, 1943: 192, 195). Our observations show further that, like other members of the subfamily Mussinae , it has a predominantly parathecal corallite wall; centres of calcification within the costosepta and columella that form a medial line crossed by well-developed clusters of centres; spine-shaped septal teeth; and septal granules consisting of aligned spikes. In addition to colony form, this genus differs from the meandroid members of the subfamily Mussinae by having four septal cycles and a spongy columella. Atlantic Mussa is superficially similar in growth form to Indo-Pacific Lobophyllia , but differs by having trabecular linkage (not lamellar) between corallite centres, better developed septal granules, and limited thickening deposits (e.g. thin septa).

The genus Mussa is recognized as monotypic by Walton Smith (1971); Zlatarski & Estalella (1982); Cairns, Hoeksema & Land (1999); and Veron (2000).

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 9. Type specimens of type species of genera in the subfamily Mussinae. A, B, genus Mussa Oken, 1815; Madrepora angulosa Pallas, 1766; neotype (designated herein) = YPM9035, Lime Cay, Port Royal, Jamaica. C, D, genus Isophyllia Milne Edwards & Haime, 1851a; Oulophyllia? spinosa Milne Edwards & Haime, 1849 [= Isophyllia sinuosa (Ellis & Solander)]; holotype = MNHN-scle866, unknown locality. E, F, genus Mycetophyllia Milne Edwards & Haime, 1848; Mycetophyllia lamarckiana Milne Edwards & Haime, 1849; holotype = MNHN-scle910, unknown locality. G, H, genus Scolymia Haime, 1852; Madrepora lacera Pallas, 1766; neotype (designated herein) = YPM9036, Rio Bueno, Jamaica.

Figure 12. Mussa and Scolymia macromorphology. Mussa and Scolymia have large discrete calices (> 4 cm), and a trabecular columella; however Mussa is colonial (phaceloid) and Scolymia is solitary. Mussa has four complete septal cycles, whereas Scolymia has five. A, B, Mussa angulosa (Pallas, 1766); figured specimen = SUI102763 (FA1135), Key Largo, Florida, USA. C, Scolymia lacera (Pallas, 1766); figured specimen = YPM7567, Runaway Bay, Jamaica. D, Scolymia lacera (Pallas, 1766); figured specimen = YPM7568, Runaway Bay, Jamaica. E, F, Scolymia cubensis (Milne Edwards & Haime, 1849); neotype (designated herein) = YPM7569, Runaway Bay, Jamaica. G, H, Scolymia wellsi (Laborel, 1967); holotype = MNHN-scle20175, Abrolhos Reef, Abrolhos Archipelago, Bahia, Brazil.

Figure 18. Mussa and Scolymia micromorphology (scanning electron microscopy): left column, wall; middle column, mid-septum; right column, columella. Both Mussa and Scolymia have high, spine-shaped teeth. Mussa is distinguished by thinner septa, and a distinctively horizontally layered interarea. The columellae of Scolymia have thick, paddle-shaped teeth, in comparison to the thinner platy teeth of Mussa. A–C, Mussa angulosa (Pallas, 1766); figured specimen = SUI102761 (FA1012), Bocas del Toro, Panama. D–F, Scolymia lacera (Pallas, 1766); figured specimen = USNM84920, Discovery Bay, Jamaica. G–I, Scolymia cubensis (Milne Edwards & Haime, 1849); figured specimens = USNM84940, Maria Buena Bay, Jamaica (G, H); SUI102777 (FA1097, SCUB16), Bocas del Toro, Panama (I). J–L, Scolymia wellsi (Laborel, 1967); figured specimen = USNM84926, Angel Reef, Tobago.

Figure 22. Mussa and Scolymia microstructure (transverse thin section): left column, wall; middle column, mid-septum; right column, close-up of clusters. Both Mussa and Scolymia have parathecal walls (w); however, trabeculothecal elements and thickening deposits are better developed in Scolymia. Both genera form well-developed clusters of calcification centres (c) that cross medial lines. These clusters are more closely spaced in Scolymia. A–C, Mussa angulosa (Pallas, 1766); figured specimen = SUI102761 (FA1012), Bocas del Toro, Panama. D-F, Scolymia lacera (Pallas, 1766); figured specimen = USNM1090899, Bahia Concha, Colombia. G–I, Scolymia cubensis (Milne Edwards & Haime, 1849); figured specimen = USNM84939, Maria Buena Bay, Jamaica. J–L, Scolymia wellsi (Laborel, 1967); figured specimen = USNM84926, Angel Reef, Tobago.