Terebra Bruguière, 1789

Fedosov, Alexander E, Malcolm, Gavin, Terryn, Yves, Gorson, Juliette, Modica, Maria Vittoria, Holford, Mandë & Puillandre, Nicolas, 2019, Phylogenetic classification of the family Terebridae (Neogastropoda: Conoidea), Journal of Molluscan Studies The Malacological Society of London 85 (4), pp. 359-388 : 9-12

Genus Terebra Bruguière, 1789

( Figs 4 , 5 )

Type species: Buccinum subulatum Linnaeus, 1767 ; SD ( Lamarck, 1799: 71).

Synonyms: Triplostephanus Dall, 1908 (type species Terebra triseriata Gray, 1834 ; OD); Cinguloterebra Oyama, 1961 (type species Terebra hedleyana Pilsbry, 1905 = Terebra adamsii E.A. Smith, 1873 ; OD); Dimidacus Iredale, 1929 (new name for Terebrina Bartsch, 1923 , non Rafinesque, 1815; type species Terebra cingulifera Lamarck, 1822 , by typification of replacement name); Myurellina Bartsch, 1923 (type species Terebra ornata Gray, 1834 ; OD); Subula Schumacher, 1817 (unnecessary replacement name for Terebra ; type species Buccinum subulatum , by typification of replacement name); Terebrina Bartsch, 1923 (invalid: junior homonym of Terebrina Rafinesque, 1815 ; type species Terebra cingulifera Lamarck, 1822 , OD); Terebrum Montfort, 1810 (unnecessary emendation of Terebra Bruguière, 1789 ; type species Buccinum subulatum Linnaeus, 1767 , by typification of replaced name); Paraterebra Woodring, 1928 (type species Terebra texana Dall, 1898 ; OD); Panaterebra Olsson, 1967 (type species Terebra robusta Hinds, 1844 ; OD).

Definition: Primarily defined based on phylogenetic analysis of Modica etal. (2019); includes all species in clade Cof Modica etal. (2019), and species showing resemblance in shell morphology, anatomy and distribution to Terebra subulata or any genetically proven member of this clade.

Diagnosis: Diagnostic nucleotide combinations (provided separately for the seven clades of the genus inferred by Modica et al. (2019) in Table 3 .

Shell: Elongate, medium-sized to large, reaching 192 mm; truncated base abruptly constricted to siphonal canal, sometimes with distinct angulation. Sculpture from very weak, limited to often obsolete subsutural groove, to very strong. Subsutural band simple, or consisting of two closely set cords, often gemmate. Lower whorl portion smooth or with varying sculpture, with spiral elements being as strong or stronger than axials. Shell base separated from siphonal canal by concave waist. Aperture elongate to quadrangular.

Anatomy: Rhynchodeal introvert, proboscis, venom gland, salivary glands and radula well developed. Radula of hypodermic marginal teeth, with only bases attached to strongly reduced membrane. Accessory proboscis structure present or absent.

Distribution: Indo-Pacific, West Africa, tropical East Pacific, Caribbean and Western Atlantic.

Remarks: The genus Terebra is here established with boundaries consistent with clade Cof Modica etal. (2019). This clade is subdivided into eight lineages, referred to as C1–C7 ( Fig. 4 ), their relationships being unresolved. Clades C1, C2, C3-2, C4 and C7 are well supported; clade C5 comprises one species only— T. argus . Because of the extreme heterogeneity of clade C, our attempts to provide a molecular diagnosis failed and, therefore, we compiled separate diagnoses for the inferred lineages within clade C ( Table 3 ). Although lineages C3-1 and C3-2 do not constitute a supported clade, this arrangement is not rejected by the phylogenetic analysis and we have grouped them together based on biogeographic considerations. The genus Terebra is also very heterogeneous in regard to shell morphology ( Fig. 5 ); some common morphotypes can be distinguished, but their correspondence with inferred phylogenetic groupings is far from perfect. Below we provide a brief overview of these morphotypes.

Typical Terebra are characterized by a weakly sculptured or smooth, medium-sized shell, with gently convex or subcylindrical whorls, often bearing a pattern of large spots. Species referable to this morphotype are included in clades C1 ( T. subulata and T. guttata ), C4 ( T. ornata ) and C6 ( T. argus ). This morphotype is closest in appearance to Oxymeris and differentiation can be difficult. In most cases Terebra species can be recognized by the narrower anterior notch; however, for definite allocation, examination of the foregut is advised to determine whether proboscis and radula are present.

The fenestrata morphotype comprises the most heavily sculptured species, with a strong, often elevated, gemmate subsutural band that is closely followed by a second spiral band of similar morphology, but usually weaker and/or narrower. The lower portion of the whorl is sculptured with spiral cords, or has a cancellate pattern. Species exhibiting this morphotype include clade C2, and some strikingly similar species in clades C7 ( T. aff. adamsii , T. fenestrata MNHN IM-2013-14908, T. anilis ) and C8 ( T. cumingi species complex). Strong, often elevated, gemmate or beaded spiral elements readily differentiate this morphotype from most terebrid genera. However, a similar pattern is present in Granuliterebra , the species of which are differentiated by their single subsutural band and usually by predominantly axial sculpture on the lower portion of the whorl.

The Triplostephanus morphotype unifies species with a very high spire and very small, quadrate aperture. Whorls are flattened or slightly concave due to a raised subsutural band and the lower part of the whorl is sculptured by regular cords, while axial sculpture is not developed. Most species in clade C5 exhibit this morphotype; however, species with subcylindrical whorls and stepped spire outline (e.g. T. laevigata and T. funiculata ) are found in C5 as well. The combination of a very high spire and flattened whorl outline makes this morphotype very distinctive among Terebridae .

While the three described morphotypes represent extremes of the conchological diversity of Terebra , there is a plethora of intermediate forms. For example, T. taurina and T. fujitai of clade C3 have a divided ribbed subsutural band, similar to the fenestrata morphotype, although notably lower. Similarly, a divided, nodulose subsutural band is present in T. corrugata , a species close to T. subulata in clade C1. The apparent lack of phylogenetic congruence in the distribution of these morphotypes across clade C precludes assignment of any taxonomic status to them. Moreover, the general lack of homogeneity in shell characteristics within the subclades of Terebra makes their establishment as supraspecific taxonomic units pointless as well.

Taking into consideration the great conchological variation within Terebra , it is difficult to suggest general diagnostic criteria for this genus. However, it should be noted that the predominantly spiral sculpture below the subsutural band allows differentiation of Terebra from most other terebrid genera. Similarly, a divided subsutural band has not been recorded in any species outside Terebra . These characters, in combination with the presence of a complete complex of foregut organs and radular teeth of hypodermic type, allow for reliable differentiation of Terebra species.

Included species:

Terebra achates Weaver, 19602 ;

T. adamsii (E. A. Smith, 1873) 2;

T. albocancellata Bratcher, 19883 ;

T. albomarginata Deshayes, 18591 ∗;

T. amanda Hinds, 18441 ;

T. anilis (Röding, 1798) 1;

T. archimedis Deshayes, 18591 ∗;

T. argosyia Olsson, 19712 ;

T. argus Hinds, 18441 ;

T. babylonia Lamarck, 18221 ;

T. balabacensis Aubry & Picardal, 20113 ;

T. bellanodosa Grabau & King, 19283 ;

T. binii (Aubry, 2014) 2;

T. boucheti (Bratcher, 1981) 2;

T. bratcherae Cernohorsky, 19873 ;

T. caddeyi (Bratcher & Cernohorsky, 1982) 2;

T. caelata Adams & Reeve, 18501 ∗;

T. castaneostriata Kosuge, 19793 ;

T. cingulifera Lamarck, 18221 ;

T. circinata Deshayes, 18572 ∗;

T. cognata E. A. Smith, 18773 ;

T. commaculata (Gmelin, 1791) 2;

T. connelli (Bratcher & Cernohorsky, 1985) 2;

T. consobrina Deshayes, 18571 ;

T. corrugata Lamarck, 18221 ;

T. cossignanii Aubry, 20082 ;

T. cumingii (Deshayes, 1857) 1;

T. deshayesii Reeve, 18602 ;

T. donpisori Terryn, 20173 ;

T. elliscrossi (Bratcher, 1979) 1;

T. erythraeensis Terryn & Dekker, 20173 ;

T. eximia (Deshayes, 1859) 2;

T. fenestrata (Hinds, 1844) 1;

T. fernandae Aubry, 19953 ;

T. fernandesi Bouchet, 19833 ;

T. fijiensis (E. A. Smith, 1873) 3;

T. floridana (Dall, 1889) 3;

T. formosa Deshayes, 18571 ;

T. fujitai (Kuroda & Habe, 1952) 1;

T. funiculata Hinds, 18441 ;

T. gabriellae Aubry, 20083 ;

T. gaiae Aubry, 20083 ;

T. giorgioi Aubry, 19993 ;

T. grayi E. A. Smith, 18773 ;

T. guineensis Bouchet, 19833 ;

T. guttata (Röding, 1798) 1;

T. helichrysum Melvill & Standen, 19033 ;

T. histrio Deshayes, 18573 ;

T. hoaraui (Drivas & Jay, 1988) 1;

T. insalli (Bratcher & Burch, 1976) 2;

T. irregularis Thiele, 19253 ;

T. jacksoniana (Garrard, 1976) 3;

T. jenningsi (Burch, 1965) 1;

T. knudseni Bratcher, 19832 ;

T. laevigata Gray, 18341 ;

T. lauretanae Tenison-Woods, 18783 ;

T. levantina Aubry, 19993 ;

T. ligata Hinds, 18442 ;

T. lillianae Withney, 19762 ∗;

T. lima (Deshayes, 1857) 2;

T. lindae Petuch, 19872 ;

T. mamillata (Watson, 1886) 2;

T. mariesi (E. A. Smith, 1880) 2;

T. marrowae (Bratcher & Cernohorsky, 1982) 2;

T. montgomeryi Burch, 19652 ;

T. neglecta (Poppe, Tagaro & Terryn, 2009) 2;

T. nodularis Deshayes, 18593 ;

T. noumeaensis Aubry, 19993 ;

T. ornata Gray, 18341 ;

T. pellyi E. A. Smith, 18773 ;

T. picta Hinds, 18443 ;

T. polygonia Reeve, 18603 ;

T. praelonga Deshayes, 18592 ;

T. pretiosa Reeve, 18422 ;

T. pseudopicta Aubry, 20083 ;

T. pseudoturbonilla Talavera, 19753 ;

T. punctatostriata Gray, 18342 ;

T. punctum (Poppe, Tagaro & Terryn, 2009) 2;

T. quoygaimardi Cernohorsky & Bratcher, 19761 ;

T. raybaudii Aubry, 19932 ;

T. reticularis (Pecchioli in Sacco, 1891) 3;

T. robusta Hinds, 18441 ;

T. rosae Aubry, 20153 ;

T. russetae (Garrard, 1976) 3;

T. salisburyi Drivas & Jay, 19982 ;

T. stearnsii Pilsbry, 18911 ;

T. straminea Gray, 18341 ∗;

T. subangulata Deshayes, 18593 ;

T. subulata (Linnaeus, 1767) 1;

T. succinea Hinds, 18443 ;

T. swobodai Bratcher, 19813 ;

T. tagaroae Terryn, 20172 ;

T. taiwanensis Aubry, 19993 ;

T. taurina (Lightfoot, 1786) 1;

T. tessellata Gray, 18342 ;

T. tricolor G. B. Sowerby I, 18251 ;

T. triseriata (Gray, 1834) 1;

T. twilae Bouchet, 19833 ;

T. unicolor Preston, 19081 ∗;

T. vanuatuensis Aubry, 19993 ;

T. vappereaui Tröndlé, Boutet & Terryn, 20132 ;

T. venilia Tenison-Woods, 18793 ;

T. vicdani (Kosuge, 1981) 2;

T. virgo Schepman, 19133 ;

T. waikikiensis (Pilsbry, 1921) 2.

Figures

Figure 4. Phylogenetic relationships of the subclades of the genus Terebra. Schematic of subclades C1–C7 in the genus Terebra; see Supplementary Material Fig. S1 for species composition (after Modica et al., 2019).

Figure 5. Genus Terebra. A. T. subulata (Subclade C1), MNHN-IM-2013-47287, KAVIENG 2014 Stn KR12, 02◦36.3'S, 150◦46.3'E, 0 m, 62.8 mm. B. T. guttata (Subclade C1) radula, MNHN-IM-2007-30376, SANTO 2006 Stn FR08, 15◦33,1'S, 167◦12.2'E, 3–40 m, 74.6 mm. C. T. aff. fenestrata (Subclade C2), MNHN-IM-2013-46010, MADEEP Stn CP4330, 06◦07.63'S, 149◦12.1'E, 315–625 m, 43.5 mm. D. T. aff. fenestrata 2 (Subclade C2) radula, MNHN- IM-2007-30418, PANGLAO 2005 Stn CP2331, 09◦39'N, 123◦48'E, 256–268 m, 23.1 mm. E. T. fujitai (Subclade C3-1), MNHN-IM-2007-15724, PANGLAO 2005 Stn CP2343, 09◦27'N, 123◦49'E, 273–356 m, 95.7 mm. F. T. triseriata (Subclade C4), MNHN-IM-2013-51211, KAVIENG 2014 Stn KD13, 02◦44.6'S, 150◦43.1'E, 0–15 m, 25.6 mm. G. T. argus (Subclade C5), MNHN-IM-2013-46900, KAVIENG 2014 Stn KR06, 02◦36.3'S, 150◦46.2'E, 3–12 m, 53.7 mm. H. T. babylonia (Subclade C6), MNHN-IM-2013-51267, KAVIENG 2014 Stn KR54, 02◦42.3'S, 150◦39.1'E, 7–10 m, 38.5 mm. I. T. sp. aff. cumingii (Subclade C7), MNHN-IM-2013-46237, MADEEP Stn CP4335, 06◦05'S, 149◦18'E, 240–250 m, 62.5 mm. J. T. cingulifera (Subclade C7) radula, MNHN-IM-2007-30382, SANTO 2006 Stn VM32, 15◦26.6'S, 167◦15.2'E, 0–1 m, 49.7 mm.

Tables

Table 3. Diagnostic combinations of nucleotides for seven subclades of genus Terebra in COI alignment. Subclades named as in Modica et al. (2019).

C1
Species/sequences analysed	4/30
Diagnostic nucleotides:	31: A, 242: C, 265: G, 508: T, 547: T,
	607: A
C2
Species/sequences analysed	4/16
Diagnostic nucleotides:	190: T, 334: A, 536: T, 538: A, 607: G
C3
Species/sequences analysed	5/34
Diagnostic nucleotides:	58: T, 94: A, 154: C, 253: A, 283: G,
	337: A, 409: T, 433: G, 553: T, 631:
	T, 641: T
C4
Species/sequences analysed	9/71
Diagnostic nucleotides:	58: T, 121: T, 127: T, 278: C, 289: T,
	641: C, 643: T
C5
Species/sequences analysed	1/9
Diagnostic nucleotides:	61: G, 274: G, 412: T, 508: C
C6
Species/sequences analysed	8/44
Diagnostic nucleotides:	88: G, 95: T, 148: A, 278: C, 379: T,
	409: T, 481: G, 484: G, 499: G, 562:
	T
C7
Species/sequences analysed	10/19
Diagnostic nucleotides:	76: T, 79: T, 221: G, 222: T