Amalda hilgendorfi (von Martens, 1897 )

Kantor, Yuri I., Castelin, Magalie, Fedosov, Alexander & Bouchet, Philippe, 2020, The Indo-Pacific Amalda (Neogastropoda, Olivoidea, Ancillariidae) revisited with molecular data, with special emphasis on New Caledonia, European Journal of Taxonomy 706, pp. 1-59 : 14-23

Amalda hilgendorfi (von Martens, 1897)

Figs 2–4 , 5–6 , 7 A–G, 8I–J

Ancillaria hilgendorfi von Martens, 1897: 167 , pl. 16 figs 26–27.

Amalda hilgendorfi richeri Kilburn & Bouchet, 1988: 285–287 , figs 18–22 [not figs 23–24 = Amalda cacao sp. nov.].

Amalda vernedei herlaari van Pel, 1989: 14 , figs 1–3.

Amalda hilgendorfi vezzaroi Cossignani, 2015: 24–25 , text figures.

Baryspira hilgendorfi – Kira 1962: 208, pl. 71 fig. 1. — Kuroda et al. 1971: 300 [Japanese text], 196 [English text], pl. 54. fig. 1.

Amalda aureomarginata Northern New Caledonia form – Kilburn & Bouchet 1988: 284, Fig. 13 .

Amalda aureomarginata Chesterfield form – Kilburn & Bouchet 1988: 284, figs 14–17.

? Amalda (Alcospira) hilgendorfi – Ninomiya 1990: pl. 2 fig. 5.

Amalda hilgendorfi – Okutani 2000: 523, pl. 260 fig. 2 (erroneously labelled A. hayashii on the plate) [not pl. 260 fig. 3= A. hayashii ]. — Gratecap 2016b: 4, 12, figs 3–4. — Tsuchida 2017: 995, pl. 288 fig. 3.

Amalda vernedei herlaari – Poppe 2008: pl. 546, figs 7–9.

Amalda hilgendorfi richeri – Gratecap 2014 (part): 14, 19, figs 19–23 [not figs 24–25 = Amalda cacao sp. nov.]

Type material

JAPAN • Holotype of Ancillaria hilgendorfi ; ZMB 31632 .

NEW CALEDONIA • Holotype of Amalda hilgendorfi richeri ; North of New Caledonia , Grand Passage; 18°57′ S, 163°14′ E; 480 m deep; MNHN IM-2000-1378.

ARAFURA SEA • Holotype of Amalda vernedei herlaari ; Arafura Sea; 150 fathoms [270 m]; formerly ZMA Moll. no. 3.88.040, now NBC .

PHILIPPINES • Holotype of Amalda hilgendorfi vezzaroi ; Philippines, Aliguay island; MMM.

Description

SHELL. Variable, narrowly to broadly fusiform with high, acuminate spire; thin to thick microshagreened primary callus impressed at suture, forming distinct to very distinct, obtuse keel above suture. Protoconch exposed, medium large (n =2, first whorl diameter 0.75–0.92 mm), border with teleoconch indistinct. Secondary callus very thin to distinct, tongue-shaped, broadening in middle part and rounded adapically, extending on last three whorls, seemingly less shagreened than primary callus. Plication plate with 2–7 weak ridges, sometimes nearly obsolete. Olivoid groove from narrow and distinct to broad and shallow or nearly obsolete, labral tooth distinct, obtuse. Upper anterior band usually thickened, sometimes heavily. Colour variable, from pale yellowish to brown, olivoid band always lighter than body whorl cloak, anterior band the darkest anterior zone of shell, plication plate usually nearly white, primary callus bordered by lighter narrow band (or line). Height to 81 mm, exceptionally up to 98 mm.

RADULA (n =16 of different morphs). Lateral teeth very similar in all species of Amalda , unicuspid, hook-shaped ( Fig. 7A ). Central tooth normally tricuspid with central cusp shortest. Some variation in central tooth shape ( Fig. 7 B–G); central cusp from extremely short, nearly obsolete, to subdivided in two cusplets, or with additional denticles on side. Cusps of the central tooth either with smooth edges, or serrated ( Fig. 7G ). Morphological variation not related to geographical distribution.

Remarks

Molecular analysis demonstrated high heterogeneity of this species with several subclades, mostly geographically determined ( Fig. 2 ), with groupings from Japan, the Philippines, Papua New Guinea and the Solomon Islands, north of New Caledonia and the Coral Sea, and south of New Caledonia and Norfolk Ridge. This structure is, however, not clear-cut; for example, individuals with identical haplotypes are found in northern New Caledonia (MNHN IM-2009-33734) and Papua New Guinea (MNHN IM-2009-22244) (Haplotype #18, Fig. 3 ). At the same time, the specimens collected in the south of New Caledonia are grouped in two different subclades, one of which also includes one specimen from Papua New Guinea, while the second one includes specimens from southern and northern New Caledonia and the Coral Sea, as well as one specimen from Papua New Guinea.

This suggests that despite a non-planktotrophic larval development, larval dispersal in A. hilgendorfi over time can take place across large geographic distances. The presence in New Caledonia of two highly divergent genetic groups (marked by green oval and green rectangle on Fig. 3 ), both with affinities with haplotypes from Papua New Guinea, suggests that larval exchange between these distant regions might have been quite frequent.

The species is variable in shell shape and colouration. Several morphs could be distinguished, mostly geographically determined and not necessarily distinct molecularly. This has resulted in the description of three subspecies. Moreover, morphologically very similar sympatric specimens may belong to different subclades. For a better characterization of the variability, we describe these morphs separately.

General distribution

Amalda hilgendorfi is broadly distributed in the West Pacific, recorded from Japan, the Philippines, Papua New Guinea and the Solomon Islands, eastern Australia, the Coral Sea, and New Caledonia.

Nominotypical ( Japan) morph Figs 2 (as Japan), 4A–D

Material examined

Three sequenced specimens ( Table 1).

Remarks

Morph with a single identified haplotype ( Fig. 3 ).

Shell broad-fusiform (SL up to 53 mm, holotype 50 mm) dark-coloured, with chestnut-brown primary callus and well-defined light purplish secondary callus ( Fig. 4 A–D). Body cloak orange-brown. Olivoid band light yellowish. Upper anterior band strongly convex, of same colour as body whorl cloak, lower anterior band much lighter, yellowish. Plication plate white, with 3–4 indistinct to nearly obsolete plicae. First protoconch whorl diameter 0.8–0.92 mm (mean 0.88, n=3). Depth range 150–350 m ( Tsuchida 2017), sequenced specimens from 230– 280 m.

Philippines morph Figs 2 (as Phil), 4E–G

Material examined

Two sequenced specimens ( Table 1).

Remarks

Both sequenced specimens cluster together ( Fig. 2 ), two haplotypes identified ( Fig. 3 ).

Shell slender (largest specimen with SL 40.3 mm), coloured in different shades of brown, with lighter olivoid band and slightly convex upper anterior band having nearly median obtuse ridge ( Fig. 4 ). In shell shape and colouration this form matches the subspecies A. hilgendorfi vezzaroi Cossignani, 2015 , described from Aliguay Island, Philippines. This same morph is illustrated by Poppe (2008) as Amalda vernedei herlaari van Pel, 1989 (part: pl. 546 fig. 7) from Balut Island in 100–150 m; this illustrated shell attains 67 mm, which is significantly larger than ours. Depth range of sequenced specimens 437– 740 m.

Papua New Guinea and Solomon Islands morph Figs 2 (as PNG and Sol), 4H–L

Material examined

Sequenced material

16 sequenced specimens ( Table 1).

Not sequenced material

SOLOMON SEA • 1 lv; SE Engeneer group Island; 10°45′ S, 151°06′ E; 470–526 m deep; MADEEP; stn DW4300; MNHN IM-2013-45679 • 1 lv; SE of d’Entrecasteaux Islands; 9°48′ S, 151°33′ E; 278– 420 m deep; MADEEP; stn DW4314; MNHN IM-2013-45800 .

PAPUA NEW GUINEA • 1 lv; N Cape King William; 6°3′ S, 147°36′ E; 450–480 m deep; PAPUA NIUGINI; stn DW3992; MNHN IM-2013-19808 • 1 lv; 6°00′ S, 147°38′ E; 785 m deep; PAPUA NIUGINI; stn DW3992; MNHN IM-2013-19856 .

Remarks

The population from the Solomon Islands and Papua New Guinea is molecularly heterogeneous; although most of them forming a highly supported clade ( Fig. 2 ), some specimens are scattered along the tree. One specimen (MNHN IM-2009-23330, Fig. 4L ) groups with the morph from south of New Caledonia; while another (MNHN IM-2009-22244, Fig. 4K ) groups with the specimens from north of New Caledonia sharing the same haplotype ( Fig. 3 ). In total, seven haplotypes were identified (two from the Solomon Islands and five from Papua New Guinea).

Shell large (SL up to 81.2 mm (MNHN IM-2013-45800), although most specimens are below 55 mm), resembling the population from north of New Caledonia, although generally of darker orange-brown colour and lacking the purplish colouration of the callus that is often present in the northern New Caledonia morph. Upper teleoconch whorls sometimes with obtuse calloused carina. Upper anterior band either evenly strongly convex or with poorly defined submedian carina, lower anterior band always yellow-brown, although sometimes very light. Columellar ridges differently pronounced, 3–7 in number.

This form was described as Amalda vernedei herlaari van Pel, 1989 (Arafura Sea, no exact locality), and later considered a subspecies of A. hilgendorfi ( Cossignani 2015) . The shell can attain 98 mm (holotype of Amalda vernedei herlaari ). Depth range 335– 785 m.

New Caledonia morphs Figs 2 (as CS, nNC, sNC), 5, 6, 7F-G

Remarks

The specimens from New Caledonia form two distinct and supported molecular subclades ( Fig. 2 ). One of them includes only specimens from south of New Caledonia (mostly around Île des Pins), while the second one combines specimens from southern and northern New Caledonia as well as from the Coral Sea. Each subclade includes one specimen from Papua New Guinea (see above). Morphologically, the specimens from south of New Caledonia around Île des Pins are very similar, although they belong to different subclades. Conversely, specimens from the Coral Sea and north of New Caledonia are morphologically very variable, despite belonging to the same subclade.

Coral Sea morph Figs 2 (as CS), 5A–F, 7G

Material examined

Sequenced material

15 sequenced specimens ( Table 1).

Not sequenced material

CORAL SEA • Material listed by Kilburn & Bouchet (1988) • 1 lv; 19°34′ S, 158°40′ E; 400–413 m deep; EBISCO; stn DW2607; MNHN IM-2007-33278 • 1 lv; 20°51′ S, 161°00′ E; 557–565 m deep; EBISCO; stn CP2643; MNHN IM-2007-33292 • 1 lv; 19°45′ S, 158°40′ E; 386–428 m deep; KANADEEP 1; stn DW4975; MNHN IM-2013-63902 .

Remarks

Shell large (SL up to 66 mm), usually light coloured, rarely nearly white except light yellowish primary callus and anterior band. Very distinct callused carina occupying mid-whorl position appearing on fourth or fifth teleoconch whorl ( Fig. 5 A–B, D). Secondary callus indistinct. Young specimens oval ( Fig. 5 E–F), large ones fusiform. Upper part of plication plate light yellowish. Upper anterior band strongly convex, in large specimens with obtuse and very broad (about ¾ of anterior band) ridge. At least one specimen (SL 51.3 mm, MNHN IM-2007-33289, Fig. 5C ) did not have a callused carina on the spire and had a uniformly white plication plate. Number of columellar ridges variable from 2–3 in small specimens to 6–7 in medium-sized and larger ones. First protoconch whorl diameter 0.75–0.92 mm (mean 0.82, n= 5). The younger specimens of this morph are somewhat similar in colouration to A. aureomarginata and were erroneously identified as such by Kilburn & Bouchet (1988). Depth range 390– 750 m.

Northern New Caledonia morph (“ A. hilgendorfi richeri ”) Figs 2 (as nNC), 5G–K

Material examined

Sequenced material

15 sequenced specimens ( Table 1).

Not sequenced material

Material listed by Kilburn & Bouchet (1988).

Remarks

Shell large (SL up to 76 mm), somewhat similar to the morph from the Coral Sea, although adult shells are more slender and the callused carina is less developed. Upper anterior band with more defined, relatively narrow, median carina. Plication plate uniformly white. Smaller specimens are more ovoid in shape, with relatively more pronounced carina and uniformly convex upper anterior band; the upper part of plication plate can be yellowish. Upper whorls often have a purplish tint. Number of columellar ridges variable, 2 to 6, regardless of specimen size. First protoconch whorl diameter 0.80–0.84 mm (mean 0.83, n=5). Depth range 360– 750 m.

Southern New Caledonia morph (“ pupiform ”)

Figs 2 (as sNC), 6, 7F

Material examined

Sequenced material

26 sequenced specimens (all MNHN) ( Table 1).

Not sequenced material

SOUTHERN NEW CALEDONIA • Material listed by Kilburn & Bouchet (1988) • 1 dd; Île des Pins; 22°48′ S, 167°15′ E; 440–470 m deep; TERRASSES; stn CP3115 • 1 dd; SW of Île des Pins; 22°54′ S, 167°17′ E; 496–505 m deep; KANACONO; stn DW4722 • 2 dd; W of Île des Pins; 22°50′ S, 167°16′ S; 480–505 m deep; VAUBAN 1978–1979; stn DR23 • 5 lv, 1 dd, S of Île des Pins; 22°53′ S, 167°17′ E; 570–610 m deep; BIOCAL; stn DW 46 • 1 dd; S of Grande Terre; 22°56′ S, 167°17′ E; 485–520 m deep; MUSORSTOM 4; stn CP215 • 1 dd; S of Grande Terre; 22°56′ S, 167°17′ E; 485–520 m deep; MUSORSTOM 4; stn DW223 • 2 worn dd; 22°51′ S, 167°13′ E; 445–460 m deep; MUSORSTOM 4; stn DW229 • 2 dd; S of Île des Pins; 22°52′ S, 167°13′ E; 415 m deep; SMIB 1; stn DW02 • 7 dd; S of Île des Pins; 22°55′ S, 167°16′ E; 490–495 m deep; SMIB 2; stn DW10 • 1 dd; Banc Éponge; 24°54′ S, 168°22′ E; 530 m deep; SMIB 3; stn CP04; • 1 worn dd; Kaimon Maru Bank; 24°45′ S, 168°08′ E; 233 m deep; SMIB 3; stn DW08 • 1 lv; SW of Île des Pins; 22°59′ S, 167°19′ E; 525 m deep; SMIB 3; stn DW21 • 1 lv, 1 dd; SW of Île des Pins; 23°03′ S, 167°19′ E; 503 m deep; SMIB 3; stn DW22.

Remarks

A very peculiar morph with medium-sized shell (SL up to 53.7 mm, usually less than 35 mm), occurring only in southern New Caledonia, mostly off Île des Pins, with a few specimens collected on Norfolk Ridge. Despite morphological similarity between specimens, these are genetically heterogeneous, belonging to different highly divergent assemblagies of haplotypes (marked by yellow in Fig. 3 ), some being closer to specimens from northern New Caledonia and the Coral Sea, while others constituting a subclade on the tree ( Fig. 2 ). In total eight haplotypes were identified within this morph.

Shell shape pupiform due to very strong development of primary and secondary calluses on upper teleoconch whorls, while uppermost 2.5–3 whorls (including those of protoconch) remain uncovered, revealing the papillate apex. Except the large development of the callus, the shell shape is rather similar to those in the north New Caledonia morph and some specimens with less developed callus (e.g., MNHN IM-2013-69558 or MNHN IM-2007-43673 on Fig. 6C ) are practically indistinguishable (e.g., MNHN IM-2009-11918, Fig. 5I ). Columellar ridges rather distinct, 6–7. Upper anterior band usually evenly convex, not subdivided by a ridge. First protoconch whorl diameter 0.84–0.90 mm (mean 0.86, n= 5). Depth range 233– 610 m.

On Norfolk Ridge and off southern New Caledonia, some specimens very similar to those from north of New Caledonia were found in deeper water in 560–650 m in addition to the pupiform morph. One specimen was collected on Banc Eponge ( Fig. 6I ) in a haul with a very large depth range, 564–1144 m, but the deepest record needs confirmation. Although none of these specimens were sequenced, there is no doubt of their identity.

Figures

Fig. 2. Molecular phylogeny of Amalda hilgendorfi (von Martens, 1897) produced by a Bayesian analysis of the Cox1 gene dataset. Outgroups and other species of Amalda have been removed from the tree. Only posterior probabilities ± 90% are shown. The unit for the scale is “substitutions/site”. The geographical distribution and morphological morphs are coded for each specimen: Phil =Philippines; Sol =Solomon Islands; PNG= Papua New Guinea; sNC = South New Caledonia; nNC = North New Caledonia; CS=Coral Sea. Numbers in parentheses at the tips of the tree link the MNHN IM voucher number to the corresponding photo on the right.

Fig. 3. Median-joining haplotype network based on Cox1 sequences of Amalda hilgendorfi (von Martens, 1897). Circles are colour coded by general location reported on the map and sized according to each haplotype’s relative abundance. Lengths of the lines connecting haplotype circles are proportional to the number of nucleotide differences among haplotypes. Green rectangle and oval encircle assemblages of haplotypes from New Caledonia (each including a specimen from Papua New Guinea).

Fig. 4. Amalda hilgendorfi (von Martens, 1897). A–D. Typical morph, Japan. A–C. MNHN IM-2019- 616, SL 53.1 mm. D. MNHN IM-2019-621, SL 50.0 mm. E–G. Philippine morph. E. MNHN IM-2007- 31950, SL 38.7 mm. F–G. MNHN IM-2007-33427, SL 40.3 mm. H–L. Solomon Islands and Papua New Guinea (PNG) morph. H. Solomons, MNHN IM-2007-33286, SL 52.6 mm. I. PNG, MNHN IM-2013- 44995, SL 51.3 mm. J. Solomons, MNHN IM-2009-11961, SL 32.9 mm. K. PNG, MNHN IM-2009- 22244, SL 63.1 mm. L. PNG, MNHN IM-2009-23330, SL 69.3 mm. M. Amalda tankervillii (Swainson, 1825), Venezuela, Isla de Margarita, 30–35 m, collection of Ron Voskuil, RV 0175, SL 80 mm. Photo by Ron Voskuil et al. (2011) (http://olivirv.myspecies.info/en/taxon-pages/ancillaria-tankervillii). Shells (except M, reduced) at the same scale.

Fig. 5. Amalda hilgendorfi (von Martens, 1897). A–F. Coral Sea morph. A-B. MNHN IM-2007- 33313, SL 66 mm. C. MNHN IM-2007-33289, SL 51.3 mm. D. MNHN IM-2007-33288, SL 60.3 mm. E. MNHN IM-2013-63901, SL 27-3 mm. F. MNHN IM-2007-33312, SL 25.9 mm. G–K. Northern New Caledonia morph = A. hilgendorfi richeri Kilburn & Bouchet, 1988. G. Holotype, MNHN IM-2000- 1378, SL 66.9 mm. H. MNHN IM-2009-11916, SL 65 mm. I. MNHN IM-2009-11918, SL 43.2 mm. J. MNHN IM-2007-42675, SL 48.7 mm. K. MNHN IM-2009-11966, SL 29 mm. Shells at the same scale.

Fig. 6. Amalda hilgendorfi (von Martens, 1897). Southern New Caledonia morph. A–D and E–H belong to two molecularly distinct subclades. A–B. MNHN IM-2007-43664, SL 30.6 mm. C. MNHN IM- 2007-43673, SL 34.2 mm. D. MNHN IM-2009-11964, SL 15.2 mm. E–F. MNHN IM-2007-43671, SL 33.8 mm. G. MNHN IM-2007-43674, SL 34.7 mm. H. MNHN IM-2009-11945, SL 31.6 mm. I. Norfolk Ridge, Banc Éponge, NORFOLK 1, stn DW 1693, 24°55′ S, 168°21′ E, 564–1144 m, SL 61 mm, specimen not sequenced, shell not to scale. Shells (except I, reduced) at the same scale.

Fig. 7. Radulae of species of Amalda H. Adams & A. Adams, 1853. A–G. A. hilgendorfi (von Martens, 1897). A–B. MNHN IM-2019-621 (shell on Fig. 4D). C. MNHN IM-2009-11961 (shell on Fig. 4J). D. MNHN IM-2013-58045, Papua New Guinea. E. MNHN IM-2013-19909, Papua New Guinea. F. MNHN IM-2013-63430, southern New Caledonia. G. MNHN IM-2007-33312 (shell on Fig. 5F). H. A. aureomarginata Kilburn & Bouchet, 1988, MNHN IM-2013-63421, specimen not sequenced, southern New Caledonia. I–J. A. miriky sp. nov. I. Miriky, stn CP3210, specimen not sequenced, Madagascar. J. Miriky, stn DW3215 (shell on Fig. 10J). K–L. A. cacao sp. nov., holotype, MNHN IM- 2000-35296 (shell on Fig. 11A–E).

Fig. 13. Radulae of species of Amalda H. Adams & A. Adams, 1853. A–C. A. montrouzieri (Souverbie, 1860). A–B. Île Ouen – Baie du Prony, LAGON, stn DW239, 22°24.3′ S, 166°57.8′ E, 42–43 m, SL 20.2 mm. C. Grand Récif Sud, LAGON, stn DW544, 22°50.8′ S, 166°48.5′ E, 25 m, SL 25.4 mm (shell on Fig. 12I). D–E. A. alabaster sp. nov. D. Holotype, MNHN IM-2007-43627, SL 26.7 mm (shell on Fig. 15A–B). E. MNHN IM-2007-43636, SL 17.6 mm. F. A. cf. alabaster, MNHN IM-2013-63897, SL 18.1 mm (shell on Fig. 15H–I). G. A. allaryi Bozzetti, 2007, MNHN IM-2013- 68272 (shell on Fig. 17A). H. A. coriolis Kilburn & Bouchet, 1988, MNHN IM-2013-63899 (shell on Fig. 18H–I).