The Shell Structure of the Recent Patellogastropoda (Mollusca: Gastropoda)

Home , Acmaea, Acmaea mitra, Acmaeidae, Archaeogastropoda, Bathyacmaea, Cellana

Paleontological Research, vol. 9, no. 2, pp. 143–168, June 30, 2005 6 by the Palaeontological Society of Japan

The shell structure of the Recent Patellogastropoda (Mollusca: Gastropoda)

TAKESHI FUCHIGAMI1 AND TAKENORI SASAKI2

1Department of Earth and Planetary Sciences, Faculty of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033 2The University Museum, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033 ([email protected])

Received March 25, 2005; Revised manuscript accepted March 28, 2005

Abstract. The shell microstructure of 44 species belonging to 19 genera and 5 families of Patellogas- tropoda was observed by scanning electron microscopy on the basis of material mainly from the Northwest Pacific. As a result, 17 microstructures of prismatic, crossed, and lamellar structures were recognized. The comparison among species revealed 20 shell structure groups which are defined by microstructures and shell layer arrangement. The relations between taxa and shell structural composition indicate that the Recent patellogastropods generally have distinctive and stable shell structures at the genus level. This high level of consistency provides a firm basis for the application of shell structural characters to identify fossil patellogastropods. However, the evolutionary process of microstructures and homology across different shell layers are mostly ambiguous in the absence of robust phylogeny and undoubted positional criteria for comparison. More studies from phylogenetic, ontogenetic and mineralogical viewpoints should be under- taken to discuss the process of shell structure diversification in patellogastropods.

Key words: Shell microstructure, new deﬁnition, taxonomic occurrence, Patellogastropoda, Recent

Introduction tropods using soft-part characters have repeatedly corroborated many cases in which macroscopic tele- Studies of shell microstructure are particularly im- oconch morphology is useless in determining higher portant because they provide information for the tax- systematic position (Haszprunar, 1988; Ponder and onomic and phylogenetic analysis of molluscs includ- Lindberg, 1997). Limpets, including patelliform gas- ing fossil taxa. Detailed comprehensive works have tropods and also monoplacophorans, are particularly been published for various shell-bearing molluscs, es- notorious as a case of multiple convergence. Several pecially bivalves (e.g., Taylor et al., 1969, 1973; Taylor, different major taxa are inferred to have evolved 1973; Carter, 1990a, b), gastropods (Carter and Hall, similar-looking limpet-form shells. Among them pa- 1990; Bandel, 1990a), and cephalopods (e.g., Bandel, tellogastropods are one of the outstanding groups 1990b; Kulicki, 1996). However, studies of shell struc- comprising limpet-shaped species exclusively. ture in gastropods are limited to a relatively small Patellogastropods share many apomorphic charac- number of specific taxonomic groups (e.g., Taylor and ters anatomically, and their monophyly is strongly Reid, 1990 for Littorinidae; Bandel and Geldmacher, supported (Ponder and Lindberg, 1997; Sasaki, 1998). 1996 for Patella; Sasaki, 2001 for Neritoidea; Kiel, Recent phylogenetic studies revealed that the patello- 2004 for gastropods from vents/seeps) and their taxo- gastropods constitute a well-defined independent clade nomic coverage is insufficient compared to other ma- (Eogastropoda), being clearly separated from the jor conchiferan molluscs. Therefore, the gastropod rest of the gastropods (Orthogastropoda) (Ponder shell structure is not well understood in general over- and Lindberg, 1997; Sasaki, 1998). When the shell view even at present. is perfectly intact, the patellogastropods can be dis- One of the difficulties in systematic investigations of tinguished from other gastropods by (1) a conical fossil gastropods is the low preservative potential of shell with an anteriorly positioned apex (except lep- soft parts. Meanwhile, gastropod higher taxa are de- etid Propilidiinae having a posteriorly situated apex: fined primarily by the anatomy of soft tissue in the Lindberg, 1998: 649), (2) a thick horseshoe-shaped Recent groups. Phylogenetic analyses on Recent gas- muscle scar of the shell muscle with constricted outline 144 Takeshi Fuchigami and Takenori Sasaki and a thin scar of the pallial retractor muscle, (3) a to a thickness of 400 A˚ . The three-dimensional shell symmetrically little coiled protoconch (Sasaki, 1998), microstructures were observed in their radial and and (4) a characteristic scar in the apex of the tele- commarginal sections and inner shell surface with oconch after the protoconch is detached (cf. Sasaki, scanning electron microscopes (SEM, HITACHI S- 1998: figure 21g, h). Unless these characters are ob- 2400S in Department of Earth and Planetary Science, servable, it is not possible to detect the systematic po- University of Tokyo and HITACHI S-4500 in Uni- sition of limpets in question based on shell morphol- versity Museum, University of Tokyo). All specimens ogy only. In such a case, the shell structure characters observed with SEM are registered and preserved in must be useful, if their original structures are well the Department of the Historical Geology and Pale- preserved. ontology, University Museum, University of Tokyo The systematization of patellogastropod shell (UMUT) (Table 1). structure was first established by MacClintock (1967). The descriptive terminology used in this study basi- He investigated shell structures of 120 Recent and cally follows MacClintock (1967) and Carter et al. fossil patellogastropod species by optical microscopy (1990). The shell layers are divided into outer and in- and proposed 9 microstructures and 17 shell structure ner layers by a myostracum which corresponds to the groups. He also clarified a high degree of consistency insertion of muscles on the shell. The position of each between taxonomic categories and shell structure shell layer is indicated by its arrangement relative to groups. Lindberg (1988a) further generalized the sig- the myostracum (abbreviated as M). In this nomen- nificance of shell structural characters in patellogas- clature outer shell layers are described as Mþ1, Mþ2, tropod systematics, and this methodology has been Mþ3, etc. from the inner to the outer side, and like- broadly applied to the identification of fossil patello- wise inner layers as M1, M2, M3, etc. from the gastropods by Lindberg and Hickman (1986), Lind- outer to the inner side. Each layer reclines at small berg (1988a, b), Lindberg and Marincovich (1988), angles with the inner surface, and its distribution is Lindberg and Squires (1990), Kase (1994), Kase visible as a concentric ring in ventral view (Figure 1). and Shigeta (1996), Lindberg and Hedegaard (1996), Some layers with identical microstructure were de- and Hedegaard et al. (1997). However, the existing scribed separately as ‘‘concentric’’ or ‘‘radial’’ layers knowledge on patellogastropod shell structure still under the criterion of its first-order unit arrangement. largely depends on the descriptions of MacClintock To avoid confusion, the four terms regarding ‘‘shell (1967) at the level of optical microscopy, although structure’’ were used in the following sense in this recent standards in studies on calcified hard tissue study. (1) Microstructure – The morphology of crystal essentially require SEM-level information. Hence, units and their mode of aggregation. (2) Shell layer – the reinvestigation of patellogastropod shell struc- A sheet-like component consisting of single micro- ture at finer resolution has been an unquestionable structure. (3) Shell structure – The total composition of primary subject in the studies of molluscan shell mi- microstructures and shell layers constituting the shell. crostructure. In this study, we attempted to provide (4) Shell structure group – The group of species having detailed SEM-level descriptions to advance the the identical order of shell layer arrangement and knowledge on patellogastropod shell structure. microstructure. In the descriptions the dip angle indicates the angle between growth axis of crystal units and inner shell surface, unless otherwise mentioned. Materials and methods The identification of crystal forms of calcium car- bonate (aragonite or calcite) using X-ray diffraction The materials used in this study include 44 species was not carried out in this study. Feigl stain (see Car- belongingto19generaof5families.Theywerecol- ter and Ambrose, 1989 for details), which can distin- lected alive mainly around Japan and some non- guish aragonite from calcite by staining in black, was Japanese species, especially type species of several preliminarily tested for some species but generally this genera, were also included for comparison (Table 1). method yielded poor results. Most shallow-water spe- Immediately after capture, the soft parts were re- cies are originally pigmented a dark color on their moved from the shell. The shell of each species was inner surfaces, and such a dark background color broken in approximately radial or transverse direc- hindered a clear identification of a series of tightly tion, and pieces of shell fragments were treated with stratified thin shell layers. Therefore, determination of bleach for 24 hours and etched with 3% acetic acid crystal forms for each microstructure of the respective for three seconds. After cleaning with an ultrasonic species is a subject for future study and was not re- cleaner, they were coated with platinum – palladium solved in this study. Shell structure of Patellogastropoda 145

Table 1. Material examined in this study

Species Locality Register Number Lottiidae Niveotectura pallida (Gould) Shiofukiiwa, Miyako, Iwate, Japan RM28482, 28483 Niveotectura pallida (Gould) Benten, Matsumae, Hokkaido, Japan RM28484 Yayoiacmea oyamai (Habe) Banda, Tateyama, Chiba, Japan RM28485–28488 Patelloida saccharina lanx (Reeve) Mitsuishi, Manazuru, Kanagawa, Japan RM28489–28492 Patelloida pygmaea (Dunker) Araihama, Misaki, Kanagawa, Japan RM28493 Patelloida pygmaea (Dunker) Makurazaki, Kagoshima, Japan RM28494 Lottia gigantea Sowerby California, USA RM28495–28496 Lottia cassis (Eschscholtz) Nemuro, Hokkaido, Japan RM28497–28500 Lottia sp. cf. borealis (Lindberg) Nemuro, Hokkaido, Japan RM28501–28504 Lottia dorsuosa (Gould) Araihama, Misaki, Kanagawa, Japan RM28505–28506 Lottia dorsuosa (Gould) Mitsuishi, Manazuru, Kanagawa, Japan RM28507 Lottia langfordi (Habe) Mitsuishi, Manazuru, Kanagawa, Japan RM28508–28510 Lottia kogamogai Sasaki & Okutani Mitsuishi, Manazuru, Kanagawa, Japan RM28511–28512 Lottia tenuisculpta Sasaki & Okutani Mitsuishi, Manazuru, Kanagawa, Japan RM28513–28514 Lottia lindbergi Sasaki & Okutani Nagahama, Kanagawa, Japan RM28515 Lottia lindbergi Sasaki & Okutani Araihama, Misaki, Kanagawa, Japan RM28516 Nipponacmea schrenckii (Lischke) Mitsuishi, Manazuru, Kanagawa, Japan RM28517–28520 Nipponacmea gloriosa (Habe) Mitsuishi, Manazuru, Kanagawa, Japan RM28521–28524 Nipponacmea boninensis (Asakura & Nishihama) Chichijima Island, Ogasawara Islands, Japan RM28525–28526 Nipponacmea concinna (Lischke) Mitsuishi, Manazuru, Kanagawa, Japan RM28527–28529 Nipponacmea fuscoviridis (Teramachi) Mitsuishi, Manazuru, Kanagawa, Japan RM28530–28532 Nipponacmea radula (Kira) Goto Islands, Nagasaki, Japan RM28533 Nipponacmea radula (Kira) Kuwabara, Tokuyama, Yamaguchi, Japan RM28534–28535 Nipponacmea nigrans (Kira) Mitsuishi, Manazuru, Kanagawa, Japan RM28536 Nipponacmea teramachii (Kira) Mitsuishi, Manazuru, Kanagawa, Japan RM28537 Nipponacmea habei Sasaki & Okutani Nojima, Otsuchi, Iwate, Japan RM28538–28540 Tectura emydia (Dall) Akkeshi, Hokkaido, Japan RM28541–28542 Tectura emydia (Dall) Nemuro, Hokkaido, Japan RM28543 Tectura virginea (Mu¨ ller) Algeciras, South Spain RM28544 Tectura virginea (Mu¨ ller) Off Roscoff, France RM28545 Atalacmea fragilis (Sowerby) Lyle Bay, Wellington, New Zealand RM28546 Atalacmea fragilis (Sowerby) Evans Bay, Wellington, New Zealand RM28547–28548 ‘‘Lottia’’ scabra (Gould) California, USA RM28549–28551 Discurria insessa (Hinds) California, USA RM28552–28553 Patellidae Patella vulgata Linnaeus Ile d’Oleron, Charente Maritime, France RM28554–28557 Scutellastra flexuosa (Quoy & Gaimard) Makurazaki, Kagoshima, Japan RM28558 Scutellastra flexuosa (Quoy & Gaimard) Banda, Tateyama, Chiba, Japan RM28559–28561 Scutellastra optima (Pilsbry) Yokoatejima Island, Amami Islands, Japan RM28562–28565 Nacellidae Nacella deaurata (Gmelin) Fuego Island, Argentina RM28566–28568 Cellana toreuma (Reeve) Makurazaki, Kagoshima, Japan RM28569–28570 Cellana enneagona (Reeve) Chichijima Island, Ogasawara Islands, Japan RM28571–28572 Cellana nigrolineata (Reeve) Araihama, Misaki, Kanagawa, Japan RM28573–28576 Cellana testudinaria (Linnaeus) Iriomote Island, Okinawa, Japan RM28577–28578 Cellana grata (Gould) Araihama, Misaki, Kanagawa, Japan RM28579–28580 Cellana mazatlandica (Sowerby) Ogasawara Islands, Japan RM28581–28582 Lepetidae Lepeta caeca pacifica Moskalev Daikokujima Islet, Akkeshi, Hokkaido, Japan RM28583–28584 Cryptobranchia kuragiensis (Yokoyama) Suehirocho, Wakkanai, Hokkaido, Japan RM28585 Cryptobranchia kuragiensis (Yokoyama) Asamushi, Aomori, Japan RM28586 Limalepeta lima (Dall,1918) OffKushiro,Hokkaido,Japan,50–100mdeep RM28587–28590 Sagamilepeta sagamiensis (Kuroda & Habe) Off Hota, Chiba, Japan, ‘‘200–300’’ m deep RM28591 Sagamilepeta sagamiensis (Kuroda & Habe) Off Kanaya, Chiba, Japan, 160–180 m deep RM28592–28593 Acmaeidae Acmaea mitra (Rathke) California, USA RM28594 Pectinodonta rhyssa Dall Kii Channel, Japan RM28595–28596 Pectinodonta orientalis Schepman Tosa Basin, Japan, 1034–1036 m deep RM28597–28600 Bathyacmea secunda Okutani, Fujikura & Sasaki Izena Hole, Okinawa Trough, 1340 m deep RM28601–28603 146 Takeshi Fuchigami and Takenori Sasaki

Definition.—First-order prisms ornamented with sharp-edged straight keels parallel to their growth axis, elongated in the radial direction; width of prism almost constant with growth. Second-order units arranged parallel to the first-order units, triangular or blade-shaped in cross-section, visible as aggregations of triangular lines on inner shell surface. Dip angle.—Roughly perpendicular in first-order units. Size.—5–20 mm wide in first-order units. Taxonomic and layer distribution.—Outermost layer of Cellana (Figure 2). Remarks.—Complex prismatic structure (cp) in Groups 12 and 13 of MacClintock (1967) corresponds to SP-A. According to MacClintock (1967: p. 15), ‘‘cp’’ was defined as ‘‘regularly or irregularly shaped first-order prisms which, in turn, contain parallel or fan-shaped aggregates of fibrils or second-order prisms.’’ Prisms that contain parallel aggregates of fi- Figure 1. Descriptive terminology of shell layers. Layer brils may be compared to this structure or irregular distribution is shown in sagittal section (left) and on inner surface (right). spherulitic structure type-B (ISP-B) (described below). Although he mentioned differences in ‘‘cp’’ of groups 12 and 13 (MacClintock, 1967: 57–83), it was Descriptions treated as a single structure. However, because there are discretely distinguishable differences under SEM, SEM-level observations on 44 species in this study SP-A and ISP-B were separated in this study. Hede- revealed 17 microstructures of prismatic, laminar and gaard et al. (1997) and Lindberg (1998) treated com- crossed structures (Figure 2). Their morphological plex (cp) and simple (sp) prismatic structures of Mac- definition and taxonomic and layer distribution are Clintock (1967) as calcitic homogeneous structure, but described below for each microstructure. these layers consist of prismatic crystal units. Prismatic structure Simple prismatic structure type-B (SP-B)

Definition.—‘‘Mutually parallel, elongate, adjacent (Figures 3E–F, 8B, 17B) structural units that do not interdigitate strongly along Definition.—Single prism of first-order units smooth their mutual boundaries’’ (Carter, 1990c). without ornamentation, hexangular in cross section, Taxonomic and layer distribution.—Outer layers slightly curved, reclined against inner surface, elon- of most taxa of Lottiidae, Nacellidae and Acmaeidae gated in radial direction; width of prism almost (Figure 2). constant with growth. Second-order units fibrous, ar- Remarks.—Many kinds of prismatic structures have ranged oblique to the axis of the first-order units. been proposed in molluscan shell. They are generally Dip angle.—Ca. 60 degrees in first-order, roughly categorized into simple prismatic structure, fibrous perpendicular (30 degrees to growth axis) in second- prismatic structure, composite prismatic structure and order units. spherulitic prismatic structure (Carter, 1990c). In Size.—10–60 mm wide in first-order units, 0.5 mmin Patellogastropoda, a variety of prismatic structures diameter in second-order units. have been described under the names of simple pris- Taxonomic and layer distribution.—Mþ2 layer of matic structure, spherulitic prismatic structure, fibrous Tectura virginea (Figure 2). prismatic structure, etc. (MacClintock, 1967; Lind- Remarks.—This structure has never been reported berg, 1998; Carter, 1990c, etc.). They were classified in patellogastropods in detail. MacClintock (1967) de- and redefined as follows. scribed this structure as ‘‘fibrillar prismatic (fp)’’ in Mþ2orMþ3 layer of some lottiid limpets. Fibrous- Simple prismatic structure type-A (SP-A) like structures in T. virginea and other lottiids, how- (Figures 3A–D, 8A, 17A) ever, can be clearly separated by second-order mor- Shell structure of Patellogastropoda 147

Figure 2. Layer distribution of microstructures in the species examined in this study. The type species of genera are denoted by as- terisks. Bar (-) indicates the absence of shell layer. Abbreviations: CCCL, cone complex crossed lamellar structure; CP-ISP, prismatic structure with minor irregular spherulitic prismatic structure; FP-ISP, fibrous prismatic structure with minor irregular spherulitic prismatic structure; ICCF, irregular complex crossed foliated structure; ICCL, irregular complex crossed lamellar structure; ICF, irregular crossed foliated structure; IFF, irregular fibrous foliated structure; ISP-A, irregular spherulitic prismatic structure type-A; ISP-B, irregular spherulitic prismatic structure type-B; NCP, Niveotectura-type composite prismatic structure; RFF, regular fibrous foliated structure; SF, semi- foliated structure; SP-A, simple prismatic structure type-A; SP-B, simple prismatic structure type-B; cCF, concentric crossed foliated structure; cCL, concentric crossed lamellar structure; cRF, concentric regularly foliated structure; rCF, radial crossed foliated structure; rCL, radial crossed lamellar structure. phology. Thus, MacClintock’s ‘‘fibrillar prismatic’’ is Fibrous prismatic structure with minor irregular divided into SP-B, fibrous prismatic structure with spherulitic prismatic structure (FP-ISP) minor irregular spherulitic prismatic structure (FP- (Figures 4A–D, 8C) ISP) and composite prismatic structure with minor irregular spherulitic prismatic structure (CP-ISP) (de- Definition.—First-order prisms fibrous, much longer scribed blow). than wide, widened and branched mainly near their 148 Takeshi Fuchigami and Takenori Sasaki

Figure 3. Scanning electron micrographs of prismatic structures (1). A–D. Simple prismatic structure type-A (SP-A). A. Oblique view of radial section. The left top of the figure is the apical side of the shell. B. Cross section of first-order unit. C–D. Ventral view on inner shell surface. E–F. Simple prismatic structure type-B (SP-B). E. Radial section. F. Dorsal view of hexagonal cross section of first- order prisms. A, C. Cellana toreuma (A. UMUT RM28569; C. UMUT RM28570). B. Cellana enneagona (UMUT RM28571). D. Cellana nigrolineata (UMUT RM28573). E–F. Tectura virginea (UMUT RM28545). origin, keeping their width almost constant along their Dip angle.—80 degrees. length; surfaces of well-matured prisms ornamented Size.—1–2 mmwide. with oblique lines, but immature ones smooth; growth Taxonomic and layer distribution.—Yayoiacmea axes of these fibrils slightly curved, arranged in radial oyamai (Mþ2 layer) (Figure 2). direction; cross sections irregular. Unlike simple pris- Remarks.—This layer is similar to composite matic structures, second-order units absent. prismatic structure with minor irregular spherulitic Shell structure of Patellogastropoda 149

Figure 4. Scanning electron micrographs of prismatic structures (2). A–D. Fibrous prismatic structure with minor irregular spherulitic prismatic structure (FP-ISP). A. Radial section exhibiting oblique sculpture on prisms. The left top of the figure shows apical side of the shell. B. Commarginal section near shell margin. C. Enlarged view of Figure 4B, D. Oblique view of cross section near shell margin. A– D. Yayoiacmea oyamai (A. UMUT RM28485; B–C. UMUT RM28486; D. UMUT28488). prismatic structure (CP-ISP) (see below). However, Remarks.—‘‘Simple prismatic structure’’ of Mac- prisms of FP-ISP are narrower, dip at larger degrees, Clintock (1967) in Discurria, Nacella, Acmaea and branch more frequently, and their surface has differ- Cryptobranchia should be identified as irregular ent ornamentation. spherulitic prismatic structure because second-order units are diverging from their origin. Irregular spherulitic prismatic structure type-A (ISP-A) Irregular spherulitic prismatic structure type-B (ISP-B) (Figures 5A–D, 8D, 17C) (Figures 5E–F, 9A, 17D) Definition.—First-order prisms slightly curved, oriented in the radial direction, demarcated with Definition.—First-order units slightly curved, vari- somewhat obscure boundaries, widened with crystal able from pillow-like to fan-shaped in cross section, growth, composed of very small blade-shaped second- ornamented with longitudinal creases, oriented in the order units arranged in a radiating form. radial direction, gradually increasing their width at Dip angle.—Roughly perpendicular (ca. 80 degrees initial growth stage, later maintaining nearly constant with layer boundary) in first-order units. width toward growth surface. Second-order units fi- Size.—5 mm in diameter in first-order units, 0.2 mm brous, diverse from axis of first-order units. wide in second-order units. Dip angle.—60–80 degrees in first-order units. Taxonomic and layer distribution.—Outermost Size.—5–20 mm wide in first-order units, 0.5 mmin layer of most species of Lottiinae, Nacella, Crypto- diameter in second-order units. branchia and Acmaeidae (Figure 2). Taxonomic and layer distribution.—Mþ2layerof 150 Takeshi Fuchigami and Takenori Sasaki

Figure 5. Scanning electron micrographs of prismatic structures (3). A–D. Irregular spherulitic prismatic structure type-A (ISP-A). A. Radial section. Left top of the ﬁgure is apical side of the shell. B. Commarginal section near shell margin. C. Commarginal section seen obliquely from ventral side. D. First-order units on growing surface. E–F. Irregular spherulitic prismatic structure type-B (ISP-B). E. Commarginal section. F. Ventral view on inner shell surface. The right side of the ﬁgure shows the shell margin. A–B. Nipponacmea gloriosa (A. UMUT RM28524; B. UMUT RM28523). C. Lottia dorsuosa (UMUT RM28506). D. Nipponacmea schrenckii (UMUT RM28520). E. Patelloida saccharina lanx (UMUT RM28492). F. Patelloida pygmaea (UMUT RM28494).

Patelloida (Figure 2). matic structure with minor irregular spherulitic pris- Remarks.—Complex prismatic structure (cp) in matic structure (CP-ISP) in the presence of creases on Group 2 of MacClintock (1967) is redeﬁned as ISP-B, the surface of prisms. But the ﬁrst-order units are since second-order units are diverging from their ori- much larger and the second-order units are more gin. This microstructure resembles composite pris- clearly visible in this microstructure. Shell structure of Patellogastropoda 151

Figure 6. Scanning electron micrographs of prismatic structures (4). A–F. Composite prismatic structure with minor irregular spherulitic prismatic structure (CP-ISP). A–D. Commarginal section. Bottoms of ﬁgures show ventral sides of the shells. Arrows indicate the direction of crystal growth. E. Commarginal sections seen slightly from ventral side. F. Ventral view on inner shell surface. A, D. Lottia sp. cf. borealis (A. UMUT RM28503; D. UMUT RM28501). B. Nipponacmea habei (UMUT RM28539). C. Nipponacmea concinna (UMUT RM28527). E. Nipponacmea gloriosa (UMUT RM28522). F. Nipponacmea nigrans (UMUT RM28536).

Composite prismatic structure with minor irregular widened and branched only near their origin, keeping spherulitic prismatic structure (CP-ISP) their width almost constant along their length; growth axes of these fibrils straight in radial direction; their (Figures 6A–F, 9B, 17E) cross sections diamond- to ginkgo-leaf-shaped. Sec- Definition.—First-order prisms fibrous, ornamented ond-order units absent unlike simple prismatic struc- with divaricating creases, much longer than wide, tures. 152 Takeshi Fuchigami and Takenori Sasaki

Figure 7. Scanning electron micrographs of prismatic structures (5). A–D. Niveotectura-type composite prismatic structure (NCP). A–B. Commarginal section. C. Radial section. This structure resembles concentric crossed lamellar structure (cCL) in radial section. D. Ventral view on inner shell surface. A–D. Niveotectura pallida (A. UMUT RM28483; B. UMUT RM28484; C–D. UMUT RM28482)

Dip angle.—30–45 degrees in first-order units. entated in radial direction, appearing as parallel radial Size.—2–4 mm wide in first-order units. lines on the inner surface. Third-order units fibrous, Taxonomic and layer distribution.—Mþ2orMþ3 arranged in parallel. layer of most taxa of Lottiinae (Figure 2). Dip angle.—Vertical in first-order units, ca. 60 de- Remarks.—‘‘Fibrillar structure’’ of MacClintock grees in second-order units. (1967) was revealed to include simple prismatic struc- Size.—50–100 mm wide in first-order units, ca. 2 mm ture type-B (SP-B), fibrous prismatic structure with wide in third-order units. minor irregular spherulitic prismatic structure (FP- Taxonomic and layer distribution.—Mþ2 layer of ISP) and this structure (CP-ISP) in this study. Niveotectura pallida (Figure 2). Remarks.—This structure has never been described Niveotectura-type composite prismatic structure in detail. MacClintock (1967) identified this layer as (NCP) ‘‘fibrillar prismatic’’ and ‘‘simple prismatic’’ layers in Acmaea pallida (Niveotectura pallida in the current (Figures 7A–D, 9B, 17F) systematics). In radial section, this layer can be con- Definition.—First-order prisms of variable size, fused with concentric crossed lamellar structure (cCL) roughly rectangular, composed of a vertical stack of (Figure 7C), but the width of first-order units are divaricating platy second-order units; their growth variable unlike those of cCL. This microstructure is axes straight; boundaries with adjacent units inter- similar to ‘‘irregular crossed lamellar structure’’ of digitated in ventral view but not in vertical view; their Carter (1990c) in second-order unit morphology. width constant with growth. Second-order units ori- However, it should be grouped as prismatic structure, Shell structure of Patellogastropoda 153

Figure 8. Schematic illustrations of prismatic structures (1). A. Simple prismatic structure type-A (SP-A). B. Simple prismatic structure type-B (SP-B). C. Fibrous prismatic structure with minor irregular spherulitic prismatic structure (FP-ISP). D. Irregular spherulitic prismatic structure type-A (ISP-A). a. Inner surface. b. Commarginal vertical section. c. Radial section. d. Oblique three-dimensional view. White and gray arrows indicate the directions of crystal growth and accretionary shell growth, respectively.

because ﬁrst-order prisms are mutually parallel and and Acmaeidae, and a few species of Lottiidae (Figure have clear boundaries. 2).

Laminar structure Regularly foliated structure (RF)

(Figures 10A–D, 12A, 17G) Definition.—‘‘Rods, laths, blades or tablets com- prise sheets which are oriented parallel or nearly par- Definition.—First-order units uniformly thin and allel to the depositional surface’’ (Carter, 1990c). flat sheets formed at equal thickness; their growth Taxonomic and layer distribution.—Mainly outer front nearly straight, finely serrated; their surface layers, especially Mþ2 layer, of Nacellidae, Lepetidae almost smooth occasionally with faint striation. 154 Takeshi Fuchigami and Takenori Sasaki

Figure 9. Schematic illustrations of prismatic structures (2). A. Irregular spherulitic prismatic structure type-B (ISP-B). B. Compos- ite prismatic structure with minor irregular spherulitic prismatic structure (CP-ISP). C. Niveotectura-type composite prismatic structure (NCP). a. Inner surface. b. Commarginal vertical section. c. Radial section. d. Oblique three-dimensional view. White and gray arrows indicate the directions of crystal growth and accretionary shell growth, respectively.

Second-order units blade-like, extremely thin, mutu- 10B). Their arrangement is slightly variable individu- ally parallel. ally and not completely symmetrical relative to sagittal Dip angle.—Smaller than 10 degrees in first-order axis. units. Size.—0.5–1 mm thick in first-order units, 0.5 mm Semi-foliated structure (SF) wide in second-order units. (Figures 10E–H, 12B, 17H) Taxonomic and layer distribution.—Mþ1orMþ2 layer of Nacellidae and Acmaea mitra (Figure 2). Definition.—First-order units sheet-like, not com- Remarks.—The second-order blades grow composed of elongate blades but flakes defined by several marginally from posterior to anterior midline. (Figure growth fronts, sculptured by rough growth lines, waved Shell structure of Patellogastropoda 155 with irregular thickness; their boundaries roughly brous foliated structure (IFF) and irregular complex parallel, wavy in radial and commarginal sections; un- crossed foliated structure (ICCF). IFF was termed filled holes often visible on growing plane in ventral in connection with regular fibrous foliated structure view. Growth fronts of second-order units forming (RFF), because these structures have the identical angles of 45, 90 or 135 degrees. crystal units of 1–2 mmwide. Dip angle.—Roughly parallel in first-order units. Size.—1–2 mm thick in first-order units of most Crossed structure species, but 10–15 mmthickinBathyacmaea secunda. Taxonomic and layer distribution.—Mþ2 layer of Definition.—‘‘Microstructures showing two or more Lepetidae, and Mþ2orM1, Mþ1andMþ3layersof clearly non-horizontal dip directions of their elongate part of Acmaeidae (Figure 2). structural units relative to the depositional surface’’ Remarks.—MacClintock (1967) and Lindberg and (Carter, 1990c). Hedegaard (1996) treated this structure as foliated Taxonomic and layer distribution.—Various layers or regularly foliated structure, but it was clearly dis- of all species examined. tinguished from regularly foliated structure (RF) in Crossed lamellar structure (CL) thickness, surface sculpture and growth directions of second-order units. This structure resembles semi- (Figures 14A, 16A) foliated structure of Carter (1990c) reported in Definition.—Thick first-order lamella arranged oysters, brachiopods, bryozoans and corals. In Pa- in radial or commarginal directions. Second-order la- tellogastropoda, this structure is distributed only in mellae sheet-like, alternating at equal angle to growth subtidal and bathyal species. Its occurrence may be surfaces, but in opposite directions. Third-order la- related to deep environments. mellae arranged parallel to one another. Dip angle.—Roughly vertical in first-order units, Regular fibrous foliated structure (RFF) 20–40 degrees in second-order units. (Figures 11A–B, 12C, 17I) Size.—5–20 mm thick in first-order units, 0.5 mm wide in third-order units. Definition.—Blade-shaped units elongated in- Taxonomic and layer distribution.—Mainly M1 variably in radial direction with constant size; their and/or Mþ1 layers of all species examined except Na- surfaces smooth; cross sections roughly rectangular. cella deaurata (Figure 2). Dip angle.—20–30 degrees. Remarks.—This structure is very common in the Size.—1 mmwideand0.5mmthick. shells of patellogastropods. In the inner layers, this Taxonomic and layer distribution.—Mþ2 layer of structure often has pseudolayers that are insertions of Lottia langfordi (Figure 2). thin prismatic layers parallel to the inner surface (see Remarks.—This structure resembles lath-type fi- MacClintock, 1967; p. 52). This structure can often be brous prismatic structure of Carter (1990c). However, confused with cone complex crossed lamellar structure it should be included in laminar structure, because the (CCCL) in that some first-order lamellae are occa- morphology of the growing front of crystal units is of sionally wavy with variable thickness on the inner foliated type, and their dip angles are small. surface. However, adjacent first-order lamellae of CL do not interdigitate, unlike CCCL. Irregular fibrous foliated structure (IFF) Cone complex crossed lamellar structure (CCCL) (Figures 11C–D, 12D, 13) (Figures 14B–D, 16B 17J) Definition.—Blade-shaped units gradually changing their growth orientations from radial to commarginal Definition.—First-order lamellae irregularly colum- on outer to inner side, or from margin to center in nar, vertically oriented, strongly interdigitating along ventral view, keeping equal size with growth; their lateral boundary, appearing as radial circles in ventral surfaces smooth. view. Second-order lamella cone-like or conical spiral Dip angle.—Very small. structure; apical angle of cone ranging from 30 to 45 Size.—0.5–2 mmthick. degrees. Third-order lamellae spicular plates radiating Taxonomic and layer distribution.—Mþ2 layers of from cone apex. ‘‘Lottia’’ scabra (Figure 2). Dip angle.—Generally vertical in first-order units. Remarks.—Modified foliated structure (mf) of Size.—80–100 mm in diameter in first-order units, MacClintock (1967) was recognized as irregular fi- 1 mm thick in second-order units. 156 Takeshi Fuchigami and Takenori Sasaki Shell structure of Patellogastropoda 157

Figure 11. Scanning electron micrographs of laminar structures (2). A–B. Regular ﬁbrous foliated structure (RFF). A. Inner shell surface. B. Commarginal section. C–D. Irregular ﬁbrous foliated structure (IFF). Inner shell surface. A. Lottia langfordi (UMUT RM28508). B–D. ‘‘Lottia’’ scabra (UMUT RM28550).

Taxonomic and layer distribution.—M2 layer of arranged irregularly, appearing as non-parallel lines Cellana mazatlandica (Figure 2). on any vertical section. Second-order units parallel- Remarks.—Following Carter (1990c), complex arranged lamellae; ones in adjacent first-order units crossed lamellar structure of MacClintock (1967) was having different growth directions. Third-order la- renamed cone complex crossed lamellar structure mellae thin, arranged in parallel. (CCCL). Dip angle.—Over 45 degrees in second-order units. Size.—0.5 mm thick and 5–10 mm wide in second- order units, ca. 1 mm wide in third-order units. Irregular complex crossed lamellar structure (ICCL) Taxonomic and layer distribution.—Outermost (Figures 14E–H, 16C, 17K) layer of Lepetidae excluding Cryptobranchia (Figure 2). Definition.—As in irregular complex crossed foli- Remarks.—This structure was newly described in ated structure (ICCF), patches of first-order units Patellogastropoda.

U Figure 10. Scanning electron micrographs of laminar structures (1). A–D. Regularly foliated structure (RF). A. Vertical section. B– D. Inner shell surface. B. Folia facing from left and right sides near anterior midline of the shell. Arrows indicate the direction of crystal growth. C–D. Enlarged view of serrated growing edge of folia. E–H. Semi-foliated structure (SF). E–F. Vertical section. G–H. Inner shell surface with rough growth lines and polygonal growth fronts. A. Cellana testudinaria (UMUT RM28578). B. Cellana nigrolineata (UMUT RM28573). C. Cellana toreuma (UMUT RM28570). D. Acmaea mitra (UMUT RM28594). E. Lepeta caeca paciﬁca (UMUT RM28583). F. Pectinodonta orientalis (UMUT RM28597). G. Limalepeta lima (RM28588). H. Bathyacmaea secunda (UMUT RM28601). 158 Takeshi Fuchigami and Takenori Sasaki

Figure 12. Schematic illustrations of laminar structures. A. Regularly foliated structure (RF). B. Semi-foliated structure (SF). C. Regular ﬁbrous foliated structure (RFF). D. Irregular ﬁbrous foliated structure (IFF). a. Inner surface. b. Commarginal vertical section. c. Radial section. d. Oblique three-dimensional view. White and gray arrows indicate the directions of crystal growth and accretionary shell growth, respectively.

V Figure 14. Scanning electron micrographs of crossed structures (1). A. Crossed lamellar structure (CL). Vertical cross section perpendicular to first-order lamellae. B–D. Cone complex crossed lamellar structure (CCCL). B. Oblique section. C. Inner shell surface with part of cone-like second-order lamellae re- moved. D. Intact inner shell surface with third-order lamellae radiated in a concentric form. E–H. Irregular complex crossed Figure 13. Diagram showing the distribution of irregular lamellar structure (ICCL). E. Vertical section. F–H. Inner shell fibrous foliated structure (IFF). White arrows indicate the surface showing patchy arrangement of crystal aggregation. A. growth directions of crystal units. A. Three-dimensional view in Patelloida saccharina lanx (UMUT RM28489). B–D. Cellana the whole shell. Shell layers except for IFF layer are omitted. B. mazatlandica (UMUT28582). E, F, H. Lepeta caeca pacifica (E. The shift in growth directions of crystal units from outer to inner UMUT RM28583; F, H. UMUT RM28584). G. Sagamilepeta sa- side. Their change is actually gradual. gamiensis (RM 28591). Shell structure of Patellogastropoda 159 160 Takeshi Fuchigami and Takenori Sasaki

Figure 15. Scanning electron micrographs of crossed structures (2). A–B. Crossed foliated structure (CF). Inner shell surface. A. Three adjacent ﬁrst-order units. Arrows indicate alternating direction of crystal growth. B. Enlarged view of second-order units arranged in the same direction. C–D. Irregular crossed foliated structure (ICF). C. Radial section and inner surface. This structure resembles cone complex crossed lamellar structure (CCCL) in radial section. D. Commarginal section showing mutually parallel folia. E–F. Irregular complex crossed foliated structure (ICCF). Inner shell surface. A–B. Patella vulgata (UMUT RM28555). C. Pectinodonta rhyssa (UMUT RM28595). D. Pectinodonta orientalis (UMUT RM28598). E–F. ‘‘Lottia’’ scabra (UMUT RM28551).

Crossed foliated structure (CF) foliated dipping at equal angle to growth surfaces but in opposite directions in adjacent ﬁrst-order units. (Figures 15A–B, 16D, 17L) Third-order units thin, lamellae, margined with sharp Deﬁnition.—First-order units arranged in radial or edges, arranged parallel. commarginal directions. Second-order units regularly Dip angle.—Ca. 10 degrees in second-order units. Shell structure of Patellogastropoda 161

Size.—Ca. 40 mm thick in first-order units, 0.3 mm first-order units, and ‘‘complex’’ means the arrange- thick in second-order units, 1–2 mmwideinthird- ment of folia is not unidirectional. Irregularly foliated order units. structure (ifo) of MacClintock (1967) in Nacella is Taxonomic and layer distribution.—M2, Mþ2and identified as the same structure. Mþ3 layers of Patella (Figure 2). Remarks.—This structure resembles crossed la- Discussion mellar structure (CL); but the second-order units of this structure have a smaller dip angle and the third- Shell layers order units are wider than those of CL. The number of shell layers is variable among the patellogastropods. Most species have five layers, viz. Irregular crossed foliated structure (ICF) three outer layers, myostracum and single inner layer (Figure 2), whereas Niveotectura and Patelloida, Pa- (Figures 15C–D, 16E) tella, Nacella and ‘‘Lottia’’ scabra have only four lay- Definition.—First-order units, patch-like, irregular ers, viz. two outer layers, myostracum and single inner in shape. Second-order structures arranged in radial layer.Onlylimitedtaxa(Bathyacmaea and Ata- directions; units in adjacent first-order units having lacmea) have six layers, viz. four outer layers, my- opposite dip directions. Third-order units thin, blade- ostracum and single inner layer or three outer layers, like. myostracum and two inner layers. Dip angle.—Ca. 10–20 degrees in second-order There is no doubt about the homology of the my- units. ostracum across the entire taxa of patellogastropods. Size.—Ca. 40–60 mm wide in first-order units, 1 mm It is formed at the insertions of homologous shell thick in second-order units. muscles (including pedal and pallial retractor muscles) Taxonomic and layer distribution.—M1 layer of on the interior shell surface. Therefore, it is regarded Pectinodonta (Figure 2). as an unmistakable landmark among shell layers. Remarks.—This structure was newly described in There are some tendencies in the distribution of patellogastropods. Its name was given following the shell microstructures throughout patellogastropods. scheme of irregular crossed lamellar structure (ICL) Most typically, prismatic layers are always deposited of Carter (1990c). This structure resembles compo- on the outer layer, especially on the outermost layer. site prismatic structure (CP), but the first-order struc- It is also a common characteristic that many species ture does not take a form of a prism. It is also similar share paired crossed lamellar layers (CL) across the to radial crossed lamellar structure (rCL) or cone myostracum. These layersmaybeviewedashomo- complex crossed lamellar structure (CCCL) in radial logues in congruent position. section, but the arrangement of crystal units in ICF is In some cases, homology of shell layers may be parallel in commarginal section, unlike rCL and suggested by comparable order of layer arrangement, CCCL. even though the total number of shell layers is different. For example, Atalacmea fragilis has an identical Irregular complex crossed foliated structure (ICCF) layer arrangement with other Lottiinae, except only for M+1 having radial crossed lamellar structure (Figures 15E–F, 16F) (rCL) (Figure 2). Therefore, it is considered that the Definition.—Unlike CF, the first-order structures shell structures of A. fragilis and other Lottiinae have patch-like, irregular in shape. Second-order units reg- derived from a common pattern through insertion or ularly foliated, arranged in parallel, having different deletion of a single layer. In this case, Mþilayerof growth directions in each first-order unit like ICCL. other Lottiinae should be homologous to Mþ(iþ1) Third-order units thin, blade-like. layer of A. fragilis. In the Lepetidae, the comparison Dip angle.—Ca. 10 degrees in second-order units. among the species examined suggests that the outer- Size.—Ca. 0.5 mm thick and 2–7 mmwideinthird- most layer of irregular spherulitic prismatic structure order units. type-A (ISP-A) of Cryptobranchia kuragiensis may Taxonomic and layer distribution.—Mþ2 layer of correspond to that of irregular complex crossed la- Scutellastra and M1 layer of Nacella (Figure 2). mellar structure (ICCL) in other species of the Lep- Remarks.—Crossed foliated structure with irregular etidae (Figure 2). crystal unit morphology and growth direction is re- In the remaining shell layers, homology is difficult to defined as irregular complex crossed foliated structure establish under positional criteria. More accurate re- (ICCF). ‘‘Irregular’’ implies a random form of the lations among different shell layers may be suggested 162 Takeshi Fuchigami and Takenori Sasaki

Figure 16. Schematic illustrations of crossed structures.A.Crossed lamellar structure (CL). B. Cone complex crossed lamellar structure (CCCL). C. Irregular complex crossed lamellar structure (ICCL). D. Crossed foliated structure (CF). E. Irregular crossed foliated structure (ICF). F. Irregular complex crossed foliated structure (ICCF). a. Inner surface. b. Commarginal vertical section. c. Radial section. d. Oblique three-dimensional view. White and gray arrows indicate the directions of crystal growth and accretionary shell growth, respectively. Shell structure of Patellogastropoda 163

Figure 17. Isolated crystal units of various microstructures. A. Simple prismatic structure type-A (SP-A). B. Simple prismatic structure type-B (SP-B) C. Irregular spherulitic prismatic structure type-A (ISP-A). D. Irregular spherulitic prismatic structure type-B (ISP-B) E. Composite prismatic structure with minor irregular spherulitic prismatic structure (CP-ISP). F. Niveotectura-type composite prismatic structure (NCP). G. Regularly foliated structure (RF). H. Semi-foliated structure (SF). I. Regular fibrous foliated structure (RFF). J. Cone complex crossed lamellar structure (CCCL). K. Irregular complex crossed lamellar structure (ICCL). L. Crossed foliated structure (CF). 164 Takeshi Fuchigami and Takenori Sasaki Shell structure of Patellogastropoda 165 by the sequence of shell layer appearance during on- to Nacellidae and Acmaea mitra, and semi-foliated togeny from larval to adult shells and also by the dis- structure (SF) is shared by Lepetidae and Pectino- tinction between two crystal forms of calcium carbo- dontinae. RF and SF are also formed in bivalves nates (aragonite and calcite) in each shell layer. (Carter, 1990a, b) but not in other gastropods. Regu- lar fibrous foliated structure (RFF) and irregular fi- Taxonomic distribution of microstructures brous foliated structure (IFF) are found only in Lottia The microstructures described above are not uni- langfordi and ‘‘Lottia’’ scabra. versally distributed throughout the Patellogastropoda. (3) Crossed structures: Various forms of crossed The comparison in taxonomic order (Figure 2) reveals lamellar structure (CL) are common to most taxa of that most microstructures tend to be restricted to par- gastropods. In Patellogastropoda, all genera excluding ticular taxonomic groups at genus to family levels. Nacella have this structure mainly on both sides of the (1) Prismatic structures: In Patellogastropoda, a myostracum. Irregular complex crossed lamellar majority of species in Lottiidae, Nacellidae and Ac- structure (ICCL) is shared by most taxa of Lepetidae maeidae have the prismatic structure in their outer and generally possessed by gastropods and bivalves. shell layers. Simple prismatic structure type-A (SP-A) Irregular complex crossed foliated structure (ICCF) and Irregular spherulitic prismatic structure type-B is restricted to part of bivalves and patellogastropods (ISP-B) characteristically occur in Cellana and Pa- (Carter, 1990c; this study).Crossedfoliated(CF), telloida, respectively. Fibrous prismatic structure type- irregular crossed foliated (ICF), and cone complex A (FP-A) is common to most taxa of Lottiinae. Irreg- crossed lamellar (CCCL) structures are restricted to ular spherulitic prismatic structure type-A (ISP-A) is Patella, Pectinodonta,andCellana mazatlandica,re- widely shared by Lottiinae and Acmaeidae in the spectively within Patellogastropoda. outermost layer. Simple prismatic structure type-B (SP-B), fibrous Shell structure groups prismatic structure with minor irregular spherulitic The high diversification at microstructural level prismatic structure (FP-ISP) and two types of com- in contrast to simple macroscopic morphology is posite prismatic structure (CP-ISP, NCP) are specific a noticeable characteristic of patellogastropod shells. to part of patellogastropods among gastropods. Al- MacClintock (1967) categorized patellogastropods into though ‘‘fibrous prismatic structure’’ is commonly 17 groups by combination of microstructures. Follow- found in bivalves (Carter, 1990a, b), their surface ing his concept, 20 groups were recognized in 44 spe- sculpture of first-order units is strikingly different cies in this study (Figures 2, 18). from that of patellogastropods. ‘‘Composite prismatic The comparison between MacClintock (1967) structure’’ also has been documented in other gastro- and this study revealed 7 new shell structure groups pods or bivalves, but they are identified as ‘‘denticular (Groups D, E, F, N, Q, R and S). MacClintock’s or non-denticular composite prismatic structure’’ (1967) Groups 1 and 15 can be subdivided into a few (Carter, 1990c) unlike those in patellogastropods. more groups as a result of detailed redefinition of mi- (2) Laminar structures: Nacreous structure is dis- crostructures by means of SEM. By contrast, the distributed in the Vetigastropoda and Cephalopoda as tinction between Groups 12 and 13 was not verified in columnar nacreous structure and in Bivalvia as sheet this study. The identical results were obtained be- nacreous structure (Carter, 1990c; Hedegaard, 1997). tween Groups 3 and H, 4 and I, 8 and J, 9 and K, 11 All patellogastropod taxa lack this structure. On the andL,and16andT.GroupsQ,R,andSwerenewly other hand, Nacellidae, Acmaeidae, Lepetidae and a recognized in the species that were not examined few species of Lottiidae have four kinds of foliated by MacClintock (1967). Species belonging to Mac- structures (RF, SF, RFF and IFF). These micro- Clintock’s (1967) Groups 5–7, 10 and 17 were not ex- structures are mainly distributed in Mþ2 layers except amined in this study. for Bathyacmaea (M1, Mþ1andMþ3) and Nacella Group 1 of MacClintock (1967) included many dif- (Mþ1). Regularly foliated structure (RF) is limited ferent supraspecific taxa. However, as a result of de-

U Figure 18. Comparison of shell structure groups of MacClintock (1967) and this study. Shell-layer thickness is approximately pro- portional to actual thickness except for very thin layers. Broken arrows indicate possible correspondence between different species in the same genus. See the captions of Figure 2 for abbreviations used in this study. Abbreviations used by MacClintock (1967): ccf, concentric crossed foliated; ccl, concentric crossed lamellar; cp, complex prismatic; fi, fibrillar; fo, foliated; ifo, irregular foliated; itf, irregular tabulate foliated; mf, modified foliated; rcf, radial crossed foliated; rcl, radial crossed lamellar; sp, simple prismatic; xcl, complex crossed lamellar. 166 Takeshi Fuchigami and Takenori Sasaki tailed observations, it was divided into four groups, of the Lepetidae possess semi-foliated structure (SF) Groups A (includes Lottia, Nipponacmea and Tec- and irregular complex crossed lamellar structure tura), B (Yayoiacmea and Lottia), C (Tectura)andD (ICCL), except for Cryptobranchia kuragiensis.The (Niveotectura). The distinction of these groups re- Acmaeidae is characterized by an outermost spher- sulted from the division of MacClintock’s (1967) ‘‘fi- ulitic prismatic (SpP) layer and an underlying semi- brillar prismatic (fp)’’ in the Mþ2 layer into simple foliated (SF) layer in general. In the Lottiidae most prismatic structure type-B (SP-B), fibrous prismatic species are typified by an outer layer of spherulitic structure with minor irregular spherulitic prismatic prismatic structure (SpP) and a subjacent layer of fi- (FP-ISP), and composite prismatic structure with mi- brous prismatic structure (FP-A, FP-B) except species nor irregular spherulitic prismatic (CP-ISP). Niveo- of Patelloida and Niveotectura. tectura pallida (as Acmaea pallida in MacClintock, All the above results imply that shell structures 1967) of Group F was a member of Group 1 of Mac- can be used as characters to identify systematic posi- Clintock (1967). This grouping was refined by the new tion of fossil species mostly without any information observations on the outermost layer of N. pallida. on soft parts. Thus it is possible to trace the chrono- Group 15 was divided into Groups O and P based logical distribution of patellogastropods by applying on the differences in foliated structures (RF and SF). the taxon-shell structure correlations in the Recent The units of regularly foliated structure (RF) area species to fossil patellogastropods. composed of thin blades with smooth surface and On the other hand, some groups do not conform to equal thickness. On the other hand, the foliated units a one-to-one relationship between shell structure and of semi-foliated structure (SF) consist of flakes with taxonomic groups. The inconsistency is found in the rough surface and irregular thickness. case in which species belonging to the same genus The separation of Group 13 and Group 12 by the have different shell structures. Lottia cassis or Lottia presence of irregular tabulated foliated structure (itf) kogamogai versus other species of Lottia is an exam- by MacClintock (1967) was not confirmed even under ple of such cases (Figure 2). Species currently assigned SEM-level observation. Accordingly, these two groups to the genus ‘‘Tectura’’ have composite prismatic were incorporated into Group M. Based on Mac- structure with minor irregular spherulitic prismatic Clintock’s (1967) description, Carter (1990c) re- structure (CP-ISP), but its type species, T. virginea, garded the structure (itf) as calcitic semi-nacreous, but lacks it. The taxonomic relationships of these taxa it may be transitional layer from concentric crossed may need reconsideration by further phylogenetic lamellar (ccl, Mþ1) to regularly foliated structure (fol, studies. Mþ3). The Acmaeidae and Lepetidae are the groups that have been founded on limited anatomical characters Systematic implications compared to the rest of the patellogastropods. For MacClintock (1967) stated that ‘‘there is a close example, the Acmaeidae has been defined mostly by relationship’’ between shell structure groups and clas- a single shell microstructural character, i.e., the pos- sification in patellogastropods. In the current system- session of foliated structure (Lindberg, 1988a, 1998; atics, however, his shell structure groups and taxo- Sasaki, 1998). Recently Nakano and Ozawa (2004) nomic groups have some major conflicts especially in proposed to transfer Niveotectura pallida from the the Acmaeidae, Lottiidae and Patellidae. For exam- Lottiidae to the Acmaeidae based on the results of ple, Group 1 of MacClintock (1967) has many genera molecular analysis. This new assignment is not consis- belonging to the Acmaeidae, Lottiidae and Patellidae tent with the conventional definition of the family by (MacClintock, 1967: table 5). the possession of foliated structure. Currently it is The results of this study, however, revealed that re- not possible to evaluate the validity of this systematic vised shell structure groups are more consistently cor- change from the anatomical viewpoint, because the related with taxa in the up-to-date systematics based animal of the type species of Acmaea (A. mitra)has on anatomical characters. Most genera examined have never been studied, except for its radular morphology specific and conservative shell structure, and there is (Lindberg, 1981). These less clearly defined genera almost no conflict, with a few exceptions (Figure 2). and families should be further investigated for all At the family level, all members of Patellidae secrete available characters. either crossed foliated structure (CF) or irregular Although many authors tried to reveal phylogenetic complex crossed foliated structure (ICCF), and mem- relationships of patellogastropod limpets (Dall, 1876; bers of the Nacellidae can be identified by regularly Lindberg, 1988a; McLean, 1990; Hodgson, 1995; Lind- foliated structure (RF) without exception. The species berg, 1998; Sasaki, 1998; Koufopanou et al., 1999; Shell structure of Patellogastropoda 167

Harasewych and McArthur, 2000; Nakano and Ozawa, Carter, J. G., 1990a: Evolutionary significance of shell micro- 2004), no complete consensus has been achieved yet. structure in the Palaeotaxodonta, Pteriomorphia and Iso- In ed. Therefore, the evolutionary scenario of shell micro- filibranchia (Bivalvia: Mollusca). , Carter, J. G. , Skeletal Biomineralization: Patterns, Processes and Evolu- structure is difficult to present here. A robust phylo- tionary Trends, vol. 1, p. 135–296. Van Nostrand Rein- genetic hypothesis is required to discuss the homology hold, New York. and evolutionary process of microstructural characters Carter, J. G., 1990b: Shell microstructural data for the Bivalvia. for further implications. In, Carter, J. G. ed., Skeletal Biomineralization: Patterns, Processes and Evolutionary Trends, vol. 1,p.297–411.Van Nostrand Reinhold, New York. Acknowledgements Carter, J. G., 1990c: Glossary of skeletal biomineralization. In, Carter, J. G. ed., Skeletal Biomineralization: Patterns, Pro- cesses and Evolutionary Trends, vol. 1,p.609–661.Van WeareverygratefultoJosephG.Carter,Uni- Nostrand Reinhold, New York. versity of North Carolina at Chapel Hill for iden- Carter, J. G. and Ambrose, W. W., 1989: Techniques for study- tification of various microstructures, suggestions on ing molluscan shell microstructure. In, Feldmann, R. M., research technique and literature, and for critical Chapman, R. E. and Hannibal, J. T. eds., Paleotechniques, reading of the manuscript. We also thank Klaus p. 101–119. The Paleontological Society, Special Publica- tion no. 4. Bandel, Geological-Paleontological Institute and Carter, J.G. and Hall, R.M., 1990: Polyplacophora, Scapho- Museum, Hamburg University for comments and poda, Archaeogastropoda and Paragastropoda (Mollusca). improvement of the manuscript. This study was con- In, Carter, J. 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