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1 July 2018 Cheilostome Bryozoa from the Upper Cretaceous Himenoura Group, Kyushu, Japan
Matthew H. Dick, Chika Sakamoto, Toshifumi Komatsu
Author Affiliations +
Abstract

Cheilostome bryozoans (Phylum Bryozoa; Order Cheilostomata) originated in the latest Jurassic but remained at low diversity until the late Albian–early Cenomanian, when they began an explosive radiation that has continued to the present day. Most knowledge of Late Cretaceous cheilostomes comes from Europe and the USA from deposits associated with the western Tethys Ocean. Only a few previous records of Cretaceous bryozoans exist from the margin of eastern Asia in the NW Pacific. We examined material from four localities of early– middle Campanian age in the Himenoura Group, Shimokoshikijima Island, Kagoshima Prefecture, southern Kyushu, Japan, and detected six cheilostome species but no cyclostomes. Two species were relatively common. For one of these, we erect the new genus Kenocharixa and describe a new species, Kenocharixa kashimaensis; we also transfer Charixa goshouraensis Dick, Komatsu, Takashima, and Ostrovsky and Conopeum stamenocelloides Gordon and Taylor to Kenocharixa. We describe the other common species as Marginaria prolixa sp. nov. We detected four species as a single specimen each and identified them only to genus (Charixa sp. A) or listed them as Incertae sedis (A, B and C). Among the six cheilostomes, five are primitive anascan-grade (malacostegan) species and one is an anascan-grade neocheilostome. Compared to Campanian–Maastrichtian bryozoan faunas in Europe and the USA, the Himenoura fauna is low in diversity and morphological disparity, with no cribrimorph or ascophoran species detected. Previous researchers have suggested that the NW Pacific biota became isolated from that of the Tethys in the latest Aptian–middle Albian interval. We advance the hypothesis that the Late Cretaceous bryozoan fauna in the NW Pacific is a low diversity relict of the fauna present when this isolation occurred. While Tethyan cheilostome lineages underwent a major radiation associated with the origins of cribrimorph and ascophoran frontal shields, the NE Pacific lineages failed to diversify at the same rate and remained at low diversity and disparity. Testing this hypothesis will require much further sampling in Cretaceous deposits along the margin of East Asia.

Introduction

Cheilostome bryozoans (Phylum Bryozoa, Class Gymnolaemata, Order Cheilostomata) originated in the latest Jurassic (Taylor, 1994) and existed at low diversity for about 60 my. Starting in the late Albian to early Cenomanian, they began an explosive radiation (Taylor, 1988a; Ostrovsky et al., 2008) that has continued to the present. While cyclostome bryozoans dominated assemblages throughout the Early Cretaceous, a faunal turnover occurred in the Late Cretaceous so that cheilostomes became the dominant group. This turnover apparently occurred at different times in different areas; in Cenomanian to Turonian assemblages in northern Europe, the ratio of cyclostome to cheilostome species was still roughly 3:1, whereas in a coeval assemblage in the Bagh Beds in India the ratio was reversed (Taylor and Badve, 1994).

Most knowledge of the Cretaceous radiation of cheilostomes comes from deposits in Europe and the USA associated with the western Tethys. Although Lower to Upper Cretaceous strata from brackish to marine habitats are widespread along the margin of eastern Asia (e.g. Komatsu and Maeda, 2005; Iba and Sano, 2007; Komatsu et al., 2008), knowledge of Cretaceous cheilostomes from this region is extremely limited and is restricted to the Japanese archipelago. The only previous records are Dysnoetocella? voigti Nishizawa and Sakagami, 1997 of Campanian age from Shikoku Island; an unidentified malacostegan species of middle Cenomanian age from Hokkaido (Ostrovsky et al., 2006); and an assemblage of six cheilostome species (three of which were described as incertae sedis due to limited, poorly preserved material) and one cyclostome from the upper Albian to lower Cenomanian Goshoura Group on Kyushu (Dick et al., 2013).

Elucidating the diversity and composition of Late Cretaceous cheilostome assemblages along the continental margin of eastern Asia is of evolutionary and biogeographical interest (Dick et al., 2013). While the carbonate platform biota in NE Asia (NW Pacific) belonged to the Tethyan biotic realm through most of the Early Cretaceous, Mesogean (Cretaceous Tethys) key and indicator taxa (rudists, dasycladacean algae, hermatypic corals, stromatoporoids, nerineacean gastropods, orbitolinid foraminifers, and calcareous red algae) and coated grains disappeared from carbonate platforms along the margin of NE Asia in two stages from late Aptian to middle Albian times (Iba and Sano, 2007, 2008). This demise of the Asian carbonate platform biota suggests that the Tethyan and NE Asian biotas became isolated from one another. Reflecting this isolation, many endemic species began to appear in molluscan genera in the NW Pacific in the middle Albian, signaling the beginning of an endemic North Pacific fauna. It is not clear how this late Aptian to middle Albian biotic turnover in the NW Pacific affected the composition and diversity of bryozoans, as no bryozoan assemblages of this age have yet been documented in the region.

The Upper Cretaceous Himenoura Group, consisting of non-marine and marine siliciclastics, crops out on the central west side of Kyushu, Japan (Ueda and Furukawa, 1960; Tashiro et al., 1986; Komatsu et al., 2008; Kojo et al., 2011), and includes marine deposits of Santonian to Campanian age containing abundant molluscan fossils (Komatsu et al., 2008). The upper part of the Himenoura Group is exposed in the Kashima area (Figure 1A), northern Shimokoshikijima Island (Kagoshima Prefecture), off the SW coast of Kyushu. These brackish to marine, lower to middle Campanian deposits contain abundant molluscan fossils (Tanaka and Teraoka, 1973; Tashiro, 1976; Inoue et al., 1982; Kanoh et al., 1989; Komatsu et al., 2014), among which bryozoans are moderately common, often encrusting bivalves. The goal of this study was to document the composition of this Campanian bryozoan assemblage for comparison with coeval Tethyan bryozoan assemblages.

Material and methods

Geological setting and fossil sites

Units U-I, U-IIa–d, and U-IIIa–d of the Himenoura Group are exposed on Shimokoshikijima Island (Tashiro, 1976; Kanoh et al., 1989), with U-IIb–d and U-IIIa–b occurring in our study area (Figures 1, 2) in the Kashima region (Figure 1A, B). U-II is composed mainly of fossiliferous marine sandstone and mudstone intercalated with abundant shell concentrations that include the lower and middle Campanian inoceramids Sphenoceramus orientalis and S. schmidti, and the ammonoids Eupachydiscu s haradai and Eulophoceras sp. (Noda et al., 1995; Miyake et al., 2011; Komatsu et al., 2014; Misaki et al., 2016). U-III consists of non-marine and shallow marine conglomerate, sandstone, and mudstone, and contains Crassostrea oyster banks, trigoniid bivalves, and isolated dinosaur remains (Toshimitsu et al., 1990; Miyake et al., 2011; Komatsu et al., 2014). Aramaki et al. (2013) reported middle Campanian radiolarian assemblages characterized by Amphipyndax pseudoconulus from the upper part of U-III.

Bryozoans were collected at four localities (Figure 1): Loc. 1 (Figure 2A), NE side of Tsuburazaki Point (31°47′10″N, 129°47′24″E); Loc. 2 (Figure 2E, F), Kumagasehana Point (31°45′37″N, 129°48′13″E); Loc. 3 (Figure 2B–D), Ukimizuura (31°45′18″N, 129°47′09″E); and Loc. 4, Higireura (31°44′25″N, 129°46′48″E). Bryozoans occur commonly in unit U-IIb at Locs. 1 and 3, and uncommonly in unit U-IIb at Loc. 4 and in unit U-IIIa at Loc. 2 (Figures 36). Unit IIb is dominated by dark gray mudstone containing very fine, parallel-laminated sandstones that accumulated in an outer shelf environment. U-III is characterized by sandstones containing Crassostrea oyster banks and tidal bundles (Dalrymple, 1992) that were deposited in intertidal to subtidal environments.

At Locs. 1, 3, and 4, outer shelf mudstones contain abundant lenticular shell concentrations 1–5 cm thick consisting of fragments of inoceramid shells (which are commonly encrusted by bryozoans) (Figure 2C, D), serpulid tubes, and corals. Fragments of branched, erect bryozoan colonies also occasionally occur in these shell concentrations. At Loc. 2, the Crassostrea oyster banks are overlain by a concentration of mainly broken Crassostrea shells that also occasionally contain bryozoans.

Collection and handling of specimens

Bryozoans were collected by breaking apart fossiliferous rocks with hammer and chisel and searching by eye and with a hand lens for bryozoan colonies encrusting the surfaces of fossil bivalves and the molds left by bivalves in the rock matrix, and for fragments of erect colonies in the matrix itself. Cretaceous bryozoans in Japan are usually detected as the basal surface of the colony visible on the surface of a rock cast or mold left by the original, usually molluscan substrate, the colony having separated from the shell. In many cases, natural dissolution of the skeleton of the bryozoan colony itself leaves a mold from which a detailed vinyl polysiloxane (VPS) silicone cast can be made, which can then be viewed by scanning electron microscope (SEM) (Dick et al., 2009, 2013). The methods used in this study to prepare specimens, make VPS casts, and prepare the casts for SEM were as described by Dick et al. (2009). Bryozoan specimens and silicone casts were coated with Au in a JEOL JFC-1500 quick auto coater (JEOL Ltd., Tokyo) and images were captured with a JEOL JSM-6360LV scanning electron microscope (JEOL Ltd., Tokyo).

Figure 1.

A, map of Kyushu, southern Japan (left), showing the location of the Koshikijima Islands (shaded box), enlarged on the right. Unshaded box on right indicates the area enlarged in panel B. B, geological map of the northern part of Shimokoshikijima Island, indicating strata of the Himenoura Group. Lines X–X′ and Y–Y′ indicate the positions of the cross-sections at the upper left and lower right, respectively.

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Figure 2.

Selected photographs from collecting localities on Shimokoshikijima Island. A, locality 1, Tsuburazaki. Star indicates where bryozoans were found. B, locality 3, Nakayama (western area). Stars indicate bryozoan sites. C, locality 3, Inoceramus cycloides encrusted by bryozoan colonies. D, locality 3, outer mold of large inoceramid shell fragment. Arrows indicate the outline of a large bryozoan colony. E, locality 2, Ukimizuura. Circle indicates the site where a specimen of Incertae sedis C was collected. F, enlargement of the rock face circled in panel E, showing the positions of bivalve shell concentrations and oyster colonies. Star indicates where Incertae sedis C was collected.

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Figure 3.

Stratigraphic column at Locality 1 (see Figure 1) within the Himenoura Group. Filled circles indicate the occurrences of bryozoan species, as well as of indicator bivalve and ammonoid species.

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Zooidal characters were measured from SEM images by using ImageJ software ( http://rsbweb.nih.gov/ij/); the target sample size for measurements was 15 zooids in the zone of astogenetic repetition in each colony, although in some cases fewer adequate zooids were available. Specimen HimeL2-1 was photographed with a Nikon D5200 digital camera mounted on a Nikon SMZ1500 stereoscopic microscope, and zooidal measurements were made from photomicrographs after scales were determined with an ocular micrometer and a 1.00 mm objective rule divided into 0.01 mm units. Measurements of zooidal characters are defined in the text by combinations of the following abbreviations: Av, avicularium; Cp, zooid with closure plate; Ip, interzooidal polymorph; Iz, interzooidal; L, length; Op, opesia; Ov, ovicell; W, width; Z, autozooid. For example, ZOpL = auto zooidal opesia length, CpL = length of zooid with closure plate, IzAvL = interzooidal avicularium length, and so forth.

Figure 4.

Stratigraphic column at Locality 2 (see Figure 1) within the Himenoura Group. Filled circles indicate the occurrence of the bryozoan Incertae sedis C, as well as of indicator bivalve species.

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Figure 5.

Stratigraphic column at Locality 3 (see Figure 1) within the Himenoura Group. Filled circles indicate the occurrences of bryozoan species, as well as of indicator bivalve and ammonoid species.

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All specimens, including type material and casts, have been deposited in the National Museum of Nature and Science (Department of Geology and Paleontology), Tsukuba, Japan, under catalog numbers with the prefix NMNS PA, with the number referring to both the specimen and the cast. Specimens examined in this study are listed in Table 1, with entries including both the NMNS PA number and the original specimen number; the table also indicates type specimens. The classification presented herein above the genus level is that of Gordon (2017).

Systematic descriptions

Class Gymnolaemata Allman, 1856
Order Cheilostomata Busk, 1852a
Suborder Malacostegina Levinsen, 1902
Superfamily Membraniporoidea Busk, 1852b
Family Electridae Stach, 1937
Genus Kenocharixa gen. nov.

  • Type species.—Kenocharixa kashimaensis sp. nov., by original designation.

  • Additional species.—We here transfer to Kenocharixa the species Charixa goshouraensis Dick, Komatsu, Takashima and Ostrovsky, 2013 and Conopeum stamenocelloides Gordon and Taylor, 2015.

  • Etymology.—The name combines Charixa, referring to similarity to that genus, with “keno”. referring to the characteristic kenozooidal extensions filling interzooidal grooves.

  • Diagnosis.—Colony encrusting, unilaminar, sheet-like or erect, bilaminar. Gymnocyst moderate to negligible; long cauda lacking. Opesia occupying most of frontal surface, oval or elliptical in outline. Cryptocyst sloping, granulated. Zooids with closure plates scattered throughout colony, often grouped; variable in frequency. Spines lacking. Medium-sized kenozooids (here termed ‘interzooidal polymorphs’ to distinguish them from the smaller proximolateral kenozooids) present or absent; scattered throughout colony. Small kenozooids arise from proximolateral corners of zooids on one or both sides, sending out long extensions that fill interzooidal grooves. Zooids have distal and distolateral buttressed recesses leading to multiporous septula. Ancestrula initially buds three zooids, distally and distolaterally; ancestrula and several generations of daughter zooids can have closure plates. Avicularia, ovicells lacking.

  • Remarks.—In the type species, most zooids bear paired, initially triangular kenozooids covering the proximal gymnocyst, a feature that along with the absence of avicularia and ovicells suggested placement in Conopeum Gray, 1848, the type species of which, Millepora reticulum Linnaeus, 1767, has similar kenozooids. Dick et al. (2013) discussed at length the taxonomic problems associated with Conopeum, noting that few Recent or fossil species currently placed in that genus show the same suite of characters as the type species. In particular, it is controversial whether paired proximal kenozooids are diagnostic for the genus. Dick et al. (2013) described from southern Japan another malacostegan species, Charixa goshouraensis, of late Albian–early Cenomanian age. The genus Charixa Lang, 1915 provided a reasonable but not entirely satisfactory fit for that species, which has a multiserial colony with contiguous zooids and commonly has zooids with closure plates. In Charixa, colonies tend to be pluriserial with irregularly arranged, partly contiguous zooids, and closure plates are generally uncommon. With regard to generic placement, we realized that both Charixa goshouraensis and the new species from Shimokoshikijima resembled species in the Cretaceous genera Charixa and Spinicharixa Taylor, 1986a, but shared a unique character not present in the latter two genera—proximolaterally derived kenozooids that ramify into the surrounding interzooidal grooves, eventually connecting with rami from other kenozooids and filling the grooves. We thus erect the new genus Kenocharixa for these two species from the Cretaceous of southern Japan.

  • We also transfer to Kenocharixa the species Conopeum stamenocelloides Gordon and Taylor, 2015, described from the Eocene of New Zealand; this species resembles Kenocharixa kashimaensis in having paired, triangular proximolateral kenozooids that extend into and fill the interzooidal grooves, and autozooids with closure plates. The cryptocyst in C. stamenocelloides is much wider than in K. kashimaensis, especially proximally, whereas that in K. goshouraensis is intermediate between the two, and generally wider proximally than laterally. Kenocharixa goshouraensis lacks the obligate paired, triangular kenozooids seen in the other two species, but they are often paired and triangular (e.g. Dick et al., 2013: figs. 7B, D, E; 8B). Conopeum stamenocelloides differs from K. kashimaensis and K. goshouraensis in forming an erect, bilaminar colony and in having interzooidal connections in the form of small mural septula (Gordon and Taylor, 2015). The difference in colony form is not an impediment to placement in the same genus, as various cheilostome genera contain both encrusting unilaminar and erect species (e.g. Thalamoporella, Porella). The nature of the interzooidal connections need also not be an impediment; the septula in C. stamenocelloides appear to be set in mural depressions (Gordon and Taylor, 2015: fig. 21A, B) that may be the vestiges of the buttressed recesses seen in K. kashimaensis and K. goshouraensis.

  • Characters in Kenocharixa patchily overlap with those in Spinicharixa and Charixa. The primary difference between the latter two genera is that zooids in Spinicharixa have numerous spine bases around the margin of the cryptocyst, whereas those in Charixa lack spine bases or have only a small distal pair (Taylor, 1986a). The three species we place in Kenocharixa appear to lack spine bases altogether, a feature shared with some species in Charixa but distinguishing it from Spinicharixa. Taylor (1986a) also considered Spinicharixa and Charixa to differ in the degree of colony coherence, with species in Spinicharixa having pluriserial or multiserial colonies with regularly arranged zooids, and those in Charixa having pluriserial colonies with irregularly arranged zooids. This difference is not as clear as with the presence or absence of marginal spines; of the two species currently placed in Spinicharixa, S. pitti Taylor, 1986a has a multiserial colony with zooids in regular quincuncial arrangement, whereas S. dimorpha Taylor, 1986a has a pluriserial colony with zooids less tightly packed, as is more typical of Charixa. The three species we place in Kenocharixa have multiserial, sheet-like colonies with tightly packed zooids, although the arrangement of zooids is less regular in K. goshouraensis than in the other two. The frequency of closure plates may also provide a useful diagnostic character; zooids with closure plates appear to be variably present and generally uncommon in species of Spinicharixa and Charixa, but more common in two of the species we place in Kenocharixa; Gordon and Taylor (2015) did not observe them in K. stamenocelloides, although they examined only two small specimens. Interestingly, the key character separating Kenocharixa from Spinicharixa and Charixa—the ramifying kenozooids—occurs in rudimentary form in Charixa; one of Taylor's (1986a: fig. 7c, p. 206) figures shows a kenozooid arising from the fusion of proximal buds from several autozooids and sending short extensions into interzooidal grooves.

  • Figure 6.

    Stratigraphic column at Locality 4 (see Figure 1) within the Himenoura Group. Filled circles indicate the occurrences of bryozoan species, as well as of indicator bivalve and ammonoid species.

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    Table 1.

    List of specimens examined in this study. For all but two specimens, SEM images were made from silicone casts. Incertae sedis B was examined by SEM directly, without casting, and Incertae sedis C was examined by light microscopy.

    t01_239.gif

    Kenocharixa kashimaensis sp. nov.
    Figures 7, 8

  • Diagnosis.—Colony encrusting, unilaminar, sheetlike. Zooids elongate-oval, gymnocyst negligible; opesia occupying most of frontal area; mural rim narrow, coarsely granulose. Spines, ovicells, and avicularia lacking. Paired triangular kenozooids at proximal corners of zooids. Zooids with closure plates uncommon, same size as autozooids, usually grouped. Small interzooidal polymorphs occur sparsely among autozooids. Zooids interconnect via buttressed recesses leading to multiporous septula. Ancestrula and periancestrular zooids produce closure plates.

  • Etymology.—The specific name is an adjective referring to Kashima, the municipality in which the type locality is located.

  • Material examined.—Thirty-seven specimens from Locs. 1, 3, and 4. Holotype, NMNS PA18399 (Loc. 3). Paratypes, NMNS PA18400–18410. See Table 1.

  • Measurements.—Measurements from autozooids and closure plate zooids are in Table 2. Interzooidal polymorphs: IpL = 0.23–0.39 mm (0.292±0.048 mm); IpW = 0.12–0.23 mm (0.173±0.030 mm); IpOpL = 0.05–0.17 mm (0.103±0.028 mm); IpOpW = 0.04–0.09 mm (0.066±0.013 mm) [n = 15 from five colonies]. Ancestrula, NMNS PA19409: L = 0.241 mm; W = 0.150 mm; OpL = 0.086 mm; OpW = 0.076 mm [n = 1].

  • Description.—Colony encrusting, unilaminar, sheetlike (Figure 7A). Zooids in large parts of colony arranged in long, unbranched columns offset from one another one-half zooid length, giving rise to quincuncial pattern (Figure 7A). Large sectors of colony contain strictly parallel columns with no bifurcations; new sectors arise by distal-distolateral bifurcations on zooids along one side of single column. Autozooids (Figure 7B) elongate oval, delineated by narrow groove; gymnocyst negligible, covered by kenozooids. Cryptocyst moderately wide proximally and laterally around opesia, sloping at steep angle (Figure 8B), coarsely granulose; opesia occupying most of frontal surface. Most zooids produce paired triangular kenozooids (Figures 7B; 8B, C) proximolaterally; kenozooidal surface coarsely granulose, cryptocystal; kenozooids sometimes merging, forming single, broad proximal kenozooid (Figure 7B). In some cases, central opening of kenozooid seen to lead to one or two pores in proximal gymnocyst of underlying autozooid. Kenozooids extend lobes of calcification into adjacent interzooidal grooves (Figure 7B, D); with age, lobes completely fill zooidal grooves (Figures 7C; 8A, B), eventually rising above level of mural rim (Figure 8C) and forming coarse, nodular thickening covering proximal end of zooids (Figure 8D, E). Interzooidal polymorphs occur uncommonly among autozooids; usually much smaller than autozooids (arrowheads, Figure 7C) but occasionally nearly as large (upper two arrowheads, Figure 7D), with elliptical opesial opening and rounded mural rim; rim coarsely granulose in zone around opesia but smooth around margin. Zooids with closure plates occur uncommonly, singly or in groups of two to seven (Figure 7D); opesia reduced, oval or elliptical in outline, surrounded by tumid, rounded, coarsely granulose cryptocystal rim, with narrow zone of smooth gymnocyst around margin; opercular impression smooth, surrounded by horseshoe-shaped groove corresponding to opercular margin. Interzooidal polymorphs can occur among zooids with closure plates (Figure 7D). Zooids interconnect via distal and paired distolateral buttressed recesses, each leading to multiporous septulum (Figure 8A). Ancestrula (Figure 8F) budding triplet of zooids distally and distolaterally; ancestrula, triplet of zooids, and some but not all zooids in second and third generations from ancestrula forming closure plates; ancestrula and first two generations of daughter zooids with tapering proximal gymnocyst lacking kenozooids, which appear in some zooids in third generation from ancestrula. Intramural budding not observed.

  • Remarks.—The species most similar to Kenocharixa kashimaensis is the congener K. goshouraensis (Dick et al., 2013). Zooid size is similar, and in the zone of astogenetic repetition both species have elongate zooids with the opesia occupying most of the frontal area (compare Figure 7A herein with Dick et al., 2013: fig. 8A). The arrangement of zooids in the colony is less regular in K. goshouraensis, where zooids in some parts of the colony occur in quincunx but in other parts are arranged in non-offset columns, so that zooids are side-by-side in rows. Zooids of K. goshouraensis generally have a more extensive gymnocyst, especially proximally but also laterally, resulting in larger interzooidal grooves; in the zone of astogenetic change, the proximal gymnocyst can be extensive, with the opesia oval and only half as long as the zooid. As in K. kashimaensis, the kenozooids in K. goshouraensis that later elongate in the interzooidal grooves originate proximolaterally, but they are initially smaller, less regularly triangular, and less stereotyped in position (they can be paired, or lacking on one or both sides), and they tend to elongate primarily in the lateral groove between zooidal columns, rather than also filling the transverse groove between zooids (Dick et al., 2013: fig. 7A–E). Kenocharixa goshouraensis lacks the medium-sized interzooidal polymorphs seen in K. kashimaensis. The closure plates are similar between the two species, but those in K. kashimaensis are frontally tumid and convex, whereas those in K. goshouraensis are somewhat sunken inside the raised margin and have a smaller opesia. In K. goshouraensis, some intramurally budded zooids were seen to form closure plates (Dick et al., 2013: fig. 7F), whereas no intramural budding was observed in K. kashimaensis. The ancestrular budding pattem is identical in the two species; in both, the ancestrula gives rise to a triplet of daughter zooids distally and distolaterally, and the ancestrula and at least some zooids in the first three generations from the ancestrula have closure plates.

  • Zooids like those in Figure 7B might be interpreted as lacking heavy secondary calcification because they are young. However, Figure 8E shows less heavily calcified zooids adjacent and distal to heavily calcified zooids, suggesting that the former represent instead a basal primary layer of calcification that is typically overlain by a heavy secondary layer, with the latter having been diagenetically dissolved in part of the colony. The mechanism by which this could occur is not clear.

  • Figure 7.

    Kenocharixa kashimaensis sp. nov., SEM images of silicone casts from colony molds. A, paratype NMNS PA 18408, colony view showing colony-wide budding pattern; B, paratype NMNS PA18400, autozooids without heavy secondary calcification; C, paratype NMNS PA18405, autozooids and interzooidal polymorphs (arrowheads); D, holotype, NMNS PA 18399, autozooids, zooids with closure plates, and large interzooidal polymorphs (arrowheads). Scale bars: 1.0 mm (A); 0.20 mm (B, D); 0.50 mm (C).

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    Figure 8.

    Kenocharixa kashimaensis sp. nov., SEM images of silicone casts from colony molds. A, paratype NMNS PA18403, autozooids, showing interzooidal connections; B, paratype NMNS PA18409, heavily calcified autozooids, showing kenozooidal extensions in interzooidal grooves raised above the mural rims; C, paratype NMNS PA18403, moderately heavily calcified autozooids; note nodular accumulation covering proximal gymnocyst of right-center zooid; D, specimen NMNS PA18419, very heavily calcified colony, with autozooids and interzooidal polymorphs; E, paratype NMNS PA18403 showing apparent diagenetic loss of secondary calcification as seen in zooids at right, leaving primary layer as seen in zooids at left; F, paratype NMNS PA18409, ancestrula (arrowhead); ancestrula and some zooids within three generations of ancestrula appear to have closure plates. Scale bars: 0.20 mm.

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    Table 2.

    Measurements (in millimeters) for Kenocharixa kashimaensis sp. nov. For each set of values, the range is followed by the mean and standard deviation. Areas 1 and 2 in NMNS PA18404 were different parts of the same colony in the zone of astogenetic repetition; in the last column, sample sizes are indicated separately for autozooids (AZ) and zooids with closure plates (CP), with measurements of the latter presented as the average of two values.

    t02_239.gif

    Genus Charixa Lang, 1915

  • Type species.—Charixa vennensis Lang, 1915.

  • Charixa sp. A
    Figure 9

  • Material examined.—NMNS PA18434 (Loc. 1), one small colony.

  • Measurements.—ZL = 0.28–0.42 mm (0.349±0.037 mm); ZW = 0.18–0.27 mm (0.225±0.026 mm); ZOpL = 0.22–0.29 mm (0.247±0.024 mm); ZOpW = 0.11–0.18 mm (0.139±0.021 mm); n = 15.

  • Description.—Colony (Figure 9A) encrusting, unilaminar, irregular, forming pluriserial lobes. Autozooids mostly arranged in quincunx; irregularly hexagonal or oval, delineated by deep, moderately wide groove. Gymnocyst (Figure 9C) evident proximally and proximolaterally, but probably not laterally in zone of astogenetic repetition; long proximal cauda lacking. Mural rim raised; granulated cryptocyst sloping, widest proximally, tapering in width laterally around opesia, lacking distally. Opesia (Figure 9A–C) occupying most of frontal area, elongate-oval or elliptical, widest in center or proximal half. Zooids bear pair of small spine bases at distolateral corners (arrowheads, Figure 9C); ancestrula, periancestrular zooids (arrowheads, Figure 9D), and at least some autozooids (arrowheads, Figure 9B) show a larger spine base on one side in proximolateral part of mural rim. Interzooidal polymorphs occur as intramurally budded kenozooids (arrowheads, Figure 9A); center of frontal wall with small, elliptical or circular opesia. Ancestrula (arrow, Figure 9D) tatiform, with three pairs of spine bases; initially producing distal and paired distolateral daughter zooids; ancestrula possibly with closure plate, with traces of grooves corresponding to lateral opercular margins, although these apparent grooves could be casting artifacts, in which case the opesia is occupied by an intramurally budded kenozooid. Zooid distal to ancestrula with two intramural buds, with intramurally budded kenozooid forming inside those. Other zooids up to third generation from ancestrula with intramurally budded kenozooids. Proximolateral spine base enlarged on one side in ancestrula and two subsequent zooids (arrowheads, Figure 9D). Ovicells and avicularia not observed. Interzooidal connections evident as distal and one or two pairs of distolateral buttressed recesses.

  • Remarks.—We assign this species to Charixa on the basis of the generic diagnosis by Taylor (1986a). The colony is irregularly arranged; zooids have a moderately well developed proximal gymnocyst; the cryptocyst is narrow and coarsely granulose; and in most zooids, spine bases appear to be limited to a small distal pair. The occurrence of a single larger, spine base proximolaterally on the mural rim in some zooids might represent an enlarged spine or scutum. Incertae sedis A (next description) shows a raised structure in the same position, which might suggest that the two species are related, perhaps comprising a previously unrecognized genus.

  • Figure 9.

    Charixa sp. A., specimen NMNS PA18434, SEM images of silicone cast from colony mold. A, view of colony. Arrowheads indicate interzooidal polymorphs (intramurally budded kenozooids). B, group of autozooids. Arrowheads indicate enlarged proximolateral spine bases. C, group of autozooids. Arrowheads indicate distal spine bases. D, ancestrula (arrow) and several generations of daughter zooids. Arrowheads indicate enlarged proximolateral spine bases. Scale bars: 0.5 mm (A); 0.20 mm (B, D); 0.25 mm (C).

    f09_239.jpg

    Figure 10.

    Incertae sedis A, specimen NMNS PA18435, SEM images of silicone cast from colony mold. A, view of colony; B, enlargement from panel A, showing autozooids; C, enlargement from panel B, showing autozooids with distal spine bases (arrowheads) and enlarged proximolateral structure of unknown function (arrows); D, enlargement of autozooids from panel C, showing spine bases (arrowheads) and proximolateral structure (arrow). Scale bars: 1.0 mm (A); 0.50 mm (B); 0.20 mm (C, D).

    f10_239.jpg

    Incertae sedis A
    Figure 10

  • Material examined.—NMNS PA 18435 (Loc. 3), one colony, partly overgrown by Kenocharixa kashimaensis.

  • Measurements.ZL = 0.39–0.49 mm (0.425±0.032 mm); ZW = 0.25–0.32 mm (0.275±0.021 mm); OpL = 0.21–0.28 mm (0.242±0.021 mm); OpW = 0.15–0.18 mm (0.161 ±0.010 mm); all measurements, n = 15.

  • Description.—Colony (Figure 10A) unilaminar, encrusting, sheet-like. Autozooids (Figure 10B, C) oval in outline, delineated by deep groove; arranged in irregular rows, with zooids only occasionally in quincuncial pattern (Figure 10A, B). Gymnocyst evident proximally and proximolaterally. Mural rim raised, rounded, widest proximally, tapering laterally, narrow distally, covered with cryptocystal granulation; cryptocyst steep, lacking distally. Opesia oval to elongate-oval; distal end straight. Some autozooids show coarse pair of short, erect spine bases at distolateral corners (arrowheads, Figure 10C, D); small spine bases possibly present around mural rim but difficult to discern. Most zooids have a raised nodule (arrows, Figure 10C) proximolaterally on mural rim on one or occasionally both sides; nodule of ambiguous structure but in some cases appearing hollow, with opening directed proximomedially (arrow, Figure 10D), possibly representing either small avicularium or base of large spine or scutum. No ovicells, avicularia, or closure plates observed; ancestrula not observed. Nature of interzooidal connections unclear.

  • Remarks.—This species, with zooids having a proximal gymnocyst and a pair of distolateral spines, might be placed in Charixa, although the extensive, coherent, sheet-like colony is unusual for that genus. The proximolateral nodular structure in Incertae sedis A is in the same position as the large proximolateral spine base in Charixa sp. A (above), raising the possibility that the two species are closely related and represent an undescribed genus. The arrangement of zooids is different between the two; in Charixa sp. A, a mostly quincuncial arrangement of zooids appears early on (Figure 9A). While the ancestrula is not evident in our specimen of Incertae sedis A, the portion of the colony in the lower left of Figure 10A appears to be within the zone of astogenetic change, and there the zooids are arranged more in transverse rows than in quincuncial pattern. Clarifying the identity of Incertae sedis A will require additional, better material than the single specimen we have.

  • Figure 11.

    Incertae sedis B., specimen NMNS PA18436, SEM images of coated specimen. A, view of portion of erect colony : note bent, tubular zooids exposed at upper right; B, portion of colony surface with zooidal walls dissolved from around some zooids; C, view of colony surface showing small kenozooids (arrowheads) interspersed with autacoids; D, enlargement of autacoids, showing sloping, granulated cryptocyst. Scale bars: 1.0 mm (A, B); 0.50 mm (C); 0.20 mm (D).

    f11_239.jpg

    ? Family Chiplonkarinidae Taylor and Gordon, 2007
    Incertae sedis B
    Figure 11

  • Material examined.—NMNS PA 18436 (Loc. 1). The specimen consists of two fragments of the same colony in rock matrix. One fragment is part of a frontally abraded branch, with the walls partly dissolved; the other comprises the terminal part of a multiramous branch, the original frontal surface mostly intact but with the walls dissolved in one of the branch ends, showing the internal orientation of the zooids. SEM images were taken from the intact specimen rather than from a cast.

  • Measurements.—Frontal ZL = 0.28–0.37 mm (0.313 ±0.035 nm); Frontal ZW = 0.22–0.36 mm (0.269±0.050mm); OpL = 0.12–0.17mm (0.141 ±0.020 mm); OpW = 0.11–0.18 mm (0.125 ±0.026 mm); n = 6.

  • Description.—Colony erect, with subcylindrical, cylindrical, or compressed branches; terminal fragment of one branch (Figure 11 A) 7 mm long, 2.7 mm across, and 2 mm thick, with three rami at end; zooids completely surrounding branch. Zooids appear to be long, originating from central axis, overlapping one another for most of their length within branch, turning frontally near end (Figure 11A, upper right), with only most distal part of zooid showing frontally. Frontally exposed area irregular in outline: circular, oval, elliptical, or hexagonal. Opesia small; circular, oval, or elliptical; surrounded by sloping, granulated cryptocyst (Figure 11D). Gymnocyst lacking. Zooids interspersed with infrequent, irregularly occurring kenozooids (arrowheads, Figure 11C). No spine bases or ooecia observed. Neither early astogeny nor basal portions of colony observed.

  • Remarks.—Incertae sedis sp. A resembles species in the Cretaceous family Chiplonkarinidae Taylor and Gordon, 2007. Chiplonkarinidae includes malacostegangrade cheilostomes in which the colony is primarily erect, with long, tubular zooids forming an inner endozone and an outer exozone. Hollow spines and closure plates are lacking; the gymnocyst is reduced or lacking; and the cryptocyst is narrow and does not form a proximal shelf (Taylor and Gordon, 2007). The details of the inner and outer zones differ among the four genera (Bock, 2017) presently placed in the family. In Chiplonkarina Taylor and Badve, 1995, autacoids are oriented parallel to the long axis of the branch in the endozone, but turn 90° into the exozone, where they become perpendicular to the branch surface. In Heteroconopeum Voigt, 1983, the proximal parts of autacoids in the endozone are polygonal in cross section, stacked vertically along the center of the branch to form prismatic cylinders, and have pores in both the lateral and transverse walls between zooids; zooids bend sharply into the exozone and open on the colony surface. The endozone occupies a much larger proportion of the cross-sectional area of a colony branch in Heteroconopeum than in Chiplonkarina. In Zimmerella Taylor, 2008, the colony is erect and dendroid, and branches have a scalloped axial lumen surrounded by endozonal zooids, which are large and flask-shaped and produce exozonal zooids by frontal budding. Finally, in Basslerinella Taylor and McKinney, 2006, the colony forms bifoliate fronds rather than cylindrical branches; frontally, kenozooidal outgrowth fills in the spaces between autacoids and leaves a digitate edge surrounding the autozooidal opesia, which is extensive.

  • The autacoids in our specimen are clearly long, tubular, and turn frontally near their distal end (Figure 11A, upper right), suggesting the presence of an endozone and exozone, and indicating placement in Chiplonkarinidae. However, the frontal aspects of zooids evident in our specimen are not clearly identifiable with any of the four genera in this family. Determination of generic identity will ultimately require a cross-sectional view of a branch, and we were unwilling to risk damaging our only specimen, which in other respects is exceptionally good, to try to obtain this view. Further identification wifi require additional material.

  • Incertae sedis C
    Figures 12, 13

  • Material examined.—NMNS PA 18437 (Loc. 2). The specimen, consisting of calcified walls embedded in rock matrix, was observed and photographed through a stereomicroscope; no cast was possible. In life, one or more fully developed bryozoan colonies, and at least two young colonies, inhabited the highly concave interiors of two small Crassostrea valves that were probably fused together side by side when alive and remained fused either in situ or among shell rubble after death. In our specimen, the bryozoans occupy the outer surfaces of the interior casts left by the Crassostrea valves, with the mollusk shells having disappeared to expose the basal surfaces of the bryozoans. While many of the zooids in the light photomicrographs in Figures 12 and 13 appear to have the frontal walls exposed, these are actually the basal walls, and what appears to be the orifice (e.g. Figures 12D, E; 13D) in many zooids is actually a circular or oval, non-calcified distal portion of the basal wall. This is clearly evidenced by parts of colonies where the rock matrix has been partly or completely lost from the interiors of zooids, as is evident in Figure 13A; in a few of these zooids, the outline of the opesia (arrowheads, Figure 13A) and the shape of the interior of the zooidal frontal wall can be discerned. Of necessity, the description below is based mostly on the basal surface.

  • Measurements.—Primary axial zooids: ZL = 0.65– 0.82 mm (0.738±0.057 mm); ZW = 0.10–0.19 mm (0.152±0.022 mm); n = 13. Secondary axial zooids: ZL = 0.41–0.76 mm (0.529±0.105 mm); ZW = 0.15– 0.21 mm (0.183±0.018 mm); n = 12. Tertiary zooids: ZL = 0.33–0.50 mm (0.411±0.062 mm); ZW = 0.017– 0.028 mm (0.237±0.028 mm); n = 11. Orifice, secondary axial zooids: OpL = 0.14 mm; OpW = 0.10–0.11 mm; n = 2.

  • Description.—Colony encrusting; zooids in uniserial columns arranged in bipinnate branching pattern (Figures 12, 13), although capacity to become pluriserial exists (Figure 13D). Young colonies (Figures 12A, 13D) with branches well separated and distinct; older, larger colonies with branches irregularly and closely spaced, jumbled (Figure 12B). Zooids in primary axis of branch (Figures 12D, E; 13B, C) each giving rise distally to next axial zooid in series and distolaterally to zooid on each side, initiating paired, opposite secondary axial branches. Zooids in secondary axis show same budding pattern, producing next axial zooid distally and pair of tertiary zooids distolaterally. Tertiary zooids typically bud subsequent tertiary zooids only distally, without giving rise to distolateral daughter zooids. Zooids in primary axis long and narrow, with long cauda (Figures 12E; 13B, C); noncalcified portion of basal wall typically lacking. Zooids in secondary axis wider and shorter on average (Figures 12D, E; 13C), with cauda of variable length; non-calcified portion of basal wall sometimes present. Tertiary zooids relatively short and wide (Figures 12D, E; 13B, C), oval or spindle shaped, often lacking cauda altogether, with relatively large, oval or circular, non-calcified zone in distal part of basal wall. Frontal wall (inferred from two zooids in Figure 13A) transversely highly convex; opesia oval, longer than broad, occupying roughly half the noncaudate portion of frontal wall, apparently oriented nearly parallel to basal surface of colony. Lateral walls with pair of basal tubular, intramural pore chambers distolaterally, one to three smaller tubular chambers on each side more proximally (Figure 12D, arrowheads), and simple pore distally (Figure 12D, asterisked arrowhead). Zooids in some parts of colony may form pluriserial patches in which zooids interconnect via all pore chambers, as seen in young colony (Figure 13D, E). Basal walls of some primary and secondary axial zooids convex in transverse section (evident in Figures 12E; 13B, C). Ancestrula (Figure 13D, E) oval, budding one daughter zooid distolaterally and one proximally. Frontal zooidal morphology not directly observed. No evidence of ovicells or avicularia.

  • Remarks.—Although we initially interpreted this as possibly a branched, erect species, with some branches preserved in such a way that the frontal surfaces of zooids were visible, this is not the case. Flexible, noncalcified joints between zooids (as would be expected in a branched, erect species) are lacking, and what appeared to be opesiae proved to be non-calcified zones in the basal walls, as evidenced by parts of the colony (Figure 13A) in which the matrix has been lost from the interior of zooids. Finally, the colonies in our specimen are essentially twodimensional; no branches were preserved as tangential cross sections, as might be expected in the preservation of a three-dimensional colony. We interpret cases where zooids or branches overlap one another (Figures 12D, E; 13B) to represent intra-colony overgrowth. A puzzling aspect of preservation is that some primary and secondary axial zooids are not flat on the basal surface, but rather are convex in transverse section (e.g. Figures 12E; 13B, C), as might be expected in the preservation of weakly calcified, cylindrical, erect branches. However, some zooids with a convex cauda have lost the matrix inside the expanded portion of the zooid, confirming that the convex surface is the basal surface.

  • We saw no indications of ovicells, which should be evident even in basal view if present, and so we consider this species to be of malacostegan rather than neocheilostome grade. In growth form, it resembles the electrid species Spinicharixa dimorpha Taylor, 1986a in which long, narrow, caudate axial autozooids bud the next axial zooid distally and paired, non-caudate zooids distolaterally. The resulting colony is pluriserial, with zooids in large parts of the colony packed closely together. In Incertae sedis C, primary axial zooids are similarly long and narrow, but give rise distolaterally to similarly narrow secondary axial zooids, which in turn give rise distolaterally to noncaudate zooids that produce further non-caudate zooids distally. The resulting colony is more a jumble of closely packed uniserial branches than a pluriserial sheet. The autozooids in S. dimorpha are frontally quite different than those in Incertae sedis C. In S. dimorpha, the opesia in both axial and non-caudate zooids occupies the entire frontal surface and the gymnocyst is negligible (Taylor, 1986a: fig. 25 A), whereas in Incertae sedis C, the inferred opesia is oval in outline and occupies one-third or less of the total zooid length. In S. dimorpha, the opesia is surrounded by a narrow, granulated cryptocyst and the mural rim bears up to eight pairs of spine bases.

  • Other genera having uniserial budding and reported from the Cretaceous include Rhammatopora Lang, 1915; Herpetopora Lang, 1914: Pyripora d' Orbigny. 1849; and Pyriporopsis Pohowsky, 1973. As in axial zooids in Incertae sedis C, zooids in Rhammatopora have a long cauda and the opesia is similar in size and shape to that inferred for Incertae sedis C. In Rhammatopora the caudae are much longer and narrower relative to the expanded portion, lateral zooids are budded in a cruciate pattern, and the opesial rim bears the bases of many small spines.

  • Zooids in Herpetopora species (Taylor, 1988b) also have a narrower and often longer cauda relative to the expanded portion than in Incertae sedis C. Lateral budding sites in Herpetopora involve straight, tubular intramural pores, usually one but sometimes more than one on each side. In contrast, the distolateral pores in Incertae sedis C are intramural but are expanded within the wall, and zooids often have an additional two lateral intramural pores more proximally on each side, although no budding was observed from these lateral pores. Zooids in some Herpetopora species have a relatively small, oval opesia as in Incertae sedis C, with the cryptocyst narrow and non-granulated.

  • The distinctions between Pyripora and Pyriporopsis are not entirely clear; Taylor (1994) noted that Pyripora species have a better developed proximal gymnocyst (presumably, longer cauda and/or smaller opesia; see also Thomas and Larwood, 1960) than Pyriporopsis; the cryptocyst is narrow and granulose (pustulose), whereas that in Pyriporopsis is striated or lacking. Taylor (1987) noted the following features characteristic of Pyriporopsis but did not contrast these with the character states in Pyripora: zooids predominantly oval in crowded areas of colony, but pyriform (with caudae) in uniserial series in less crowded areas; spines lacking; calcified closure plates occur; the pore chambers are dilated intramural cavities; and the ancestrula is small, oval, budding daughter zooids distally and proximally (the pattern is different in Pyripora catemdaria; Taylor, 1986b).

  • Available evidence suggests placement in Pyriporopsis. Our specimen is similar to Pyriporopsis portlandensis, the type species of Pyriporopsis, in the branching pattern and distribution of caudate and non-caudate zooids (Pohowsky, 1973: fig. 1), and in having intramural pore chambers distolaterally, with one or two pores present more proximally on each side. While we infer the opesia to be smaller in our specimen than in P. portlandensis, this was based on only two axial zooids, and tertiary zooids could in fact have a larger opesia. Finally, the early budding pattern (Figure 13D, E) in our specimen seems more similar to that in P. portlandensis than in Pyripora catenularia, although which zooid in our specimen is the ancestrula is somewhat ambiguous. We interpret zooid “a” in Figure 13E to be the ancestrula, giving rise to one daughter zooid (arrow) distolaterally and another (asterisk) proximally. We infer the polarity of the ancestrula from the dark, non-calcified basal area, which is presumably distal as in other zooids. The distolaterally budded daughter zooid in turn appears to give rise to a distal zooid and one distolateral zooid, though these zooids are not well preserved. The zooid proximally budded from the ancestrula buds a triplet of zooids distally and distolaterally, each of which in turn buds distally, as well as distolaterally on one or both sides. Pyriporopsis portlandensis shows a similar pattern (Taylor, 1986b: fig. 6) in that the ancestrula buds from the distal and proximal ends, but not laterally. We note, however, that correct identification of the ancestrula is crucial; if the asterisked zooid in Fig. 13E is actually the ancestrula, and if the polarity is in the opposite direction (distal to the right), then the budding pattern is more like that in Pyripora catenularia than in Pyriporopsis portlandensis.

  • We refrain from assigning our specimen to a genus, even tentatively, because we were unable to observe key frontal features necessary for generic determination. These include variation in the extent of the opesia; the nature of the cryptocyst, if present; and the presence or absence of opesial spine bases, zooidal closure plates, and kenozooids (the narrowness of some the axial zooids raises the possibility that they are kenozooids).

  • Figure 12.

    Incertae sedis C, light photomicrographs of intact specimen NMNS PA18437. A, young colony in basal view, showing primary and secondary axes, but few tertiary branches. B, branches from one or more older colonies, in basal view, showing jumbled arrangement of zooids. Box indicates approximate region enlarged in panel C. C, portion of colony in basal view, showing bipinnate branching pattern. D, enlargement from panel C; p, zooids in primary axis; s, zooids in secondary axis; t, tertiary zooids; arrowheads, tubular pore chambers in lateral wall; asterisked arrowhead, distal pore; arrows, fine sutures between mother and daughter zooids. E, enlargement from panel C; p, s, t as in panel D; asterisks, zooids (seen in basal view) overgrowing parts of other zooids. Scale bars: 1.0 mm (A–C); 0.50 mm (D, E).

    f12_239.jpg

    Figure 13.

    Incertae sedis C, photomicrographs of intact specimen NMNS PA18437. A, portion of colony m basal view, with rock matrix eroded from interior of some zooids; arrowheads, outline of opesia evident in zooidal interior. B, portion of colony in basal view: arrowhead, primary axial zooid; arrow, secondary axial zooid; asterisk, tertiary zooid; x, primary or secondary axis of one branch overlapping primary axis of another branch. C, portion of branch in basal view, showing zooids in primary (p) and secondary (s) axes, and tertiary zooids (t). D, young colony in basal view, arising from presumed ancestrula (arrowhead). Box indicates region enlarged in panel E. Arrow indicates pluriserial portion of colony. E, presumed ancestrula (a) and zone of astogenetic change, seen in basal view, enlarged from boxed area in panel D but rotated clockwise 90 degrees: asterisk, zooid which might alternatively be ancestrula; arrow, zooid budded distolaterally from presumed ancestrula “a”; arrowheads, zooids budded from zooid marked with arrow. Scale bars: 0.50 mm (A, C, E); 1.0 mm (B, D).

    f13_239.jpg

    Suborder Flustrina Smitt, 1868
    Superfamily Calloporoidea Norman, 1903
    Family Calloporidae Norman, 1903
    Genus Marginaria Römer, 1840

  • Type species.—Cellepora elliptica von Hagenow, 1839.

  • Marginaria prolixa sp. nov.
    Figures 14, 15

  • Diagnosis.—Colony encrusting, unilaminar, sheet-like. Zooids in zone of astogenetic change oval or hexagonal; those in zone of repetition elongate, and rectangular or nearly so; opesia oval or elongate. Zooids closely set; proximal gymnocyst up to one-quarter length of some zooids, lateral gymnocyst negligible. Cryptocyst coarsely granulose. Interzooidal avicularia common proximodistally or laterally between zooids. Ooecium globose, prominent, lying on gymnocyst of next-distal zooid; subimmersed in older zooids. Ancestrula budding triplet of daughter zooids distally; subsequent periancestrular zooids include large proximolateral pair, with smaller presumed kenozooid between them. Single or paired distal and one or two pairs of distolateral buttressed recesses leading to multiporous septula. Mural spines and closure plates lacking.

  • Etymology.— The specific name is an adjective from the Latin prolixus (long, drawn out), referring to the elongate zooids.

  • Material examined.—Seven specimens from Locs. 3 and 4. Holotype: NMNS PA18438 (Loc. 3). Paratypes: NMNS PA18439-18441 (Loc. 3). See Table 1.

  • Measurements.—See Table 3.

  • Description.—Colony (Figure 14A, B) encrusting, unilaminar, sheet-like. Zooids arranged in quincunx (Figure 14E, F) or somewhat irregularly (upper right, Figure 14D); zooids small and irregularly hexagonal or oval in zone of astogenetic change (Figures 14A; 15B, D), but longer in zone of astogenetic change (Figure 14D–F); also compare ZL measurements between NMNS PA 18440 and NMNS PA18438 (Table 3). Ovicelled zooids long-oval or rectangular (Figure 14E, F), delineated laterally by narrow groove. Opesia occupying most of zooid length in young zooids, roughly two-thirds in ovicelled zooids. Opesial rim raised, rounded, coarsely and densely granulose; sloping cryptocyst lacking, except as interior side of opesial rim. Mural spine bases not observed. Interzooidal avicularia common, forming at zooidal margin (Figure 15B) distal or distolateral to autozooids; abundant in interzooidal grooves in zone of astogenetic repetition (Figures 14C, D; 15A); sometimes less abundant in zone of astogenetic change (Figures 14A, B; 15D); longer than broad, with short, smooth gymnocystal area proximally and coarsely granulose rostrum (Figure 15C); no hinge structures observed. Some avicularia have elongate opesial opening, truncate at one end, tapering toward other, with narrow end directed proximally (e.g. Figure 14F); others have irregular, circular, or oval opening. Among ovicelled zooids, avicularia often lateral to ovicell (Figure 14E, F). Ovicell (Figure 14E, F) slightly wider than long, nearly as wide as autozooids, lying on proximal gymnocyst of zooid distal to maternal zooid; initially prominent (Figure 14E) but partly immersed with increased calcification (Figure 14F). Form of interzooidal connections ambiguous due to poor preservation or casting limitations; zooids have pair of small, distal buttressed recesses (arrowheads, Figure 14D) and one or two pairs of distolateral buttressed recesses (Figures 14D, 15A) that appear to lead to multiporous septula; autozooids interconnect with interzooidal avicularia as well as neighboring autozooids. Ancestrula (Figure 15B, D) oval or rectangular, surrounded by a triplet of daughter zooids distally, a presumed kenozooidal chamber proximally, and a pair of larger periancestrular zooids proximolaterally.

  • Remarks.—Most of the approximately 15 known species of Marginaria (Bock, 2017) were described from the Late Cretaceous, although two have been reported from the Paleogene (Berthelsen, 1962; Guha and Gopikrishna, 2007). Species in Marginaria characteristically have numerous small interzooidal avicularia scattered among autozooids; these avicularia are budded at the colony margin, along with developing autozooids (Taylor and McKinney, 2006), and commonly lack calcified hingesupport structures, leading some authors (e.g. Guha and Gopikrishna, 2007) to refer to them as kenozooids rather than avicularia. However, they are distributed as one would expect for avicularia. These putative avicularia appear to lack skeletal hinge support structures in various species of Marginaria, but whatever their function, they constitute a shared character for the genus.

  • The genus Reptoflustrella d'Orbigny, 1853 is similar to Marginaria but supposedly differs from the latter in having the interzooidal avicularia in a stereotyped position proximolateral to most autozooids; in addition, the generic description of Reptoflustrella includes zooids having at least two pairs of distal spine bases and the proximal gymnocyst comprising a quarter to two-thirds the zooidal length (Gordon and Taylor, 2005). The distinctions between the genera are somewhat unclear, as some of the avicularia in R. cenomana d'Orbigny, 1853, the type species of Reptoflustrella, are arguably not in the proximolateral position (Gordon and Taylor, 2005: fig. 1D), and some species in Marginaria have spines and an extensive proximal gymnocyst, as in Reptoflustrella. Voigt (1989) included R. cenomana in Marginaria in a review of the latter genus, thus reducing Reptoflustrella to a junior synonym of Marginaria. In our holotype specimen of M. prolixa, the interzooidal avicularia are commonly in the proximolateral position in the vicinity of ovicelled zooids (Figure 14E, F), but in non-reproducing parts of the colony, they are often positioned proximodistally between successive autozooids (Figure 14D). Furthermore, zooids in M. prolixa lack spines, as is the case in about half the species in Marginaria. While Gordon and Taylor (2005) believed that it was premature to include Reptoflustrella in Marginaria, our species appears in any case to fit better in Marginaria.

  • Most species in Marginaria have zooids less than 0.40 mm long, typically with an oval or elliptical opesia, and with gymnocyst evident both proximally and laterally. Another species with larger zooids is M. caminoides (Voigt, 1967) (ZL × ZW = 0.60 × 0.45 mm), which, although encrusting, differs from M. prolixa in forming narrowly pluriserial branches; zooids are short-oval or hexagonal in outline; the opesia is oval to elliptical; the interzooidal avicularia are large; and zooids have mural spines.

  • Figure 14.

    Marginaria prolixa sp. nov., SEM images of silicone casts from colony molds. A, paratype NMNS PA18439, young colony; B, paratype NMNS PA18441, colony, showing oval autozooids in zone of astogenetic change (left) and more-elongate autozooids in zone of astogenetic repetition (right); C, NMNS PA18440, mixed oval and elongate autozooids, with scattered interzooidal avicularia; D–F, holotype, NMNS PA18438; D, autozooids and interzooidal avicularia; arrowheads, distal buttressed recesses; E, ovicelled zooids; F, ovicelled zooids in older, more heavily calcified portion of colony, showing partly immersed ooecia and interzooidal avicularia. Scale bars: 1.0 mm (A, B); 0.50 mm (C–E); 0.20 mm (F).

    f14_239.jpg

    Figure 15.

    Marginaria prolixa sp. nov., SEM images of silicone casts from colony molds; A, C, D, paratype NMNS PA18441; B, paratype NMNS PA 18439; A, autozooids, showing interzooidal connections; distal direction toward lower right; arrow, interzooidal avicularium enlarged in panel C; B, paratype NMNS PA18441, young colony, with arrowheads indicating avicularia forming at or near colony margin; asterisk, presumed ancestrula; arrow, presumed kenozooidal chamber budded proximally from ancestrula; C, enlargement of interzooidal avicularium indicated by arrow in panel A; D, ancestrula (a) and periancestrular zooids enlarged from colony in Figure 14B; arrow, presumed kenozooidal chamber budded proximally from ancestrula, lying between paired proximolateral zooids; arrowhead, another kenozooidal chamber early in astogeny. Scale bars: 0.50 mm (A, B, D); 0.10 mm (C).

    f15_239.jpg

    Table 3.

    Measurements (in millimeters) for Marginaria prolixa sp. nov. For each set of values, the top row is the range and the bottom row the mean and standard deviation.

    t03_239.gif

    Table 4.

    Cheilostome bryozoan species detected in the Upper Cretaceous Himenoura Group, Shimokoshikijima Island, Japan, with the number of specimens from each locality.

    t04_239.gif

    Discussion

    We detected six cheilostome species but no cyclostomes. Among the cheilostomes, five (83%) were of malacostegan-anascan grade, and one (Marginaria prolixa) was a neocheilostome anascan. Kenocharixa kashimaensis was the commonest species overall, occurring at three of the four sites and abundant at Loc. 3 (Table 4). Marginaria prolixa was moderately abundant at Loc. 3 and also occurred at Loc. 4. The other four species were detected as one colony each, and were not well enough preserved to identify to species (Charixa sp. A) or genus (Incertae sedis A, B, C). Locs. 1 and 3 showed equivalent diversity, with three species each, with the other localities having one or two species.

    In a tabulation of Late Cretaceous (Campanian—Maastrichtian) regional diversity in the southeastern USA, Taylor and McKinney (2006) reported 130 bryozoan species representing 77 genera, including 34 (26%) cyclostomes, 11 (8%) malacostegan cheilostomes, 44 (34%) anascan-grade neocheilostomes, 27 (21%) cribrimorphgrade neocheilostomes, and 14 (11%) ascophoran-grade neocheilostomes, noting that extensive collections remain to be studied and will certainly add to the known diversity. In the southeastern USA, then, cyclostomes comprise about one-quarter of the total diversity, and among 96 cheilostomes, species of the more primitive (sensu Taylor, 1988a) malacostegan grade occupy only 11%, with neocheilostomes comprising 89%. Though Taylor and McKinney (2006) did not report local diversities, McKinney and Taylor (2016) tabulated a diversity of six cyclostome (26%) and 17 cheilostome (74%) species from the Ripley Formation (Maastrichtian) at Coon Creek, Tennessee, within the area of the Taylor and McKinney (2006) study; among the 17 cheilostomes were four malacostegans (23%) and 13 (77%) neocheilostomes, including seven anascans (41%), three cribrimorphs (18%), and three ascophorans (18%). The local sample roughly mirrored the regional sample, with about one-quarter cyclostomes and a low proportion of malacostegans compared to neocheilostomes.

    Compared to the Campanian—Maastrichtian fauna in the southeastern USA, the lower to middle Campanian fauna detected on Shimokoshikijima was depauperate, in both species diversity (six species) and morphological range, or disparity (no cyclostomes; five (83%) malacostegan cheilostomes; one anascan-grade (17%) neocheilostome; no cribrimorphs or ascophorans). The differences in diversity between our sample and the regional and local samples from the southeastern USA mentioned above seem too extreme to be attributed to the low sample size in our study. Other surveys of nearshore, bivalve-encrusting Cretaceous faunas in Japan have been similarly depauperate: one malacostegan species of early to middle Cenomanian age from the Yezo Group in northern Japan (Ostrovsky et al., 2006), and four malacostegan and two anascan-grade neocheilostome species of Albian to early Cenomanian age from the Goshoura Group, Kyushu, Japan. In these studies, as in ours, the bryozoans were rather poorly preserved, occurring primarily as basal colony surfaces or colony molds detached from the substrate; only rarely have specimens been found with the calcified frontal surface exposed.

    From their analyses of carbonate platform biota along the NW Pacific margin, Iba and Sano (2007) concluded that the biota in this region belonged to the Tethyan biotic realm in the interval from the Middle Jurassic to early Albian, but became isolated from the latter between the latest Aptian and middle Albian as the NW Pacific became separate from the Tethyan realm. Molluscan genera subsequently began to evolve new species, leading to establishment of the North Pacific biotic province. We offer the hypothesis that the low-diversity, low-disparity bryozoan assemblages in Japan detected in the upper Albian—lower Cenomanian Goshoura Group (Dick et al., 2013) and in the lower to middle Campanian Himenoura Group (this study) may represent a relict fauna—that is, the descendants of lineages present in the North Pacific at the time this region became isolated from the Tethys. Within these relict lineages, relatively little innovation occurred, in contrast to the western Tethys, where morphological innovation led to diverse faunas that included cribrimorphs and ascophorans. This would explain the failure to date to detect cribrimorph or ascophoran cheilostomes in Cretaceous deposits in Japan.

    The fossil record lends some support to this hypothesis. The oldest cheilostome ovicells are known in the genera Wilbertopora and Marginaria from the late Albian (Ostrovsky and Taylor, 2004), and hence Marginaria, which we detected on Shimokoshikijima, could have been among the lineages retained in the NW Pacific after isolation from the Tethys, assuming a slightly earlier origin of ovicells than has been detected to date. Similarly, Charixa is known from the Hauterivian to late Albian (Early Cretaceous) (Ostrovsky et al., 2008) in the western Tethys, and could have been among the lineages retained in the NW Pacific. Finally, the earliest records available for species in the malacostegan family Chiplonkarinidae, to which we tentatively attribute Incertae sedis B, are for Chiplonkarina bretoni Taylor and Badve, 1995, from the early Cenomanian of France and Germany. However, publication is pending for a new genus and species of late Albian age in this family (Paul Taylor, personal communication), which again does not greatly postdate a presumed early to middle Albian separation of the regions. In contrast, the earliest cribrimorphs did not appear until the early Cenomanian (Larwood, 1985), and the earliest species inferred to have an ascus appeared in the Coniacian (Gordon, 2000). The origins of these novelties in Western-Tethys species thus clearly postdated the presumed isolation of malacostegan and anascan-grade neocheilostome lineages in the NW Pacific in the latest Aptian to middle Albian interval.

    The isolation hypothesis to explain low Late Cretaceous cheilostome diversity and disparity in the NW Pacific can be tested with further sampling. Discovery of a Late Cretaceous bryozoan assemblage in eastern Asia containing cribrimorphs and ascophorans, for example, would negate the hypothesis, to the extent that the high-diversity deposit did not reflect the reestablishment of exchange between the NW Pacific and the Tethys. Exchange was reestablished at some point, although when this occurred is not clear; Iba and Sano (2007) noted that the carbonate platform biota became reestablished in the NW Pacific in the Eocene, which would imply reconnection with the Tethys. If further sampling continues to find low Late Cretaceous cheilostome diversity and disparity in the NW Pacific, with a dramatic increase in the Early Paleogene, this would support the isolation hypothesis.

    Author contributions

    TK and CS initiated the study. All authors contributed to fieldwork, though CS and TK conducted most of it. CS made all silicone casts, prepared specimens for SEM, took all SEM images, and preliminarily identified specimens. MHD took light microscopic images of one specimen and made most of the measurements presented. MHD was responsible for taxonomy and wrote most of the manuscript; TK wrote the sections on geological setting. TK prepared Figures 1-6 and MHD prepared Figures 715.

    Acknowledgments

    We thank Yuka Miyake (Kumamoto University) for assistance in the field; the Kashima Town government for logistical support; and Dennis Gordon and Paul Taylor for substantial peer reviews. This study was funded in part by a Grant-in-Aid for Scientific Research (KAKENHI) to T. Komatsu (16K05593) from the Japan Society for the Promotion of Science.

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    © by the Palaeontological Society of Japan
    Matthew H. Dick, Chika Sakamoto, and Toshifumi Komatsu "Cheilostome Bryozoa from the Upper Cretaceous Himenoura Group, Kyushu, Japan," Paleontological Research 22(3), 239-264, (1 July 2018). https://doi.org/10.2517/2017PR022
    Received: 7 September 2017; Accepted: 9 November 2017; Published: 1 July 2018
    KEYWORDS
    Bryozoa
    cheilostome diversity
    Cretaceous
    isolation
    morphological grade
    Tethys
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